GibbonFACS: A Muscle-Based Facial Movement Coding System for Hylobatids

Abstract

The evolution and function of human and nonhuman primate facial expression can be better understood through multispecies comparative analyses. Anatomically based coding systems (Facial Action Coding Systems [FACS]) are developed to enable such analyses because they are standardized and systematic and aid identification of homologous expressions underpinned by similar muscle contractions. To date, FACS has been developed for humans, and subsequently modified for chimpanzees and rhesus macaques. Through detailed examination of facial anatomy and spontaneous movement, here we present a FACS for hylobatids (gibbons and siamangs): apes living in small groups and often thought not to display extensive facial movement. We identified and described 18 independent facial movements (Action Units and Action Descriptors) in the hylobatid face, and compared to humans, chimpanzees, and rhesus macaques. The findings show that the facial movement capacity of hylobatids bears great similarity to species living in much larger groups. The findings could be explained by phylogenetic inertia (especially because pair-bonding is likely to have emerged from social living) and/or the social demands of pair-bonding.

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References

  1. Baldwin, L. A., & Teleki, G. (1976). Patterns of gibbon behavior on Hall’s Island, Bermuda: A preliminary ethogram for Hylobates lar. In D. Rumbaugh (Ed.), Gibbon and siamang (Vol. 4). Basel: Karger.

    Google Scholar 

  2. Burrows, A. M., Waller, B. M., Parr, L. A., & Bonar, C. J. (2006). Muscles of facial expression in the chimpanzee (Pan troglodytes): Descriptive, comparative, and phylogenetic contexts. Journal of Anatomy, 208(2), 153–168.

    PubMed  Article  Google Scholar 

  3. Burrows, A. M., Waller, B. M., & Parr, L. A. (2009). Facial musculature in the rhesus macaque (Macaca mulatta): Evolutionary and functional contexts with comparisons to chimpanzees and humans. Journal of Anatomy, 215, 320–334.

    PubMed  Article  Google Scholar 

  4. Burrows, A. M., Diogo, R., Waller, B. M., Bonar, C. J., & Liebal, K. (2011). Evolution of the muscles of facial expression in a monogamous ape: Evaluating the relative influence of ecological and phylogenetic factors. Anatomical Record, 294, 645–663.

    Article  Google Scholar 

  5. Chivers, D. J. (1976). Communication within and between family groups of siamang (Symphalangus syndactylus). Behaviour, 57, 116–135.

    Article  Google Scholar 

  6. Diogo, R., Wood, B. A., Aziz, M. A., & Burrows, A. M. (2009). On the origin, homologies and evolution of primate facial muscles, with a particular focus on hominoids, and a suggested unifying nomenclature for the facial muscles of the Mammalia. Journal of Anatomy, 215, 300–319.

    PubMed  Article  CAS  Google Scholar 

  7. Dobson, S. D. (2009). Socioecological correlates of facial mobility in nonhuman anthropoids. American Journal of Physical Anthropology, 139, 413–420.

    PubMed  Article  Google Scholar 

  8. Duchenne de Boulogne, G. B. (1862). In R. A. Cuthbertson (Ed.), The mechanism of human facial expression. New York: Cambridge University Press.

    Google Scholar 

  9. Ekman, P., & Friesen, W. V. (1978). Facial action coding system. Palo Alto: Consulting Psychology Press.

    Google Scholar 

  10. Ekman, P., Friesen, W. V., & Hager, J. C. (2002a). Facial action coding system. Salt Lake City: Research Nexus.

    Google Scholar 

  11. Ekman, P., Friesen, W. V., & Hager, J. C. (2002b). Facial action coding system—investigator’s guide. Salt Lake City: Research Nexus.

    Google Scholar 

  12. Fischer, J. O., & Geissmann, T. (1990). Group harmony in gibbons: Comparison between white-handed gibbon (Hylobates lar) and siamang (H. syndactylus). Primates, 31(4), 481–494.

    Article  Google Scholar 

  13. Fox, G. J. (1977). Social dynamics in siamang. Ph.D. thesis, University of Wisconsin—Milwaukee.

  14. Hewitt, G., MacLarnon, A., & Jones, K. E. (2002). The functions of laryngeal air sacs in primates: a new hypothesis. Folia Primatologica, 73, 70–94.

    Article  Google Scholar 

  15. Hjortsjo, C. H. (1970). Man's face and mimic language. Malmö: Nordens Boktryckeri.

    Google Scholar 

  16. Huber, E. (1931). Evolution of facial musculature and facial expression. Oxford: Oxford University Press.

    Google Scholar 

  17. Liebal, K., Pika, S., & Tomasello, M. (2004). Social communication in siamangs (Symphalangus syndactylus): use of gestures and facial expressions. Primates, 45, 41–57.

    PubMed  Article  Google Scholar 

  18. Maestripieri, D. (1999). Primate social organization, gestural repertoire size, and communication dynamics: A comparative study of macaques. In B. J. King (Ed.), The origins of language: what nonhuman primates can tell us. Santa Fe: School of American Research Press.

    Google Scholar 

  19. Orgeldinger, M. (1999). Paarbeziehungen beim Siamang-Gibbon (Hylobates syndactylus) im Zoo: Untersuchungen über den Einfluß von Jungtieren auf die Paarbindung. Münster: Schüling.

    Google Scholar 

  20. Parr, L. A., & Waller, B. M. (2007). The evolution of human emotion. In T. M. Preuss, & J. H. Kaas (Eds.), The evolution of primate nervous systems. London: Elsevier.

  21. Parr, L. A., Waller, B. M., Burrows, A. M., Gothard, K. M., & Vick, S. J. (2010). MaqFACS: a muscle-based facial movement coding system for the rhesus macaque. American Journal of Physical Anthropology, 143, 625–630.

    PubMed  Article  CAS  Google Scholar 

  22. Preuschoft, S. (1995). Laughter and smiling in macaques—an evolutionary perspective. Ph.D. thesis, University of Utrecht.

  23. Reichard, U. (1995). Extra-pair copulations in a monogamous gibbon (Hylobates lar). Ethology, 100, 99–112.

    Article  Google Scholar 

  24. Roos, C., & Geissmann, T. (2001). Molecular phylogeny of the major hylobatid divisions. Molecular Phylogenetics and Evolution, 19, 486–494.

    PubMed  Article  CAS  Google Scholar 

  25. Rowe, N. (1996). The pictorial guide to the living primates. Charlestown: Pogonias.

    Google Scholar 

  26. Shultz, S., & Dunbar, R. (2007). The evolution of the social brain: anthropoid primates contrast with other vertebrates. Proceedings of the Royal Society of London B: Biological Sciences, 274, 2429–2436.

    Article  Google Scholar 

  27. Shultz, S., Opie, C., & Atkinson, Q. D. (2011). Stepwise evolution of stable sociality in primates. Nature, 479, 7372.

    Article  Google Scholar 

  28. van Hooff, J. A. R. A. M. (1967). The facial displays of the Catarrhine monkeys and apes. In D. Morris (Ed.), Primate ethology (pp. 7–68). Chicago: Aldine.

    Google Scholar 

  29. Vick, S. J., & Paukner, A. (2010). Variation and context of yawns in captive chimpanzees (Pan troglodytes). American Journal of Primatology, 72, 262–269.

    PubMed  Article  Google Scholar 

  30. Vick, S. J., Waller, B. M., Parr, L. A., Smith Pasqualini, M. C., & Bard, K. A. (2007). A cross-species comparison of facial morphology and movement in humans and chimpanzees using the facial action coding system (FACS). Journal of Nonverbal Behavior, 31, 1–20.

    PubMed  Article  Google Scholar 

  31. Waller, B. M., Vick, S.-J., Parr, L. A., Smith Pasqualini, M. C., Bard, K. A., Gothard, K., & Fuglevand, A. J. (2006). Intramuscular electrical stimulation of facial muscles in humans and chimpanzees: Duchenne revisited and extended. Emotion, 6, 367–382.

    PubMed  Article  Google Scholar 

  32. Waller, B. M., Bard, K. A., Vick, S. J., & Smith Pasqualini, M. C. (2007). Perceived differences between chimpanzee and human facial expressions are related to emotional interpretation. Journal of Comparative Psychology, 121(4), 398–404.

    PubMed  Article  Google Scholar 

  33. Waller, B. M., Parr, L. A., Gothard, K. M., Burrows, A. M., & Fuglevand, A. J. (2008a). Mapping the contribution of single muscles to facial movements in the Rhesus Macaque. Physiology & Behavior, 95, 93–100.

    Article  CAS  Google Scholar 

  34. Waller, B. M., Cray, J. J., & Burrows, A. M. (2008b). Selection for universal facial emotion. Emotion, 8(3), 435–439.

    PubMed  Article  Google Scholar 

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Acknowledgments

This project was funded by Deutsche Forschungsgemeinschaft (DFG) within the Excellence initiative Languages of Emotion (Project leaders: Katja Liebal, Bridget Waller and Anne Burrows): “Comparing emotional expression across species – GibbonFACS.” We thank Robert Zingg and Zoo Zurich (Switzerland), Jennifer Spalton and Twycross Zoo (UK), Neil Spooner and Howletts Wild Animal Park (UK), and Corinne Di Trani and Mulhouse Zoo (France) for allowing us to collect footage of their animals. We also thank Gill Vale and Andrea van Allmen for support in collecting some of the video footage, Cátia Caeiro for reliability coding, and Joanna Setchell and two anonymous reviewers for useful comments.

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Correspondence to Bridget M. Waller.

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Waller, B.M., Lembeck, M., Kuchenbuch, P. et al. GibbonFACS: A Muscle-Based Facial Movement Coding System for Hylobatids. Int J Primatol 33, 809–821 (2012). https://doi.org/10.1007/s10764-012-9611-6

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Keywords

  • Communication
  • Emotion
  • Evolution
  • Facial expression
  • FACS
  • Primates