The roar of Rancho La Brea? Comparative anatomy of modern and fossil felid hyoid bones.
Panthera atrox
Smilodon fatalis
functional morphology
vocal apparatus
Journal
Journal of morphology
ISSN: 1097-4687
Titre abrégé: J Morphol
Pays: United States
ID NLM: 0406125
Informations de publication
Date de publication:
10 2023
10 2023
Historique:
revised:
11
07
2023
received:
19
05
2023
accepted:
18
07
2023
medline:
18
9
2023
pubmed:
14
9
2023
entrez:
14
9
2023
Statut:
ppublish
Résumé
Animal vocalization is broadly recognized as ecologically and evolutionarily important. In mammals, hyoid elements may influence vocalization repertoires because the hyoid apparatus anchors vocal tissues, and its morphology can be associated with variation in surrounding soft-tissue vocal anatomy. Thus, fossil hyoid morphology has the potential to shed light on vocalizations in extinct taxa. Yet, we know little about the hyoid morphology of extinct species because hyoid elements are rare in the fossil record. An exception is found in the Rancho La Brea tar pits in Los Angeles, California, where enough hyoids have been preserved to allow for quantitative analyses. The La Brea Tar Pits and Museum houses one of the largest and most diverse collections of carnivore fossils, including hyoid elements from the extinct felids Smilodon fatalis and Panthera atrox. Here, we found that extant members of Felinae (purring cats) and Panthera (roaring cats) showed characteristic differences in hyoid size and shape that suggest possible functional relationships with vocalization. The two extinct taxa had larger and more robust hyoids than extant felids, potentially reflecting the ability to produce lower frequency vocalizations as well as more substantial muscles associated with swallowing and respiration. Based on the shape of the hyoid elements, Panthera atrox resembled roaring cats, while Smilodon fatalis was quite variable and, contrary to suggestions from previous research, more similar overall to purring felids. Thus P. atrox may have roared and S. fatalis may have produced vocalizations similar to extant purring cats but at a lower frequency. Due to the confounding of vocalization repertoire and phylogenetic history in extant Felidae, we cannot distinguish between morphological signals related to vocalization behavior and those related to shared evolutionary history unrelated to vocalization.
Banques de données
Dryad
['10.5061/dryad.j6q573nkp']
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e21627Informations de copyright
© 2023 The Authors. Journal of Morphology published by Wiley Periodicals LLC.
Références
Arcadi, A. C., Robert, D., & Boesch, C. (1998). Buttress drumming by wild chimpanzees: Temporal patterning, phrase integration into loud calls, and preliminary evidence for individual distinctiveness. Primates, 39(4), 505-518. https://doi.org/10.1007/BF02557572
Assar, S., Durhman, M., Townsend, K. E. B., & Echols, M. S. (2021). Anatomy of the hyoid musculature in the snow leopard (Panthera uncia). The FASEB Journal, 35(S1), fasebj.2021.35.S1.02918. https://doi.org/10.1096/fasebj.2021.35.S1.02918
Barnett, R., Barnes, I., Phillips, M. J., Martin, L. D., Harington, C. R., Leonard, J. A., & Cooper, A. (2005). Evolution of the extinct sabretooths and the American cheetah-like cat. Current Biology, 15(15), R589-R590. https://doi.org/10.1016/j.cub.2005.07.052
Barnett, R., Shapiro, B., Barnes, I., Ho, S. Y. W., Burger, J., Yamaguchi, N., Higham, T. F. G., Wheeler, H. T., Rosendahl, W., Sher, A. V., Sotnikova, M., Kuznetsova, T., Baryshnikov, G. F., Martin, L. D., Harington, C. R., Burns, J. A., & Cooper, A. (2009). Phylogeography of lions (Panthera leo ssp.) reveals three distinct taxa and a late pleistocene reduction in genetic diversity. Molecular Ecology, 18(8), 1668-1677. https://doi.org/10.1111/j.1365-294X.2009.04134.x
Bergman, T. J., Cortés-Ortiz, L., Dias, P. A. D., Ho, L., Adams, D., Canales-Espinosa, D., & Kitchen, D. M. (2016). Striking differences in the loud calls of howler monkey sister species (Alouatta pigra and A. palliata). American Journal of Primatology, 78(7), 755-766. https://doi.org/10.1002/ajp.22539
Capasso, L., Michetti, E., & D'Anastasio, R. (2008). A homo erectus hyoid bone: possible implications for the origin of the human capability for speech. Collegium Antropologicum, 32(4), 1007-1011.
Christiansen, P. (2008). Phylogeny of the great cats (Felidae: Pantherinae), and the influence of fossil taxa and missing characters. Cladistics, 24(6), 977-992. https://doi.org/10.1111/j.1096-0031.2008.00226.x
Christiansen, P., & Harris, J. M. (2005). Body size of smilodon (Mammalia: Felidae). Journal of Morphology, 266(3), 369-384.
D'Anastasio, R., Wroe, S., Tuniz, C., Mancini, L., Cesana, D. T., Dreossi, D., Ravichandiran, M., Attard, M., Parr, W. C. H., Agur, A., & Capasso, L. (2013). Micro-biomechanics of the kebara 2 hyoid and its implications for speech in neanderthals. PLoS One, 8(12), e82261. https://doi.org/10.1371/journal.pone.0082261
Dickinson, E., Elminowski, E. E., Flores, D., Eldridge, E. I., Granatosky, M. C., & Hartstone-Rose, A. (2022). A morphological analysis of carnivoran ossicles from Rancho La Brea. Journal of Morphology, 283(10), 1337-1349. https://doi.org/10.1002/jmor.21506
Evans, H. E. (1959). Hyoid muscle anomalies in the dog (Canis familiaris). The Anatomical Record, 133(2), 145-162. https://doi.org/10.1002/ar.1091330204
Flores, D., Eldridge, E. I., Elminowski, E. E., Dickinson, E., & Hartstone-Rose, A. (2020). The howl of Rancho La Brea: comparative anatomy of modern and fossil canid hyoid bones. Journal of Morphology, 281, 646-652. https://doi.org/10.1002/jmor.21130
Hartstone-Rose, A., Dundas, R. G., Boyde, B., Long, R. C., Farrell, A., & Shaw, C. A. (2015). The bacula of Rancho La Brea. Natural History Museum of Los Angeles County Contributions in Science, 42, 53-63.
Hartstone-Rose, A., Long, R. C., Farrell, A. B., & Shaw, C. A. (2012). The clavicles of smilodon fatalis and panthera atrox (Mammalia: Felidae) from Rancho La Brea, Los Angeles, California. Journal of Morphology, 273, 981-991. https://doi.org/10.1002/jmor.20036
Hast, M. H. (1986). The larynx of roaring and non-roaring cats. Journal of Anatomy, 149, 221-222.
Hast, M. H. (1989). The larynx of roaring and non-roaring cats. Journal of Anatomy, 163, 117-121.
Humphries, J. M., Bookstein, F. L., Chernoff, B., Smith, G. R., Elder, R. L., & Poss, S. G. (1981). Multivariate discrimination by shape in relation to size. Systematic Biology, 30(3), 291-308. https://doi.org/10.1093/sysbio/30.3.291
Ji, A., Johnson, M. T., Walsh, E. J., McGee, J., & Armstrong, D. L. (2013). Discrimination of individual tigers (Panthera Tigris) from long distance roars. The Journal of the Acoustical Society of America, 133(3), 1762-1769. https://doi.org/10.1121/1.4789936
King, L. M., & Wallace, S. C. (2014). Phylogenetics of panthera, including panthera atrox, based on craniodental characters. Historical Biology, 26(6), 827-833. https://doi.org/10.1080/08912963.2013.861462
Koukouvinis, P., Bruecker, C., & Gavaises, M. (2017). Unveiling the physical mechanism behind pistol shrimp cavitation. Scientific Reports, 7(1), 13994. https://doi.org/10.1038/s41598-017-14312-0
Lieberman, P., Laitman, J. T., Reidenberg, J. S., & Gannon, P. J. (1992). The anatomy, physiology, acoustics, and perception of speech-essential elements in analysis of the evolution of human speech. Journal of Human Evolution, 23(6), 447-467. https://doi.org/10.1016/0047-2484(92)90046-c
van Lunteren, E., Haxhiu, M. A., & Cherniack, N. S. (1987a). Mechanical function of hyoid muscles during spontaneous breathing in cats. Journal of Applied Physiology (1985), 62(2), 582-590. https://doi.org/10.1152/jappl.1987.62.2.582
van Lunteren, E., Haxhiu, M. A., & Cherniack, N. S. (1987b). Relation between upper airway volume and hyoid muscle length. Journal of Applied Physiology (1985), 63(4), 1443-1449. https://doi.org/10.1152/jappl.1987.63.4.1443
Merriam, J. C., & Stock, C. (1932). The Felidae of Rancho La Brea (p. 231). Carnegie institution of Washington.
Milovancev, M., Wilson, D. M., Monnet, E., & Seguin, B. (2014). Partial resection of the hyoid apparatus during surgical treatment of ectopic thyroid carcinomas in dogs: 5 cases (2011-2013). Journal of the American Veterinary Medical Association, 244(11), 1319-1324.
Murray, J. L., & Gardner, G. L. (1997). Leopardus pardalis. Mammalian Species, 548, 1-10. https://doi.org/10.2307/3504082
Norris, K. S., & Evans, E. C. (1988). On the evolution of acoustic communication systems in vertebrates. In P. E. Nachtigall, & P. W. B. Moore (Eds.), Animal sonar: Processes and performance (pp. 655-669). Springer US.
Owen, R. (1834). On the anatomy of the cheetah, Felis jubata, Schreb. The Transactions of the Zoological Society of London, 1, 129-136.
Pecon-Slattery, J., Pearks Wilkerson, A. J., Murphy, W. J., & O'Brien, S. J. (2004). Phylogenetic assessment of introns and SINEs within the Y chromosome using the cat family felidae as a species tree. Molecular Biology and Evolution, 21(12), 2299-2309. https://doi.org/10.1093/molbev/msh241
Pérez, L. M., Toledo, N., De Iuliis, G., Bargo, M. S., & Vizcaíno, S. F. (2010). Morphology and function of the hyoid apparatus of fossil xenarthrans (Mammalia). Journal of Morphology, 271(9), 1119-1133. https://doi.org/10.1002/jmor.10859
Peters, G. (1978). Vergleichende untersuchung zur lautgebung einiger feliden (Mammalia, felidae). Spixiana Journal of Zoology, Supp 1, 1-206.
Peters, G. (1983). Beobachtungen zum lautgebungsverhalten des karakal, Caracal caracal (Schreber, 1776) (Mammalia, Carnivora, Felidae). Bonner zoologische Beiträge, 34(1-3), 107.
Peters, G. (2002). Purring and similar vocalizations in mammals. Mammal Review, 32(4), 245-271. https://doi.org/10.1046/j.1365-2907.2002.00113.x
Peters, G., & Hast, M. H. (1994). Hyoid structure, laryngeal anatomy, and vocalization in felids (Mammalia: Carnivora: Felidae). Zeitschrift fur Saugetierkunde, 59(2), 87-104.
Pocock, R. I. (1916). XXII.-On the hyoidean apparatus of the lion (F. leo) and related species of felidae. Annals and Magazine of Natural History, 18(104), 222-229.
Quinn, J. P., Heath, E. G., & Lewis, W. L. (1992). Rancho La Brea: Geologic setting, late Quaternary depositional patterns and mode of fossil accumulation. In E. G. Heaph, & W. L. Lewis (Eds.), The regressive pleistocene shoreline, Southern California: South coast geological society guidebook (pp. 221-232). Santa Ana.
Schaller, G. E. (1963). The mountain gorilla: Ecology and behavior. Univer., Chicago Press.
Schultz, N. G., Lough-Stevens, M., Abreu, E., Orr, T., & Dean, M. D. (2016). The baculum was gained and lost multiple times during mammalian evolution. Integrative and comparative biology, 56(4), 644-656. https://doi.org/10.1093/icb/icw034
Searcy, W., & Nowicki, S. (2005). The Evolution of Animal Communication: Reliability and Deception in Signaling Systems (Vol. 56).
Shaw, C. A. (1982). Techniques used in excavation, preparation, and curation of fossils from Rancho La Brea. Curator: The Museum Journal, 25(1), 63-77. https://doi.org/10.1111/j.2151-6952.1982.tb00583.x
Shaw, C. A. (2018). Implied vocalization based on the morphology of the hyoid apparatus in the sabertoothed cat, Smilodon fatalis (mammalia, felidae, machaerodontinae) from Rancho La Brea, Los Angeles, California. Paper presented at the Society of Vertebrate Paleontology, Albuquerque, NM.
Shaw, C. A., Kunitomi, D. S., Mulqueen, S. P., & Hesson, B. H. (2007). The history, geology and paleontology of the La Brea tar pits. In D. S. Kunitomi, S. P. Mulqueen, & B. H. Hesson (Eds.), (pp. 1-9). National AAPG Convention.
Shaw, C. A., & Quinn, J. P. (1986). Rancho La Brea: A look at coastal Southern California's past. California. Geology, 39(6), 123-133.
Sissom, D. E. F., Rice, D. A., & Peters, G. (1991). How cats purr. Journal of Zoology, 223(1), 67-78. https://doi.org/10.1111/j.1469-7998.1991.tb04749.x
Tecumseh Fitch, W., & Reby, D. (2001). The descended larynx is not uniquely human. Proceedings of the Royal Society of London. Series B: Biological Sciences, 268(1477), 1669-1675. https://doi.org/10.1098/rspb.2001.1704
Thexton, A. J., & McGarrick, J. D. (1994). The electromyographic activities of jaw and hyoid musculature in different ingestive behaviours in the cat. Archives of Oral Biology, 39(7), 599-612.
Titze, I., Riede, T., & Mau, T. (2016). Predicting achievable fundamental frequency ranges in vocalization across species. PLoS Computational Biology, 12(6), e1004907. https://doi.org/10.1371/journal.pcbi.1004907
Venables, W. N., & Ripley, B. D. (2002). Modern applied statistics with S (fourth ed.). Springer.
Weissengruber, G. E., Forstenpointner, G., Peters, G., Kubber-Heiss, A., & Fitch, W. T. (2002). Hyoid apparatus and pharynx in the lion (Panthera leo), jaguar (Panthera onca), tiger (Panthera Tigris), cheetah (Acinonyx jubatus) and domestic cat (Felis silvestris f. catus). Journal of Anatomy, 201(3), 195-209. https://doi.org/10.1046/j.1469-7580.2002.00088.x
Werdelin, L., McDonald, H. G., & Shaw, C. A. (2018). Smilodon: The iconic sabertooth. Johns Hopkins University Press.
Wheeler, H. T., & Jefferson, G. T. (2009). Panthera atrox: body proportions, size, sexual dimorphism, and behavior of the cursorial lion of the North American plains. papers on geology, vertebrate paleontology, and biostratigraphy in honor of michael O Woodburn. Museum of Northern Arizona Bulletin, 65, 423-444.
Wiegand, D. A., & Latz, B. (1991). Effect of geniohyoid and sternohyoid muscle contraction on upper airway resistance in the cat. Journal of Applied Physiology, 71(4), 1346-1354. https://doi.org/10.1152/jappl.1991.71.4.1346
Zhu, M. (2014). Bone gain and loss: insights from genomes and fossils. National Science Review, 1(4), 490-492. https://doi.org/10.1093/nsr/nwu062