Abstract
Comparing homologous expressions between species can shed light on the phylogenetic and functional changes that have taken place during evolution. To assess homology across species we must approach primate facial expressions in an anatomical, systematic, and standardized way. The Facial Action Coding System (FACS), a widely used muscle-based tool for analyzing human facial expressions, has recently been adapted for chimpanzees (Pan troglodytes: ChimpFACS), rhesus macaques (Macaca mulatta: MaqFACS), and gibbons (GibbonFACS). Here, we present OrangFACS, a FACS adapted for orangutans (Pongo spp.). Orangutans are the most arboreal and the least social great ape, so their visual communication has been assumed to be less important than vocal communication and is little studied. We scrutinized the facial anatomy of orangutans and coded videos of spontaneous orangutan behavior to identify independent movements: Action Units (AUs) and Action Descriptors (ADs). We then compared these facial movements with movements of homologous muscles in humans, chimpanzees, macaques, and gibbons. We also noted differences related to sexual dimorphism and developmental stages in orangutan facial morphology. Our results show 17 AUs and 7 ADs in orangutans, indicating an overall facial mobility similar to that found in chimpanzees, macaques, and gibbons but smaller than that found in humans. This facial movement capacity in orangutans may be the result of several, nonmutually exclusive explanations, including the need for facial communication in specialized contexts, phylogenetic inertia, and allometric effects.
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References
Andrew, R. J. (1963a). Evolution of facial expression. Science, 142(3595), 1034–1041.
Andrew, R. J. (1963b). The origin and evolution of the calls and facial expressions of the primates. Behaviour, 20, 1–107.
Bard, K. A., Gaspar, A., & Vick, S. J. (2011). Chimpanzee faces under the magnifying glass: emerging methods reveal cross-species similarities and individuality. In A. Weiss, J. King, & L. Murray (Eds.), Personality and behavioral syndromes in nonhuman primates. New York: Springer.
Bennett, E. L. (1998). The natural history of the orangutan. Kota Kinabalu: Natural History Publications.
Blomberg, S. P., & Garland, T. (2002). Tempo and mode in evolution: phylogenetic inertia, adaptation and comparative methods. Journal of Evolutionary Biology, 15, 899–910.
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.
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.
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.
Chevalier-Skolnikoff, S. (1982). A cognitive analysis of facial behavior in Old World monkeys, apes, and human beings. In C. T. Snowdon, C. H. Brown, & M. R. Petersen (Eds.), Primate communication (pp. 303–368). Cambridge, UK: Cambridge University Press.
Darwin, C. (1872). The expression of the emotions in man and animals. Chicago and London: The University of Chicago Press.
Davila Ross, M., & Geissmann, T. (2007). Call diversity of wild male orangutans: a phylogenetic approach. American Journal of Primatology, 69, 305–324.
Davila Ross, M., Menzler, S., & Zimmermann, E. (2008). Rapid facial mimicry in orangutan play. Biology Letters, 4, 27–30.
Davila Ross, M., Owren, M. J., & Zimmermann, E. (2009). Reconstructing the evolution of laughter in great apes and humans. Current Biology, 19(13), 1106–1111.
Duchenne de Boulogne, G. B. (1990). The mechanism of human facial expression. In R. A. Cuthbertson (Ed and translator). New York: Cambridge University Press. (Reprinted from Mécanisme de la Physionomie Humaine, 1862, Paris, Jules Renouard Libraire).
Delgado, R. A., & van Schaik, C. P. (2000). The behavioral ecology and conservation of the orangutan: a tale of two islands. Evolutionary Anthropology, 9, 201–218.
Delgado, R. A., Lameira, A. R., Davila Ross, M., Husson, S. J., Morrogh-Bernard, H. C., & Wich, S. A. (2009). Geographical variation in orangutan long calls. In S. A. Wich, S. S. Utami-Atmoko, T. Mitra Setia, & C. P. van Schaik (Eds.), Orangutans: geographic variation in behavioural ecology and conservation (pp. 215–224). New York: Oxford University Press.
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.
Dobson, S. D. (2009a). Allometry of facial mobility in anthropoid primates: implications for the evolution of facial expression. American Journal of Physical Anthropology, 138(1), 70–81.
Dobson, S. D. (2009b). Socioecological correlates of facial mobility in nonhuman anthropoids. American Journal of Physical Anthropology, 139(3), 413–420.
Dobson, S. D., & Sherwood, C. C. (2011). Correlated evolution of brain regions involved in producing and processing facial expressions in anthropoid primates. Biology Letters, 7(1), 86–88.
Ekman, P., & Friesen, W. V. (1978). The facial action coding system: a technique for the measurement of facial movement. Palo Alto: Consulting Psychologist Press.
Ekman, P., Friesen, W. V., & Hager, J. C. (2002). Facial action coding system. Salt Lake City: Research Nexus.
Galdikas, B. M. F. (1983). The orangutan long call and snag crashing at Tanjung Puting Reserve. Primates, 24(3), 371–384.
Goossens, B., Chikhi, L., Jalil, M. F., James, S., Ancrenaz, M., Lackman-Ancrenaz, I., & Bruford, M. W. (2009). Taxonomy, geographic variation and population genetics of Bornean and Sumatran orangutans. In S. A. Wich, S. S. Utami-Atmoko, T. Mitra Setia, & C. P. van Schaik (Eds.), Orangutans: geographic variation in behavioural ecology and conservation (pp. 215–224). New York: Oxford University Press.
Hardus, M. E., Lameira, A. R., Singleton, I., Knott, C. D., Morrogh-Bernard, H. C., Ancrenaz, M., Utami-Atmoko, S. S., & Wich, S. A. (2009). A description of the orangutan's vocal and sound repertoire, with a focus on geographic variation. In S. A. Wich, S. S. Utami-Atmoko, T. Mitra Setia, & C. P. van Schaik (Eds.), Orangutans (pp. 49–64). Oxford: Oxford University Press.
Hens, S. M. (2003). Growth and sexual dimorphism in orangutan crania: a three-dimensional approach. American Journal of Physical Anthropology, 121, 1–29.
Hinde, R. A., & Rowell, T. (1962). Communication by postures and facial expressions in the rhesus monkey (Macaca mulatta). Proceedings of the Zoological Society of London, 138, 1–21.
Huber, E. (1931). Evolution of the facial musculature and facial expression. Baltimore: Johns Hopkins University Press and London: Oxford University Press.
Kuze, N., Malim, T. P., & Kohshima, S. (2005). Developmental changes in the facial morphology of the Borneo orangutan (Pongo pygmaeus): possible signals in visual communication. American Journal of Primatology, 65, 353–376.
Lameira, A. R., & Wich, S. A. (2008). Orangutan long call degradation and individuality over distance: a playback approach. International Journal of Primatology, 29, 615–625.
Leavens, D. (2007). Animal cognition: multimodal tactics of orangutan communication. Current Biology, 17(17), 762–764.
Leigh, S. R. (1992). Patterns of variation in the ontogeny of primate body size dimorphism. Journal of Human Evolution, 23, 27–50.
Liebal, K., Pika, S., & Tomasello, M. (2006). Gestural communication of orangutans (Pongo pygmaeus). Gesture, 6(1), 1–38.
Lightoller, G. S. (1928). The facial muscles of three orangutans and two cercopithecidae. Journal of Anatomy, 63, 19–81.
MacKinnon, J. R. (1974). The behaviour and ecology of wild orang-utan (Pongo pygmaeus). Animal Behaviour, 22, 3–74.
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 (pp. 55–77). Santa Fe: School of American Research.
Marler, P. (1965). Communication in monkeys and apes. In I. Devore (Ed.), Primate behavior: field studies of monkeys and apes (pp. 544–584). New York: Holt, Rinehart and Winston.
Mitra Setia, T., Delgado, R. A., Utami Atmoko, S. S., Singleton, I., & van Schaik, C. P. (2009). Social organization and male-female relationships. In S. A. Wich, S. S. Utami Atmoko, T. Mitra Setia, & C. P. van Schaik (Eds.), Orangutans: geographic variation in behavioral ecology and conservation (pp. 245–253). New York: Oxford University Press.
Nakamichi, M. (2004). Tool-use and tool-making by captive, group-living orangutans (Pongo pygmaeus abelii) at an artificial termite mound. Behavioural Processes, 65(1), 87–93.
O’Malley, R. C., & McGrew, W. C. (2000). Oral tool use by captive orangutans (Pongo pygmaeus). Folia Primatologica, 71, 334–341.
Parr, L. A., & Maestripieri, D. (2003). Nonvocal communication in nonhuman primates. In D. Maestripieri (Ed.), Primate psychology: the mind and behavior of human and nonhuman primates (pp. 324–358). Chicago: Chicago University Press.
Parr, L. A., Waller, B. M., Vick, S. J., & Bard, K. A. (2007). Classifying chimpanzee facial expressions using muscle action. Emotion, 7(1), 172–181.
Parr, L. A., Waller, B. M., Burrows, A. M., Gothard, K. M., & Vick, S. J. (2010). Brief communication: MaqFACS: a muscle-based facial action coding system for the rhesus macaque. American Journal of Physical Anthropology, 143, 625–630.
Preuschoft, S. (1992). “Laughter” and “smile” in Barbary macaques (Macaca sylvanus). Ethology, 9(1), 200–236.
Preuschoft, S., & van Hooff, J. A. R. A. M. (1995). Homologizing primate facial displays: a critical review of methods. Folia Primatologica, 65, 121–137.
Preuschoft, S., & van Hooff, J. A. R. A. M. (1997). The social function of “smile” and “laughter”: variations across primate species and societies. In U. Segerstrale & P. Mobias (Eds.), Nonverbal communication: where nature meets culture (pp. 252–281). Mahwah, NJ: Lawrence Erlbaum.
Rijksen, H. D., & Meijaard, E. (1999). Our vanishing relative: the status of wild orang-utans at the close of the twentieth century. Dordrecht: Kluwer Academic.
Rowe, C. (1999). Receiver psychology and the evolution of multicomponent signals. Animal Behaviour, 58, 921–931.
Schaller, G. B. (1961). The orang-utan in Sarawak. Zoologica, 46(2), 72–82.
Seiler, R. (1971). Facial musculature and its influence on the facial bones of catarrhine Primates. III. Gegenbaurs Morphologisches Jahrbuch, 116, 347–376.
Shea, B. T. (1986). On skull form and the supraorbital torus in primates. Current Anthropology, 27(3), 257–260.
Sherwood, C. C., Holloway, R. L., Gannon, P. J., Semendeferi, K., Erwin, J. M., Zilles, K., & Hof, P. R. (2003). Neuroanatomical basis of facial expression in monkeys, apes, and humans. Annals of the New York Academy of Sciences, 1000, 99–103.
Sherwood, C. C., Hof, P. R., Holloway, R. L., Semendeferi, K., Gannon, P. J., Frahm, H. D., & Zilles, K. (2005). Evolution of the brainstem orofacial motor system in primates: a comparative study of trigeminal, facial and hypoglossal nuclei. Journal of Human Evolution, 48, 45–84.
Sonntag, C. F. (1924). The morphology and evolution of apes and man. London: John Bale, Sons and Danielsson.
Steiner, J. E., Glaser, D., Hawilo, M. E., & Berridge, K. C. (2001). Comparative expression of hedonic impact: affective reactions to taste by human infants and other primates. Neuroscience and Biobehavioral Reviews, 25(1), 53–74.
Utami Atmoko, S. S., & van Hooff, J. A. R. A. M. (2004). Alternative male reproductive strategies: male bimaturism in orangutans. In P. Kappeler & C. P. van Schaik (Eds.), Sexual selection in primates: new and comparative perspectives (pp. 196–207). Cambridge, UK: Cambridge University Press.
van Hooff, J. A. R. A. M. (1962). Facial expressions in higher primates. Symposia of the Zoological Society of London, 8, 97–125.
van Hooff, J. A. R. A. M. (1972). A comparative approach to the phylogeny of laughter and smiling. In R. A. Hinde (Ed.), Non-verbal communication. Cambridge, UK: Cambridge University Press.
van Lawick-Goodall, J. (1968). A preliminary report on expressive movements and communication in the Gombe stream chimpanzees. In P. C. Jay (Ed.), Primates: studies in adaptation and variability. New York: Holt.
van Schaik, C. P. (1999). The socioecology of fission-fusion sociality in orangutans. Primates, 40(1), 69–86.
van Schaik, C. P. (2004). Among orangutans: red apes and the rise of human culture. Cambridge: The Belknap Press of Harvard University Press.
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 FACS. Journal of Nonverbal Behaviour, 31, 1–20.
Waller, B. M., Vick, S. J., Parr, L. A., Bard, K. A., Pasqualini, M. C., Gothard, K. M., & Fuglevand, A. J. (2006). Intramuscular electrical stimulation of facial muscles in humans and chimpanzees: Duchenne revisited and extended. Emotion, 6, 367–382.
Waller, B. M., Parr, L. A., Gothard, K. M., Burrows, A. M., & Fuglevand, A. J. (2008). Mapping the contribution of single muscles to facial movements in the rhesus macaque. Physiology & Behaviour, 95, 93–100.
Waller, B. M., Lembeck, M., Kuchenbuch, P., Burrows, A. M., & Liebal, K. (2012). GibbonFACS: a muscle-based facial movement coding system for hylobatids. International Journal of Primatology, 33(4), 809–821.
Wexler, D. A. (1972). Method for unitizing protocols of descriptions of emotional states. Journal of Supplemental Abstracts Service, Catalogue of Selected Documents in Psychology, American Psychological Association, 2, 116.
Wich, S. A., Sterck, E. H. M., & Utami, S. S. (1999). Are orangutan females as solitary as chimpanzee females? Folia Primatologica, 70, 23–28.
Wich, S. A., Utami-Atmoko, S. S., Mitra Setia, T., Rijksen, H. R., Schürmann, C., van Hooff, J. A. R. A. M., & van Schaik, C. P. (2004). Life history of wild Sumatran orangutans (Pongo abelii). Journal of Human Evolution, 47, 385–398.
Wich, S. A., Vries, H., Ancrenaz, M., Perkins, L., Shumaker, R. W., Suzuki, A., & van Schaik, C. P. (2009). Orangutan life history variation. In S. A. Wich, S. S. Utami Atmoko, T. Mitra Setia, & C. P. van Schaik (Eds.), Orangutans: geographic variation in behavioral ecology and conservation (pp. 65–76). New York: Oxford University Press.
Wilson, E. O. (1975). Sociobiology: the new synthesis. Cambridge: Harvard University Press.
Winkler, L. A. (1989). Morphology and relationships of the orangutan fatty cheek pads. American Journal of Primatology, 17(4), 305–319.
Acknowledgments
This project was funded by European Commission Leonardo da Vinci grant (to C. C. Caeiro), Center for Systems Neuroscience Hannover, Forschungszentrum Jülich, Gesellschaft der Freunde der TiHo, and University of Veterinary Medicine Hannover (to M. Davila-Ross), and a University of Portsmouth Department of Psychology Small Grant (to B. M. Waller and M. Davila-Ross). We further thank Faculdade de Ciências da Universidade de Lisboa and University of Portsmouth for a mobility partnership; Apenheul Primate Park, Leipzig Zoological Garden, Sepilok Rehabilitation Centre, Tierpark Carl Hagenbeck, and Zoo Wilhelma for allowing data collection; S. Alsisto, E. Bosi, Sabah Wildlife Department, and Economic Planning Unit for giving M. Davila-Ross support and permission to conduct research on orangutans in Sabah, Borneo; C. Schopf, E. Ey, M. Wessels, S. Johnson, and R. Sharma for assistance in collecting data; M. Lembeck and W. Hoffmann for reliability coding; K. Peirce for OrangFACS website; and J. Setchell and two anonymous reviewers for valuable comments on the manuscript.
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Online Resources 1 (mpg file
Video example of Action Unit 1+2 – inner and outer brow raiser. (MPG 4724 kb)
Online Resources 2 (mpg file
Video example of Action Unit 4 - glabella lowerer. (MPG 1184 kb)
Online Resources 3 (mpg file
Video example of Action Unit 6 - cheek raiser. (MPG 1636 kb)
Online Resources 4 (mpg file
Video example of Action Unit 9 – nose wrinkler. (MPG 832 kb)
Online Resources 5 (mpg file
Video example of Action Unit 10 - upper lip raiser. (MPG 3366 kb)
Online Resources 6 (mpg file
Video example of Action Unit 12 - lip corner puller. (MPG 366 kb)
Video example of Action Unit 16 - lower lip depressor. (MPG 2870 kb)
Online Resources 8 (mpg file
Video example of Action Unit 17 – chin raiser. (MPG 25282 kb)
Online Resources 9 (mpg file
Video example of Action Unit 18 – lip pucker. (MPG 5092 kb)
Online Resources 10 (mpg file
Video example of Action Unit 22 - lip funneler. (MPG 364 kb)
Online Resources 11 (mpg file
Video example of Action Unit 24 - lip presser. (MPG 978 kb)
Online Resources 12 (mpg file
Video example of Action Unit 28 - lips suck. (MPG 278 kb)
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Caeiro, C.C., Waller, B.M., Zimmermann, E. et al. OrangFACS: A Muscle-Based Facial Movement Coding System for Orangutans (Pongo spp.). Int J Primatol 34, 115–129 (2013). https://doi.org/10.1007/s10764-012-9652-x
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DOI: https://doi.org/10.1007/s10764-012-9652-x