Functional morphology of the Alligator mississippiensis larynx with implications for vocal production
Abstract
Sauropsid vocalization is mediated by the syrinx in birds and the larynx in extant reptiles; but whereas avian vocal production has received much attention, the vocal mechanism of basal reptilians is poorly understood. The American alligator (Alligator mississippiensis) displays a large vocal repertoire during mating and in parent-offspring interactions. Although vocal outputs of these behaviors have received some attention, the underlying mechanism of sound production remains speculative. Here, we investigate the laryngeal anatomy of juvenile and adult animals by macroscopic and histological methods. Observations of the cartilaginous framework and associated muscles largely corroborate earlier findings, but one muscle, the cricoarytenoideus, exhibits a heretofore unknown extrinsic insertion that has important implications for effective regulation of vocal fold length and tension. Histological investigation of the larynx revealed a layered vocal fold morphology. The thick lamina propria consists of non-homogenous extracellular matrix containing collagen fibers that are tightly packed below the epithelium but loosely organized deep inside the vocal fold. We found few elastic fibers but comparatively high proportions of hyaluronan. Similar organizational complexity is also seen in mammalian vocal folds and the labia of the avian syrinx: convergent morphologies that suggest analogous mechanisms for sound production. In tensile tests, alligator vocal folds demonstrated a linear s…
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Percussion is a means of acoustic signalling involving sounds created by body-body or body‐object striking, such as jaw pops and headslaps.
“A third means of acoustic signalling is percussion, involving sounds created by body–body or body‐object striking, such as jaw pops and headslaps (Vergne et al. 2009; Riede et al. 2011, 2015).”
From Roars, Rumbles, and Resonance: A Systematic Review and Meta‐Analysis of Crocodylian Acoustic Signals (2026) · cites this paper as Riede et al. 2015
Cites
Metscher, B. D. (2009) · BMC Physiology · doi:10.1186/1472-6793-9-11 · Cited by 1,086 · see citing works
Synthesis of Voiced Sounds From a Two-Mass Model of the Vocal Cords
Ishizaka, K., & Flanagan, J. L. (1972) · Bell System Technical Journal · doi:10.1002/j.1538-7305.1972.tb02651.x · Cited by 899 · see citing works
The physics of small-amplitude oscillation of the vocal folds
Titze, I. R. (1988) · The Journal of the Acoustical Society of America · doi:10.1121/1.395910 · Cited by 869 · see citing works
Morphological Structure of the Vocal Cord as a Vibrator and its Variations
Hirano, M. (2009) · Folia Phoniatrica et Logopaedica · doi:10.1159/000263771 · Cited by 624 · see citing works
Myoelastic-Aerodynamic Theory of Voice Production
van den Berg, J. (1958) · Journal of Speech and Hearing Research · doi:10.1044/jshr.0103.227 · Cited by 522 · see citing works
Crocodilian biology and evolution
Grigg, G. C., Seebacher, F., & Franklin, C. E. (2001) · Cited by 399 · see citing works
On the relation between subglottal pressure and fundamental frequency in phonation
Titze, I. R. (1989) · The Journal of the Acoustical Society of America · doi:10.1121/1.397562 · Cited by 392 · see citing works
Bifurcations in an asymmetric vocal-fold model
Steinecke, I., & Herzel, H. (1995) · The Journal of the Acoustical Society of America · doi:10.1121/1.412061 · Cited by 345 · see citing works
The myoelastic aerodynamic theory of phonation
Titze, I. R. (2006) · Cited by 245 · see citing works
Vocal fold physiology : biomechanics, acoustics, and phonatory control
Titze, I. R., & Scherer, R. C. (1983) · Medical Entomology and Zoology · Cited by 238 · see citing works
Evolutionary Origins for Social Vocalization in a Vertebrate Hindbrain–Spinal Compartment
Bass, A. H., Gilland, E., & Baker, R. G. V. (2008) · Science · doi:10.1126/science.1157632 · Cited by 211 · see citing works
Social Signals and Behaviors of Adult Alligators and Crocodiles
GARRICK, L. D., & LANG, J. W. (1977) · American Zoologist · doi:10.1093/icb/17.1.225 · Cited by 193 · see citing works
Riede, T., & Goller, F. (2010) · Brain and Language · doi:10.1016/j.bandl.2009.11.003 · Cited by 159 · see citing works
Self-citationAcoustic communication in crocodilians: from behaviour to brain
Vergne, A. L., Pritz, M. B., & Mathevon, N. (2009) · Biological Reviews · doi:10.1111/j.1469-185x.2009.00079.x · Cited by 151 · see citing works
Phonation threshold pressure in a physical model of the vocal fold mucosa
Titze, I. R., Schmidt, S. S., & Titze, M. R. (1995) · The Journal of the Acoustical Society of America · doi:10.1121/1.411870 · Cited by 143 · see citing works
Dependence of phonation threshold pressure on vocal tract acoustics and vocal fold tissue mechanics
Chan, R. W., & Titze, I. R. (2006) · The Journal of the Acoustical Society of America · doi:10.1121/1.2173516 · Cited by 127 · see citing works
Social Displays of the American Alligator (<i>Alligator mississippiensis</i>)
VLIET, K. A. (1989) · American Zoologist · doi:10.1093/icb/29.3.1019 · Cited by 127 · see citing works
Relative Contributions of Collagen and Elastin to Elasticity of the Vocal Fold Under Tension
Chan, R. W., Fu, M., Young, L. B., & Tirunagari, N. (2007) · Annals of Biomedical Engineering · doi:10.1007/s10439-007-9314-x · Cited by 116 · see citing works
Integrative physiology of fundamental frequency control in birds
Goller, F., & Riede, T. (2012) · Journal of Physiology-Paris · doi:10.1016/j.jphysparis.2012.11.001 · Cited by 82 · see citing works
Self-citationCrocodilian behaviour: a window to dinosaur behaviour?
Brazaitis, P., & Watanabe, M. E. (2011) · Historical Biology · doi:10.1080/08912963.2011.560723 · Cited by 73 · see citing works
Hartman, C. G. (1916) · Journal of Morphology · doi:10.1002/jmor.1050270102 · Cited by 71 · see citing works
Morphological basis for the evolution of acoustic diversity in oscine songbirds
Riede, T., & Goller, F. (2014) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.2306 · Cited by 57 · see citing works
Self-citationObservations on Maternal Behavior of the American Alligator, Alligator mississippiensis
Hunt, R. H., & Watanabe, M. E. (1982) · Journal of Herpetology · doi:10.2307/1563716 · Cited by 55 · see citing works
Fee, M. S. (2002) · Journal of Comparative Physiology A · doi:10.1007/s00359-002-0349-z · Cited by 53 · see citing works
The anatomy of vocal divergence in North American Elk and European red deer
Frey, R., & Riede, T. (2012) · Journal of Morphology · doi:10.1002/jmor.20092 · Cited by 46 · see citing works
Self-citationAdapted to Roar: Functional Morphology of Tiger and Lion Vocal Folds
Klemuk, S. A., Riede, T., Walsh, E. J., & Titze, I. R. (2011) · PLoS ONE · doi:10.1371/journal.pone.0027029 · Cited by 45 · see citing works
Self-citationAcoustic signals of Chinese alligators (<i>Alligator sinensis</i>): Social communication
Wang, X., Wang, D., Wu, X., Wang, R., & Wang, C. (2007) · The Journal of the Acoustical Society of America · doi:10.1121/1.2714910 · Cited by 41 · see citing works
Glottal configuration associated withfundamental frequency and vocal register
Murry, T., Xu, J., & Woodson, G. E. (1998) · Journal of Voice · doi:10.1016/s0892-1997(98)80074-x · Cited by 41 · see citing works
Vocalization in juvenile crocodilians.
Herzog, H. A., & Burghardt, G. M. (1977) · PubMed · Cited by 40 · see citing works
Elasticity and stress relaxation of rhesus monkey (Macaca mulatta) vocal folds
Riede, T. (2010) · Journal of Experimental Biology · doi:10.1242/jeb.044404 · Cited by 39 · see citing works
Self-citationRiede, T., Lingle, S., Hunter, E. J., & Titze, I. R. (2009) · Journal of Morphology · doi:10.1002/jmor.10774 · Cited by 38 · see citing works
Self-citationHenle, J. (1839) · Leopold Voss eBooks · doi:10.5962/bhl.title.64345 · Cited by 38 · see citing works
Observations on the acoustic behavior of crocodilians
Campbell, H. W. (1973) · Zoologica scientific contributions of the New York Zoological Society · doi:10.5962/p.203220 · Cited by 38 · see citing works
Laryngotracheal morphology of Afro-Madagascan Geckos: A comparative survey
Russell, A. P., Rittenhouse, D. R., & Bauer, A. M. (2000) · Journal of Morphology · doi:10.1002/1097-4687(200009)245:3 · Cited by 34 · see citing works
Larynx morphology and sound production in three species of Testudinidae
Sacchi, R., Galeotti, P., Fasola, M., & Gerzeli, G. (2004) · Journal of Morphology · doi:10.1002/jmor.10236 · Cited by 33 · see citing works
Todd, N. P. M. (2007) · The Journal of the Acoustical Society of America · doi:10.1121/1.2785811 · Cited by 30 · see citing works
Riede, T., Tokuda, I. T., & Farmer, C. G. (2011) · Journal of Experimental Biology · doi:10.1242/jeb.051110 · Cited by 29 · see citing works
Self-citationMoore, B. A., Russell, A. P., & Bauer, A. M. (1991) · Journal of Morphology · doi:10.1002/jmor.1052100303 · Cited by 28 · see citing works
Homology between and Antiquity of Stereotyped Communicatory Behaviors of Crocodilians
Senter, P. (2008) · Journal of Herpetology · doi:10.1670/07-150.1 · Cited by 27 · see citing works
Der Kehlkopf der Amphibien und Reptilien
Göppert, E. (1898) · Cited by 25 · see citing works
Opening and closing mechanisms of the leatherback sea turtle larynx: a crucial role for the tongue
Fraher, J., Davenport, J., Fitzgerald, E. J., McLaughlin, P., Doyle, T. K., Harman, L. A., & Cuffe, T. (2010) · Journal of Experimental Biology · doi:10.1242/jeb.042218 · Cited by 17 · see citing works
Why do Chinese alligators (Alligator sinensis) form bellowing choruses: A playback approach
Wang, X., Wang, D., Zhang, S., Wang, C., Wang, R., & Wu, X. (2009) · The Journal of the Acoustical Society of America · doi:10.1121/1.3203667 · Cited by 13 · see citing works
Rittenhouse, D. R., Russell, A. P., & Bauer, A. M. (1998) · South African Journal of Zoology · doi:10.1080/02541858.1998.11448449 · Cited by 10 · see citing works
Sicuro, F. L., Ximenes, G. I., Wogel, H., & Bilate, M. (2013) · Revista de Biología Tropical · doi:10.15517/rbt.v61i3.11967 · Cited by 7 · see citing works
Bootz, F. (2014) · Springer eBooks · doi:10.1007/978-3-642-41866-2_273 · Cited by 6 · see citing works
Henle, F. G. J. (1939) · Cited by 3 · see citing works
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Titze, I. R., Riede, T., & Mau, T. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004907 · Cited by 103 · see citing works
Self-citationCilia-mediated Hedgehog signaling controls form and function in the mammalian larynx
Tabler, J. M., Rigney, M. M., Berman, G. J., Gopalakrishnan, S., Heude, É., Al-Lami, H. A., Yannakoudakis, B. Z., Fitch, R. D., Carter, C., Vokes, S. A., et al. (2017) · eLife · doi:10.7554/elife.19153 · Cited by 77 · see citing works
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Riede, T., Thomson, S. L., Titze, I. R., & Goller, F. (2019) · PLoS Biology · doi:10.1371/journal.pbio.2006507 · Cited by 69 · see citing works
Self-citationLessner, E. J., & Holliday, C. M. (2020) · The Anatomical Record · doi:10.1002/ar.24550 · Cited by 69 · see citing works
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Kingsley, E. P., Eliason, C. M., Riede, T., Li, Z., Hiscock, T. W., Farnsworth, M. S., Thomson, S. L., Goller, F., Tabin, C. J., & Clarke, J. A. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1804586115 · Cited by 60 · see citing works
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Farmer, C. G. (2015) · Integrative and Comparative Biology · doi:10.1093/icb/icv078 · Cited by 54 · see citing works
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Rico‐Guevara, A., Sustaita, D., Gussekloo, S. W. S., Olsen, A. M., Bright, J. A., Corbin, C. E., & Dudley, R. (2019) · Fascinating life sciences · doi:10.1007/978-3-030-13739-7_17 · Cited by 33 · see citing works
LI, Z., Ketcham, R. A., Yan, F., Maisano, J. A., & Clarke, J. A. (2016) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.22692 · Cited by 31 · see citing works
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Reber, S. A. (2018) · Springer eBooks · doi:10.1007/978-3-319-47829-6_950-1 · Cited by 3 · see citing works
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- Authors
- Riede, T., Li, Z., Tokuda, I. T., & Farmer, C. G.
- Affiliations
- Midwestern University (US)
- The University of Texas at Austin (US)
- Ritsumeikan University (JP)
- University of Utah (US)
- Corresponding author
- Riede, Tobias
- Venue
- Journal of Experimental Biology
- Publisher
- The Company of Biologists
- Published
- 2015-04-01
- Volume
- 218
- Issue
- 7
- Pages
- 991-998
- ISSN
- 0022-0949 (ISSN-L)
- 1477-9145
- OpenAlex
- W2162165024
- Cited by
- 38
- References
- 46
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 1 · 2023: 6 · 2022: 2 · 2021: 1 · 2020: 6 · 2019: 5 · 2018: 4 · 2017: 2 · 2016: 3 · 2015: 4
- FWCI
- 3.78
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Experimental Biology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Japan Society for the Promotion of Science (23300071)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Developmental Biology › Animal Vocal Communication and Behavior
- Health Sciences › Medicine › Urology › Comparative Animal Anatomy Studies
- Health Sciences › Medicine › Physiology › Voice and Speech Disorders
- Keywords
- Alligator mississippiensis, larynx, vocal fold histology, lamina propria, hyaluronic acid, extracellular matrix, vocal fold tension, stress-strain behavior, acoustic space, mating calls
- MeSH terms
- Alligators and Crocodiles, Animals, Biomechanical Phenomena, Computer Simulation, Female, Larynx, Male, Mucous Membrane, Vocal Cords, Vocalization, Animal
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