Abstract
Though many nonhuman primates possess a laryngeal sac, the great apes are unique in their great size. Though an enlarged sac probably arose in their common ancestor, its functional adaptations remain a matter of debate. Its development in extant great apes is likely to provide valuable information to clarify the issue. We used magnetic resonance imaging to examine the development of the laryngeal sac in 3 living chimpanzees, age 4 mo–5 yr, and identified 2 distinct growth phases of the sac. A gradual growth of the sac in early infancy results in a configuration so that it occupies the ventral region of the neck; many adult nonhominoid primates having a sac show the configuration. The subsequent rapid expansion of the sac in late infancy causes the final configuration in chimpanzees, wherein the sac expands into the pectoral, clavicular, and axillary regions. The latter phase possibly arose at latest in the last common ancestor of extant great apes and contributed to the evolution of the enlarged sac, despite the later evolutionary diversification in adult sac anatomy and growth. As many studies have advocated, the enlarged sac probably plays a role in vocalization in adults. However, physiological modifications in the laryngeal region during infancy are likely to provide valuable information to evaluate the functional adaptations of the enlarged sac in the great apes.
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References
Avril, C. (1963). Kehlkopf und Kehlsack des Schimpansen, Pan troglodytes (Blumenbach 1799). Gegenbaurs Morphologisches Jahrbuch, 105, 74–129.
Brandes, R. (1932). Über den Kehlkopf des Orang-Utan in verschiedenen Altersstadien mit besonderer Berücksichtigung der Kehlsackfrage. Gegenbaurs Morphologisches Jahrbuch, 69, 1–61.
Fitch, W. T. (2000). The evolution of speech: A comparative review. Trends in Cognitive Sciences, 4, 258–267.
Fitch, W. T., & Hauser, M. D. (2003). Unpacking “honesty”: Vertebrate vocal production and the evolution of acoustic signals. In A. M. Simmons, A. N. Popper, & R. R., Fay (Eds.), Acoustic communication (pp. 65–137). New York: Springer-Verlag.
Gautier, J. P. (1971). Etude morphologique et fonctionnelle des annexes extra-laryngées des Cercopithecinae; liaison avec les cris d’espacement. Biologia Gabonica, 7, 229–267.
Geist, F. D. (1965). Nasal cavity, larynx, mouth, and pharynx. In C. G. Hartman, & W. L. Straus Jr., (eds.), The anatomy of the rhesus monkey (pp. 189–209) New York: Hafner Publishing.
Gould, S. J. (1977). Ontogeny and phylogeny. Belknap Harvard, Cambridge, MA.
Hayama, S. (1970). The Saccus laryngis in primates. Journal of the Anthropological Society of Nippon, 78, 274–298, (in Japanese with English abstract).
Hayama, S. (1996). Why does not the monkey fall from a tree? The functional origin of the human glottis. Primate Research, 12, 179–206. (in Japanese with English abstract)
Hewitt, G., MacLarnon, A., & Jones, K. E. (2002). The functions of laryngeal air sac in primates: A new hypothesis. Folia Primatologica, 73, 70–94.
Hill, W. C. O., & Booth, A. H. (1957). Voice and larynx in African and Asiatic colobidae. Journal of the Bombay Natural History Society, 54, 309–321.
Huber, E. (1931). Evolution of Facial Musculature and Expression. The Johns Hopkins University Press, Baltimore.
Kelemen, G. (1948). The anatomical basis of phonation in the chimpanzee. Journal of Morphology, 82, 229–256.
Kleinschmidt, A. (1938). Die Schlund-und Kehlorgane des Gorillas “Bobby” unter besonderer Berücksichtigung der gleichen Organe von Mensch und Orang. Gegenbaurs Morphologisches Jahrbuch, 81, 78–157.
Lieberman, P. (2006). Limits on tongue deformation-Diana money formants and the impossible vocal tract shapes proposed by Riede et al. (2005). J. Human Evolution, 50, 219–221.
Marler, P., & Tenaza, R. (1977). Signaling behavior of apes with special reference to vocalization. In T. A. Sebeok (ed.), How animals communicate (pp. 965–1033) Indiana University Press, Bloomington.
Matsuzawa, T. (2003). The Ai project: Historical and ecological contexts. Animal cognition, 6, 199–211.
McKinney, M. L., & McNamara, K. J. (1991). Heterochrony: The evolution of ontogeny. Plenum Press, New York.
Napier, J. R., & Napier, P. H. (1985). The natural history of the primates. Cambridge, MA: MIT Press.
Negus, V. E. (1949). The Comparative Anatomy and Physiology of the Larynx. London: William Heinemann Medical Books.
Némai, J., & Kelemen, G. (1933). Beiträge zur Kenntnis des Gibbonkehlkopfes. Zeitschrift fuÉr Anatomie und Entwicklungsgeschichte, 100, 512–520.
Nishimura, T., Mikami, A., Suzuki, J., & Matsuzawa, T. (2003). Descent of the larynx in chimpanzee infants. Proceedings of the National Academy of Sciences, USA, 100, 6930–6933.
Nishimura, T., Mikami, A., Suzuki, J., & Matsuzawa, T. (2006). Descent of the hyoid in chimpanzees: evolution of face flattening and speech. Journal of Human Evolution, 51, 244–254.
Primate Research Institute, Kyoto University. (1986). Guide for the care and use of laboratory primates. Primate Research Institute, Kyoto University, Inuyama, Japan.
Primate Research Institute, Kyoto University. (2002). Guide for the care and use of laboratory primates, 2nd ed. Primate Research Institute, Kyoto University, Inuyama, Japan.
Raven, H. C. (1950). The Anatomy of the Gorilla. Columbia University Press, New York.
Rice, S. H. (2000). The analysis of ontogenetic trajectories: When a change in size or shape in not heterochrony. Proceedings of the National Academy of Sciences of the United States of America, 94, 907–912.
Riede, T., Bronson, E. Hatzikirou, H., & Zuberbühler, K. (2006). Multiple discontinuities in nonhuman vocal tracts—A response to Lieberman (2006). Journal of Human Evolution, 50, 222–225.
Schön, M. A. (1971). The anatomy of the resonating mechanism in howling monkeys. Folia Primatologica, 15, 117–132.
Schön Ybarra, M. A. (1995). A comparative approach to the non-human primate vocal tract: Implications for sound production. In E. Zimmerman, J. D. Newman, & U. Jürgens (eds.), Current Topics in Primate Vocal Communication. Plenum Press, New York, pp. 185–198.
Starck, D., & Schneider, R. (1960). Respirationsorgane: A. Larynx. In H., Hofer, A. H., Schultz, & D. Starck (eds.), Primatologia, Vol. 3–2. Karger, Basel, pp. 423–587.
Tucker, G., & Tucker, J. A. (1975). Observations on the primate hyoepiglottic complex. Annals of Otology, Rhinology & Laryngology, 84, 827–832.
Tuttle, R. H. (1986). Apes of the world: Their social behavior, communication, mentality, and ecology. Noyes Publications, Park Ridge, NJ.
Acknowledgments
We thank A. Kato, K. Kumazaki, N. Maeda, S. Goto, C. Hashimoto, and K. Matsubayashi, M. Tomonaga, M. Tanaka, Y. Hamada, and other staff of Primate Research Institute, Kyoto University (PRI) for permission for or help with the MRI examinations of 3 chimpanzee infants. We performed portions of this work at PRI under PRI Cooperative Research Programs (grant 4–1, 3–1 to T. Nishimura). A Research Fellowship of the Japan Society for the Promotion of Science (JSPS) for Young Scientist (grant 16000326 to T. N.), JSPS Core-to-Core program HOPE (grant 15001 to PRI), and Grants-in-Aid for Specially Promoted Research (grants 1200200916002001 to T. M.) and for the Biodiversity Research of the 21st Century Center of Excellence (grant A14 to Kyoto University) from the Ministry of Education, Culture, Sports, Sciences, and Technology of Japan provided financial support for the work.
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Nishimura, T., Mikami, A., Suzuki, J. et al. Development of the Laryngeal Air Sac in Chimpanzees. Int J Primatol 28, 483–492 (2007). https://doi.org/10.1007/s10764-007-9127-7
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DOI: https://doi.org/10.1007/s10764-007-9127-7