{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,17]],"date-time":"2026-09-17T16:37:42Z","timestamp":1789663062054,"version":"4.0.1"},"reference-count":63,"publisher":"Wiley","issue":"4","license":[{"start":{"date-parts":[[2018,2,19]],"date-time":"2018-02-19T00:00:00Z","timestamp":1518998400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/onlinelibrary.wiley.com\/termsAndConditions#vor"}],"funder":[{"DOI":"10.13039\/501100000275","name":"Leverhulme Trust","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100000275","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["onlinelibrary.wiley.com"],"crossmark-restriction":true},"short-container-title":["Journal of Anatomy"],"published-print":{"date-parts":[[2018,4]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Koalas are characterised by a highly unusual vocal anatomy, with a descended larynx and velar vocal folds, allowing them to produce calls at disproportionately low frequencies. Here we use advanced imaging techniques, histological data, classical macroscopic dissection and behavioural observations to provide the first detailed description and interpretation of male and female koala vocal anatomy. We show that both males and females have an elongated pharynx and soft palate, resulting in a permanently descended larynx. In addition, the hyoid apparatus has a human\u2010like configuration in which paired dorsal, resilient ligaments suspend the hyoid apparatus from the skull, while the ventral parts tightly connect to the descended larynx. We also show that koalas can retract the larynx down into the thoracic inlet, facilitated by a dramatic evolutionary transformation of the ventral neck muscles. First, the usual retractors of the larynx and the hyoid have their origins deep in the thorax. Secondly, three hyoid muscles have lost their connection to the hyoid skeleton. Thirdly, the genioglossus and geniohyoid muscles are greatly increased in length. Finally, the digastric, omohyoid and sternohyoid muscles, connected by a common tendinous intersection, form a guiding channel for the dynamic down\u2010and\u2010up movements of the ventral hyoid parts and the larynx. We suggest that these features evolved to accommodate the low resting position of the larynx and assist in its retraction during call production. We also confirm that the edges of the intra\u2010pharyngeal ostium have specialised to form the novel, extra\u2010laryngeal velar vocal folds, which are much larger than the true intra\u2010laryngeal vocal folds in both sexes, but more developed and specialised for low frequency sound production in males than in females. Our findings illustrate that strong selection pressures on acoustic signalling not only lead to the specialisation of existing vocal organs but can also result in the evolution of novel vocal structures in both sexes.<\/jats:p>","DOI":"10.1111\/joa.12770","type":"journal-article","created":{"date-parts":[[2018,2,21]],"date-time":"2018-02-21T18:37:00Z","timestamp":1519238220000},"page":"575-595","update-policy":"https:\/\/doi.org\/10.1002\/crossmark_policy","source":"Crossref","is-referenced-by-count":15,"title":["The remarkable vocal anatomy of the koala (<i>Phascolarctos cinereus<\/i>): insights into low\u2010frequency sound production in a marsupial species"],"prefix":"10.1111","volume":"232","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6759-761X","authenticated-orcid":false,"given":"Roland","family":"Frey","sequence":"first","affiliation":[{"name":"Leibniz Institute for Zoo and Wildlife Research (IZW) Berlin Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David","family":"Reby","sequence":"additional","affiliation":[{"name":"School of Psychology University of Sussex Brighton UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guido","family":"Fritsch","sequence":"additional","affiliation":[{"name":"Leibniz Institute for Zoo and Wildlife Research (IZW) Berlin Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Benjamin D.","family":"Charlton","sequence":"additional","affiliation":[{"name":"Behavioural Ecology Research Group Department of Biology Anglia Ruskin University Cambridge UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"311","published-online":{"date-parts":[[2018,2,19]]},"reference":[{"key":"e_1_2_7_2_1","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1071\/RD09113","article-title":"Seasonal reproduction in wild and captive male koala (Phascolarctos cinereus) populations in south\u2010east Queensland","volume":"22","author":"Allen CD","year":"2010","journal-title":"Reprod Fertil"},{"key":"e_1_2_7_3_1","doi-asserted-by":"publisher","DOI":"10.2174\/1877382601306010001"},{"key":"e_1_2_7_4_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10439-007-9314-x"},{"key":"e_1_2_7_5_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0138670"},{"key":"e_1_2_7_6_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0020329"},{"key":"e_1_2_7_7_1","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.061358"},{"key":"e_1_2_7_8_1","doi-asserted-by":"publisher","DOI":"10.1007\/s10071-012-0527-5"},{"key":"e_1_2_7_9_1","doi-asserted-by":"crossref","first-page":"e45420","DOI":"10.1371\/journal.pone.0045420","article-title":"Estimating the\u00a0active space of male koala bellows: propagation of cues to size and identity in a Eucalyptus forest","volume":"7","author":"Charlton BD","year":"2012","journal-title":"PLoS ONE"},{"key":"e_1_2_7_10_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.anbehav.2012.09.034"},{"key":"e_1_2_7_11_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.cub.2013.10.069"},{"key":"e_1_2_7_12_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pone.0070279"},{"key":"e_1_2_7_13_1","doi-asserted-by":"publisher","DOI":"10.1148\/rg.233025079"},{"key":"e_1_2_7_14_1","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1007\/978-3-211-88729-5","volume-title":"Dynamics of the Singing Voice","author":"Dayme MB","year":"2009"},{"key":"e_1_2_7_15_1","first-page":"352","volume-title":"The Functional Unity of the Singing Voice","author":"Doscher B","year":"1994"},{"key":"e_1_2_7_16_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00265-010-1136-4"},{"key":"e_1_2_7_17_1","doi-asserted-by":"publisher","DOI":"10.1007\/s00265-009-0761-2"},{"key":"e_1_2_7_18_1","doi-asserted-by":"publisher","DOI":"10.1093\/beheco\/arq216"},{"key":"e_1_2_7_19_1","volume-title":"Acoustic Theory of Speech Production","author":"Fant G","year":"1960"},{"key":"e_1_2_7_20_1","doi-asserted-by":"publisher","DOI":"10.1016\/0014-4800(80)90003-9"},{"key":"e_1_2_7_21_1","doi-asserted-by":"publisher","DOI":"10.1017\/CBO9780511817779"},{"key":"e_1_2_7_22_1","doi-asserted-by":"publisher","DOI":"10.1098\/rspb.2001.1704"},{"key":"e_1_2_7_23_1","first-page":"383","volume-title":"An Introduction to the Osteology of the Mammalia. Marsupial Hyoids, 238\u2013241 including 3 figures","author":"Flower WH","year":"1885"},{"key":"e_1_2_7_24_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-7580.2007.00818.x"},{"key":"e_1_2_7_25_1","doi-asserted-by":"publisher","DOI":"10.1002\/jmor.10656"},{"key":"e_1_2_7_26_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-7580.2011.01361.x"},{"key":"e_1_2_7_27_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-7580.2011.01467.x"},{"key":"e_1_2_7_28_1","doi-asserted-by":"publisher","DOI":"10.1126\/science.1219712"},{"key":"e_1_2_7_29_1","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.091009"},{"key":"e_1_2_7_30_1","first-page":"1","volume-title":"Speech Science","author":"Hirano M","year":"1985"},{"key":"e_1_2_7_31_1","first-page":"33","volume-title":"Vocal Fold Physiology","author":"Hirano M","year":"1981"},{"key":"e_1_2_7_32_1","doi-asserted-by":"publisher","DOI":"10.1002\/ajpa.22124"},{"key":"e_1_2_7_33_1","first-page":"3","volume-title":"Vocal Fold Physiology: Contemporary Research and Clinical Issues","author":"Kurita S","year":"1983"},{"key":"e_1_2_7_34_1","first-page":"), 740","volume-title":"Fauna of Australia","author":"Lee AK","year":"1989"},{"key":"e_1_2_7_35_1","doi-asserted-by":"publisher","DOI":"10.1016\/S0003-9969(00)00108-4"},{"key":"e_1_2_7_36_1","doi-asserted-by":"publisher","DOI":"10.1080\/00222937208696658"},{"key":"e_1_2_7_37_1","volume-title":"The Koala: Natural History, Conservation and Management","author":"Martin R","year":"1999"},{"key":"e_1_2_7_38_1","first-page":"198","volume-title":"Koala, Phascolarctos cinereus. In: The Mammals of Australia","author":"Martin R","year":"2008"},{"key":"e_1_2_7_39_1","doi-asserted-by":"crossref","first-page":"232","DOI":"10.1071\/AM15038","article-title":"Velar vocal folds are present in female and immature male koalas (Phascolarctos cinereus)","volume":"38","author":"McCurry MR","year":"2016","journal-title":"Aust Mammal"},{"key":"e_1_2_7_40_1","doi-asserted-by":"publisher","DOI":"10.1111\/j.1469-7998.2006.00144.x"},{"key":"e_1_2_7_41_1","first-page":"151","volume-title":"Biology of the Koala","author":"Mitchell P","year":"1990"},{"key":"e_1_2_7_42_1","volume-title":"Nomina Anatomica Veterinaria","author":"NAV","year":"2005"},{"key":"e_1_2_7_43_1","volume-title":"Nomina Anatomica Veterinaria","author":"NAV","year":"2012"},{"key":"e_1_2_7_44_1","doi-asserted-by":"publisher","DOI":"10.1007\/BF02118851"},{"key":"e_1_2_7_45_1","doi-asserted-by":"publisher","DOI":"10.1007\/978-1-4757-6814-5"},{"key":"e_1_2_7_46_1","doi-asserted-by":"publisher","DOI":"10.2214\/AJR.05.1066"},{"key":"e_1_2_7_47_1","first-page":"233","article-title":"Methoden zur Herstellung von Aufhellungspr\u00e4paraten","volume":"167","author":"Peters W","year":"1961","journal-title":"Zool Anz"},{"key":"e_1_2_7_48_1","unstructured":"PiechockiR(1967)Makroskopische Pr\u00e4parationstechnik. Teil I Wirbeltiere. 2. \u00fcberarbeitete und erg\u00e4nzte Auflage. X. Herstellung von Aufhellungspr\u00e4paraten pp.305\u2013346.Leipzig:Akademische Verlagsgesellschaft Geest & Portig."},{"key":"e_1_2_7_49_1","doi-asserted-by":"publisher","DOI":"10.1242\/jeb.131219"},{"key":"e_1_2_7_50_1","doi-asserted-by":"publisher","DOI":"10.2214\/AJR.05.0764"},{"key":"e_1_2_7_51_1","doi-asserted-by":"publisher","DOI":"10.1016\/j.anbehav.2006.08.005"},{"key":"e_1_2_7_52_1","first-page":"620","volume-title":"Illustrated Veterinary Anatomical Nomenclature","author":"Schaller O","year":"2012"},{"key":"e_1_2_7_53_1","first-page":"1","volume-title":"Handbuch der Zoologie \u2013 eine Naturgeschichte der St\u00e4mme des Tierreiches","author":"Schneider R","year":"1964"},{"key":"e_1_2_7_54_1","doi-asserted-by":"publisher","DOI":"10.1071\/WR9800013"},{"key":"e_1_2_7_55_1","doi-asserted-by":"crossref","first-page":"547","DOI":"10.1111\/j.1096-3642.1921.tb03280.x","article-title":"The comparative anatomy of the koala (Phascolarctos cinereus) and vulpine phalanger (Trichosurus vulpecula)","volume":"39","author":"Sonntag CF","year":"1921","journal-title":"Proc Zool Soc London"},{"key":"e_1_2_7_56_1","first-page":"863","article-title":"On the myology and classification of the wombat, koala, and phalangers","volume":"1922","author":"Sonntag CF","year":"1922","journal-title":"Proc Zool Soc London"},{"key":"e_1_2_7_57_1","first-page":"93","volume-title":"\u00dcber das Durchsichtigmachen von menschlichen und tierischen Pr\u00e4paraten","author":"Spalteholz W","year":"1914"},{"key":"e_1_2_7_58_1","first-page":"31","article-title":"The marsupial larynx","volume":"33","author":"Symington J","year":"1898","journal-title":"J Anat Physiol"},{"key":"e_1_2_7_59_1","doi-asserted-by":"crossref","first-page":"229","DOI":"10.1007\/978-3-319-27721-9_8","volume-title":"Vertebrate Sound Production and Acoustic Communication","author":"Taylor AM","year":"2016"},{"key":"e_1_2_7_60_1","first-page":"354","volume-title":"Principles of Voice Production","author":"Titze IR","year":"1994"},{"key":"e_1_2_7_61_1","doi-asserted-by":"publisher","DOI":"10.1371\/journal.pcbi.1004907"},{"key":"e_1_2_7_62_1","doi-asserted-by":"publisher","DOI":"10.1071\/9780643092204"},{"key":"e_1_2_7_63_1","first-page":"466","article-title":"Anatomy of the koala (Phascolarctos cinereus)","volume":"15","author":"Young AH","year":"1881","journal-title":"J Anat Physiol"},{"key":"e_1_2_7_64_1","first-page":"217","article-title":"The muscular anatomy of the koala (Phascolarctos cinereus), with additional notes","volume":"16","author":"Young AH","year":"1882","journal-title":"J Anat Physiol"}],"container-title":["Journal of Anatomy"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/api.wiley.com\/onlinelibrary\/tdm\/v1\/articles\/10.1111%2Fjoa.12770","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/pdf\/10.1111\/joa.12770","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,9,25]],"date-time":"2023-09-25T10:42:10Z","timestamp":1695638530000},"score":1,"resource":{"primary":{"URL":"https:\/\/onlinelibrary.wiley.com\/doi\/10.1111\/joa.12770"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,2,19]]},"references-count":63,"journal-issue":{"issue":"4","published-print":{"date-parts":[[2018,4]]}},"alternative-id":["10.1111\/joa.12770"],"URL":"https:\/\/doi.org\/10.1111\/joa.12770","archive":["Portico"],"relation":{},"ISSN":["0021-8782","1469-7580"],"issn-type":[{"value":"0021-8782","type":"print"},{"value":"1469-7580","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,2,19]]},"assertion":[{"value":"2017-12-05","order":1,"name":"accepted","label":"Accepted","group":{"name":"publication_history","label":"Publication History"}},{"value":"2018-02-19","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}