Skip to main content

Face-to-face configuration in Japanese macaques functions as a platform to establish mutual engagement in social play

Abstract

A face-to-face configuration and eye-to-eye contact are considered a basis for intersubjectivity, as they create a situation in which interactants are mutually attentive. Studies in humans have shown that the face-to-face configuration establishes active engagement by interactants in subsequent interactions, but it is not clear whether a similar function exists in non-human animals. Using data from a group of Japanese macaques (Macaca fuscata), this study compared dyadic play fighting sessions preceded and not preceded by a face-to-face configuration. During play fighting, players compete to gain an advantage over their playmates by attacking them unilaterally (i.e., attacking them without being attacked or pinning them to the ground). Defining the inter-player asymmetry of active engagement in play in terms of the difference in the duration of each individual’s advantage over the other, we found that asymmetry was lower in play bouts with a face-to-face beginning than in play bouts without one. Additionally, in play bouts not preceded by a face-to-face configuration, individuals who faced their partner at the onset of play unilaterally attacked their partner for a significantly longer duration than did those who did not face their partner at the onset of play. Conversely, in play bouts preceded by a face-to-face configuration, there was no difference in the duration of unilateral attacks. Overall, our results indicated that the face-to-face configuration in Japanese macaques functions as a platform to establish mutual engagement by interactors and enhances symmetry within play interaction.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  • Aldis O (1975) Play fighting. Academic Press, New York

    Google Scholar 

  • Altmann SA (1962) Social behavior of anthropoid primates: Analysis of recent concepts. In: Bliss EL (ed) Roots of behavior. Harper, New York, pp 277–285

    Google Scholar 

  • Argyle M, Dean J (1965) Eye-contact, distance and affiliation. Sociometry 28(3):289–304

    CAS  PubMed  Article  Google Scholar 

  • Bard KA, Leavens DA (2009) Socio-emotional factors in the development of joint attention in human and ape infants. In: Röska-Hardy L, Neumann-Held EM (eds) Learning from animals? Examining the nature of human uniqueness. Psychology Press, London, pp 89–104

    Google Scholar 

  • Bard KA, Myowa-Yamakoshi M, Tomonaga M, Tanaka M, Costall A, Matsuzawa T (2005) Group differences in the mutual gaze of chimpanzees (Pan troglodytes). Dev Psychol 41(4):616–624

    PubMed  Article  Google Scholar 

  • Bauer EB, Smuts BB (2007) Cooperation and competition during dyadic play in domestic dogs Canis familiaris. Anim Behav 73(3):489–499

    Article  Google Scholar 

  • Bavelas JB, Coates L, Johnson T (2002) Listener responses as a collaborative process: The role of gaze. J Commun 52(3):566–580

    Article  Google Scholar 

  • Bekoff M (1974) Social play and play-soliciting by infant canids. Am Zool 14(1):323–340

    Article  Google Scholar 

  • Beltrán Francés V, Castellano-Navarro A, Illa Maulany R, Ngakan PO, MacIntosh AJJ, Llorente M, Amici F (2020) Play behavior in immature moor macaques (Macaca maura) and Japanese macaques (Macaca fuscata). Am J Primatol 82(10):e23192

    PubMed  Article  Google Scholar 

  • Biben M (1986) Individual-and sex-related strategies of wrestling play in captive squirrel monkeys. Ethology 71(3):229–241

    Article  Google Scholar 

  • Brinck I (2008) The role of intersubjectivity in the development of intentional communication. In: Zlatev J, Racine TP, Sinha C, Itkonen E (eds) The shared mind: perspectives on intersubjectivity. John Benjamins, Amsterdam, pp 115–140

    Chapter  Google Scholar 

  • Brownell CA (2011) Early developments in joint action. Rev Philos Psychol 2(2):193–211

    PubMed  PubMed Central  Article  Google Scholar 

  • Burghardt GM (2005) The genesis of animal play: testing the limits. MIT Press, Cambridge

    Google Scholar 

  • Cary MS (1978) The role of gaze in the initiation of conversation. Soc Psychol (Gott) 41(3):269–271

    Article  Google Scholar 

  • Chance MRA (1967) Attention structure as the basis of primate rank orders. Man 2(4):503–518

    Article  Google Scholar 

  • Chapais B (1988) Experimental matrilineal inheritance of rank in female Japanese macaques. Anim Behav 36(4):1025–1037

    Article  Google Scholar 

  • Chevalier-Skolnikoff S (1974) Male-female, female-female, and male-male sexual behavior in the stumptail monkey, with special attention to the female orgasm. Arch Sex Behav 3:95–116

    CAS  PubMed  Article  Google Scholar 

  • Coss RG (1978) Perceptual determinants of gaze aversion by the lesser mouse lemur (Microcebus murinus), the role of two facing eyes. Behaviour 64(3–4):248–269

    Article  Google Scholar 

  • Davila-Ross M, Allcock B, Thomas C, Bard KA (2011) Aping expressions? Chimpanzees produce distinct laugh types when responding to laughter of others. Emotion 11(5):1013–1020

    PubMed  Article  Google Scholar 

  • de Waal FBM, van Roosmalen A (1979) Reconciliation and consolation among chimpanzees. Behav Ecol Sociobiol 5:55–66

    Article  Google Scholar 

  • de Waal FB, Yoshihara D (1983) Reconciliation and redirected affection in rhesus monkeys. Behaviour 1983:224–241

    Article  Google Scholar 

  • Dettmer AM, Kaburu SS, Simpson EA, Paukner A, Sclafani V, Byers KL, Murphy AM, Miller M, Marquez N, Miller GM, Suomi SJ, Ferrari PF (2016) Neonatal face-to-face interactions promote later social behaviour in infant rhesus monkeys. Nat Commun 7:11940

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Eaton GG, Johnson DF, Glick BB, Worlein JM (1986) Japanese macaques (Macaca fuscata) social development: sex differences in juvenile behavior. Primates 27(2):141–150

    Article  Google Scholar 

  • Emery NJ (2000) The eyes have it: the neuroethology, function and evolution of social gaze. Neurosci Biobehav Rev 24(6):581–604

    CAS  PubMed  Article  Google Scholar 

  • Essler JL, Cafazzo S, Marshall-Pescini S, Virányi Z, Kotrschal K, Range F (2016) Play behavior in wolves: Using the “50:50” rule to test for egalitarian play styles. PLoS ONE 11(5):e0154150

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Exline RV (1963) Explorations in the process of person perception: Visual interaction in relation to competition, sex and the need for affiliation. J Pers 31(1):1–20

    Article  Google Scholar 

  • Exline RV, Winters LC (1965) Affective relations and mutual glances in dyads. In: Tomkins S, Izzard C (eds) Affect, cognition and personality. Springer, New York, pp 319–350

    Google Scholar 

  • Exline R, Gray D, Schuette D (1965) Visual behavior in a dyad as affected by interview content and sex of respondent. J Pers Soc Psychol 1(3):201–209

    CAS  PubMed  Article  Google Scholar 

  • Exline RV, Thibaut J, Brannan C, Gumpert P (1970) Visual interaction in relation to Machiavellianism and an unethical act. In: Christie R, Geis FL (eds) Studies in Machiavellianism. Academic Press, New York, pp 53–76

    Chapter  Google Scholar 

  • Ferrari PF, Paukner A, Ionica C, Suomi SJ (2009) Reciprocal face-to-face communication between rhesus macaque mothers and their newborn infants. Curr Biol 19(20):1768–1772

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Fogel A, Messinger DS, Dickson KL, Hsu HC (1999) Posture and gaze in early mother-infant communication: Synchronization of developmental trajectories. Dev Sci 2(3):325–332

    Article  Google Scholar 

  • Friard O, Gamba M (2016) BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evol 7(11):1325–1330

    Article  Google Scholar 

  • Fröhlich M, Wittig RM, Pika S (2016) Play-solicitation gestures in chimpanzees in the wild: flexible adjustment to social circumstances and individual matrices. R Soc Open Sci 3(8):160278

    PubMed  PubMed Central  Article  Google Scholar 

  • Glick BB, Eaton GG, Johnson DF, Worlein JM (1986) Development of partner preferences in Japanese macaques (Macaca fuscata): effects of gender and kinship during the second year of life. Int J Primatol 7(5):467–479

    Article  Google Scholar 

  • Goffman E (1967) Interaction ritual: essays on face-to-face interaction. Doubleday, Garden City

    Google Scholar 

  • Gómez JC (1994) Mutual awareness in primate communication: A Gricean approach. In: Parker ST, Mietchell RW, Boccia ML (eds) Self-awareness in animals and humans. Cambridge University Press, Cambridge, pp 61–80

    Chapter  Google Scholar 

  • Gómez JC (1996) Ostensive behavior in great apes: the role of eye contact. In: Russon AE, Bard KA, Parker ST (eds) Reaching into thought: the minds of the great apes. Cambridge University Press, Cambridge, pp 131–151

    Google Scholar 

  • Gómez JC (2010) The emergence of eye contact as an intersubjective signal in an infant gorilla: implications for models of early social cognition. Acción Psicológica 7(2):35–43

    Article  Google Scholar 

  • Harrod EG, Coe CL, Niedenthal PM (2020) Social structure predicts eye contact tolerance in nonhuman primates: evidence from a crowd-sourcing approach. Sci Rep 10:6971

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Heesen R, Genty E, Rossano F, Zuberbühler K, Bangerter A (2017) Social play as joint action: a framework to study the evolution of shared intentionality as an interactional achievement. Learn Behav 45(4):390–405

    PubMed  Article  Google Scholar 

  • Held SD, Špinka M (2011) Animal play and animal welfare. Anim Behav 81(5):891–899

    Article  Google Scholar 

  • Henrich J, Heine SJ, Norenzayan A (2010) The weirdest people in the world? Behav Brain Sci 33(2–3):61–83

    PubMed  Article  Google Scholar 

  • Himmler BT, Pellis VC, Pellis SM (2013) Peering into the dynamics of social interactions: measuring play fighting in rats. J Vis Exp 71:e4288

    Google Scholar 

  • Hsu HC, Fogel A (2001) Infant vocal development in a dynamic mother–infant communication system. Infancy 2(1):87–109

    PubMed  Article  Google Scholar 

  • Huffman MA (1987) Consort intrusion and female mate choice in Japanese macaques (Macaca fuscata). Ethology 75(3):221–234

    Article  Google Scholar 

  • Iki S, Hasegawa T (2020) Face-to-face opening phase in Japanese macaques’ social play enhances and sustains participants’ engagement in subsequent play interaction. Anim Cogn 23(1):149–158

    PubMed  Article  Google Scholar 

  • Ioannou S, Gallese V, Merla A (2014) Thermal infrared imaging in psychophysiology: Potentialities and limits. Psychophysiology 51(10):951–963

    PubMed  PubMed Central  Article  Google Scholar 

  • Kano T (1980) Social behavior of wild pygmy chimpanzees (Pan paniscus) of Wamba: a preliminary report. J Hum Evol 9:243–260

    Article  Google Scholar 

  • Kano F, Hirata S, Call J (2015) Social attention in Pan: bonobos exhibit more eye contacts than chimpanzees. PLoS ONE 10:e0129684

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Kendon A (1990) Conducting interaction: patterns of behavior in focused encounters. Cambridge University Press, Cambridge

    Google Scholar 

  • Kitamura K (1989) Genito-Genital contacts in the pygmy chimpanzee. Afr Study Monogr 10(2):49–67

    Google Scholar 

  • Kleinke C (1986) Gaze and eye contact: a research review. Psychol Bull 100(1):78–100

    CAS  PubMed  Article  Google Scholar 

  • Kleinke CL, Staneski RA, Berger DE (1975) Evaluation of an interviewer as a function of interviewer gaze, reinforcement of subject gaze, and interviewer attractiveness. J Pers Soc Psychol 31(1):115–122

    CAS  PubMed  Article  Google Scholar 

  • Kobayashi H, Koshima S (2001) Unique morphology of the human eye and its adaptive meaning: comparative studies on external morphology of the primate eye. J Hum Evol 40(5):419–435

    CAS  PubMed  Article  Google Scholar 

  • Kottferová J, Skurková L, Mesarčová L, Lešková L, Demeová A, Jakuba T (2020) Friendship or competition? Symmetry in social play within the two packs of German Shepherd puppies. Animals 10(9):1627

    PubMed Central  Article  Google Scholar 

  • Laidlaw KEW, Rothwell A, Kingstone A (2016) Camouflaged attention: covert attention is critical to social communication in natural settings. Evol Hum Behav 37(6):449–455

    Article  Google Scholar 

  • Langton SRH, Watt RJ, Bruce V (2000) Do the eyes have it? Cues to the direction of social attention. Trends Cogn Sci 4(2):50–59

    CAS  PubMed  Article  Google Scholar 

  • Linnankoski I, Grönroos M, Pertovaara A (1993) Eye contact as a trigger of male sexual arousal in stump-tailed macaques (Macaca arctoides). Folia Primatol 60(3):181–184

    CAS  Article  Google Scholar 

  • Llamazares-Martín C, Scopa C, Guillén-Salazar F, Palagi E (2017) Relaxed open mouth reciprocity favours playful contacts in South American sea lions (Otaria flavescens). Behav Processes 140:87–95

    PubMed  Article  Google Scholar 

  • Lorenz K (1966) On aggression (trans: Latzke M). Methuen, London

    Google Scholar 

  • Mancini G, Ferrari PF, Palagi E (2013) In play we trust. Rapid facial mimicry predicts the duration of playful interactions in geladas. PLoS One 8(6):e666481

    Article  CAS  Google Scholar 

  • Martin P, Bateson P (2007) Measuring behavior: an introductory guide. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Mendl M, Burman O, Parker RMA, Paul ES (2009) Cognitive bias as an indicator of animal emotion and welfare: emerging evidence and underlying mechanisms. Appl Anim Behav Sci 118(3–4):161–181

    Article  Google Scholar 

  • Mondada L (2009) Emergent focused interactions in public places: A systematic analysis of the multimodal achievement of a common interactional space. J Pragmat 41(10):1977–1997

    Article  Google Scholar 

  • Palagi E (2008) Sharing the motivation to play: the use of signals in adult bonobos. Anim Behav 75(3):887–896

    Article  Google Scholar 

  • 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(1):11–21

    PubMed  Article  Google Scholar 

  • Palagi E, Antonacci D, Cordoni G (2007) Fine-tuning of social play in juvenile lowland gorillas (Gorilla gorilla gorilla). Dev Psychobiol 49(4):433–445

    PubMed  Article  Google Scholar 

  • Palagi E, Nicotra V, Cordoni G (2015) Rapid mimicry and emotional contagion in domestic dogs. R Soc Open Sci 2(12):150505

    PubMed  PubMed Central  Article  Google Scholar 

  • Palagi E, Burghardt GM, Smuts B, Cordoni G, Dall’Olio S, Fouts HN, Řeháková-Petrů M, Siviy SM, Pellis SM, (2016) Rough-and-tumble play as a window on animal communication. Biol Rev 91(2):311–327

    PubMed  Article  Google Scholar 

  • Palagi E, Marchi E, Cavicchio P, Bandoli F (2019) Sharing playful mood: rapid facial mimicry in Suricata suricatta. Anim Cogn 22:719–732

    PubMed  Article  Google Scholar 

  • Paul ES, Harding EJ, Mendl M (2005) Measuring emotional processes in animals: the utility of a cognitive approach. Neurosci Biobehav Rev 29(3):469–491

    PubMed  Article  Google Scholar 

  • Pellis SM, Pellis VC (1987) Play-fighting differs from serious fighting in both target of attack and tactics of fighting in the laboratory rat Rattus norvegicus. Aggress Behav 13(4):227–242

    Article  Google Scholar 

  • Pellis SM, Pellis VC (1997) Targets, tactics, and the open mouth face during play fighting in three species of primates. Aggress Behav 23(1):41–57

    Article  Google Scholar 

  • Perrett DI, Mistlin AJ (1990) Perception of facial characteristics by monkeys. In: Stebbins WC, Berkley MA (eds) Comparative perception: complex signals, vol 2. Wiley, New York, pp 187–215

    Google Scholar 

  • Phillips MJ, Mason WA (1976) Comparative studies of social behavior in Callicebus and Saimiri: Social looking in male-female pairs. Bull Psychon Soc 7(1):55–56

    Article  Google Scholar 

  • Pillet-Shore D (2018) How to begin. Res Lang Soc Interac 51(3):213–231

    Article  Google Scholar 

  • R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

    Google Scholar 

  • Redican WK (1975) Facial expressions in nonhuman primates. In: Rosenblum LA (ed) Primate behavior: developments in field and laboratory research, vol 4. Academic Press, New York, pp 103–194

    Chapter  Google Scholar 

  • Reinhart CJ, Pellis VC, Thierry B, Gauthier CA, 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 23(2):166–200

    Google Scholar 

  • Rijksen HD (1978) A field study on Sumatran orang utans (Pongo pygmaeus abelii Lesson 1827): Ecology, behaviour and conservation. Wageningen, H. Veenman Zonen BV

  • Rossano F (2013) Gaze in conversation. In: Sidnell J, Stivers T (eds) The handbook of conversation analysis. Wiley-Blackwell, Malden, pp 308–329

    Google Scholar 

  • Rothbart MK (1973) Laughter in young children. Psychol Bull 80(3):247–256

    CAS  PubMed  Article  Google Scholar 

  • Saito Y, Yuki S, Seki Y et al (2016) Cognitive bias in rats evoked by ultrasonic vocalizations suggests emotional contagion. Behav Processes 132:5–11

    PubMed  Article  Google Scholar 

  • Sansavini A, Zavagli V, Guarini A, Savini S, Alessandroni R, Faldella G (2015) Dyadic co-regulation, affective intensity and infant’s development at 12 months: A comparison among extremely preterm and full-term dyads. Infant Behav Dev 40:29–40

    PubMed  Article  Google Scholar 

  • Savage S, Bakeman R (1978) Sexual morphology and behavior in Pan paniscus. In: Chivers R, Herbert J (eds) Recent advances in primatology. Academic Press, New York, pp 613–616

    Google Scholar 

  • 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(2):153–161

    PubMed  Article  Google Scholar 

  • 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(6–7):795–818

    Article  Google Scholar 

  • Stawarska B (2010) Mutual Gaze and Intersubjectivity. In: Gallagher S, Schmicking D (eds) Handbook of Phenomenology and Cognitive Science. Springer, New York, pp 269–282

    Chapter  Google Scholar 

  • Stern DN (1985) The interpersonal world of the infant: a view from psychoanalysis and developmental psychology. Basic Books, New York

    Google Scholar 

  • Susswein N, Racine TP (2008) Sharing mental states: causal and definitional issues in intersubjectivity. In: Zlatev J, Racine TP, Sinha C, Itkonen E (eds) The shared mind: perspectives on intersubjectivity. John Benjamins, Amsterdam, pp 141–162

    Chapter  Google Scholar 

  • Thierry B (2000) Covariation of conflict management patterns across macaque species. In: Aureli F, De Waal FBM (eds) Natural conflict resolution. University of California Press, Berkeley, pp 106–128

    Google Scholar 

  • Thomsen CE (1974) Eye contact by non-human primates toward a human observer. Anim Behav 22(1):144–149

    Article  Google Scholar 

  • Tomasello M (2008) Origins of human communication. MIT Press, Cambridge

    Book  Google Scholar 

  • Tomonaga M, Tanaka M, Matsuzawa T, Myowa-Yamakoshi M, Kosugi Y, Mizuno Y, Okamoto S, Yamaguchi M, Bard K (2004) Development of social cognition in infant chimpanzees (Pan troglodytes): Face recognition, smiling, gaze, and the lack of triadic relations. Jpn Psychol Res 46:227–235

    Article  Google Scholar 

  • Trevarthen C, Aitken KJ (2001) Infant intersubjectivity: Research, theory, and clinical applications. J Child Psychol Psychiatry 42(1):3–48

    CAS  PubMed  Article  Google Scholar 

  • van Hooff JARAM (1967) The facial displays of the catarrhine monkeys and apes. In: Morris D (ed) Primate ethology. Aldine, Chicago, pp 7–68

    Google Scholar 

  • Verderane MP, Aguiar RM, Izar P (2020) Face–to–face interactions between mothers and female infants in wild bearded capuchin monkeys (Sapajus libidinosus). Dev Psychobiol 62(7):941–949

    PubMed  Article  Google Scholar 

  • Wada K, Ichiki Y (1980) Seasonal home range use by Japanese monkeys in the snowy Shiga Heights. Primates 21(4):468–483

    Article  Google Scholar 

  • Ward C, Bauer EB, Smuts BB (2008) Partner preferences and asymmetries in social play among domestic dog, Canis lupus familiaris, littermates. Anim Behav 76(4):1187–1199

    Article  Google Scholar 

  • Watson KK, Li D, Brent LJN, Horvath JE, GonzalezMartinez J, Ruíz-Lambides AV, Robinson AG, Skene JHP, Platt ML (2015) Genetic influences on social attention in free-ranging rhesus macaques. Anim Behav 103:267–275

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Wright KR, Mayhew JA, Sheeran LK, Funkhouser JA, Wagner RS, Sun LX, Li JH (2018) Playing it cool: characterizing social play, bout termination, and candidate play signals of juvenile and infant Tibetan macaques (Macaca thibetana). Zool Res 39(4):272–283

    PubMed  PubMed Central  Article  Google Scholar 

  • Yamagiwa J (1992) Functional analysis of social staring behavior in an all-male group of mountain gorillas. Primates 33(4):523–544

    Article  Google Scholar 

Download references

Funding

This study was supported by a Grant-in-Aid for Scientific Research on Innovative Areas No. 30172894 (“The Evolutionary Origin and Neural Basis of the Empathetic Systems”) to the second author.

Author information

Authors and Affiliations

Authors

Contributions

The first and second authors conceived and designed the study. The first author gathered the data, performed the statistical analyses, and wrote the article.

Corresponding author

Correspondence to Sakumi Iki.

Ethics declarations

Conflicts of interest

The authors declare no conflicts of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. We conducted this study following the guidelines of the Animal Experiment Committee of the University of Tokyo. This study was approved by the Animal Experiment Committee of the University of Tokyo (Permission number 28–3).

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Iki, S., Hasegawa, T. Face-to-face configuration in Japanese macaques functions as a platform to establish mutual engagement in social play. Anim Cogn 24, 1179–1189 (2021). https://doi.org/10.1007/s10071-021-01508-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-021-01508-1

Keywords

  • Social cognition
  • Rough-and-tumble play
  • Communication
  • Play fighting
  • Intersubjectivity
  • Macaca fuscata