Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2018 Apr;232(4):575-595.
doi: 10.1111/joa.12770. Epub 2018 Feb 19.

The remarkable vocal anatomy of the koala (Phascolarctos cinereus): insights into low-frequency sound production in a marsupial species

Affiliations

The remarkable vocal anatomy of the koala (Phascolarctos cinereus): insights into low-frequency sound production in a marsupial species

Roland Frey et al. J Anat. 2018 Apr.

Abstract

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-like 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-and-up 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-pharyngeal ostium have specialised to form the novel, extra-laryngeal velar vocal folds, which are much larger than the true intra-laryngeal 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.

Keywords: bellow vocalisation; descended larynx; extra-laryngeal velar vocal folds; intra-thoracic sternohyoid and sternothyroid muscles; laryngeal vocal folds; marsupials; mating calls; sexual selection.

PubMed Disclaimer

Figures

Figure 1
Figure 1
Two‐stage calling posture of an adult male koala while producing a bellow vocalisation. Initial stretched posture, head, neck, and thorax extended (A); flexed posture towards the end of the call, head angled, neck and thorax less extended (B). Landmarks used for the red longitudinal head line are the mouth opening and the visible ear base, which is close to the atlantooccipital articulation. Landmarks used for the red longitudinal body line are the visible ear base and (less reliable) the assumed position of the cranial edge of the pelvis. In (A) the head line is in straight continuation of the body line (modified from Charlton et al. 2011a,2011b)
Figure 2
Figure 2
Initial calling posture and full larynx retraction demonstrated by a CT‐based 3D reconstruction of the skeleton in an adult male specimen. Prior to CT scanning, the larynx had been externally fixed in a maximally retracted position. Left lateral view.
Figure 3
Figure 3
The nasal cavity of an adult male koala. 3D reconstruction of the skeleton of the upper body; left foreleg, clavicle and shoulder removed; virtual sagittal section of the skull and lower jaw; background: a photo of the same specimen. Tongue, soft palate and hyoid ligament manually reconstructed for full larynx retraction. Left lateral view. Note the presence of a small rostral bone riding on the incisive bone and lending support to the tip of the nose (similar to European wild boar, Sus scrofa).
Figure 4
Figure 4
Fully extended pharynx in an adult male koala. Multi Planar Reconstruction (MPR) based on a CT scan of an adult male, in which the larynx had been externally pushed back and fixed to simulate maximal larynx retraction. The ventral parts of the hyoid apparatus and the larynx are located at the thoracic inlet. Note the capacious naso‐ and oropharynx and the long soft palate. The IPO (indicated by the red ellipse) is also situated far caudally, opposite the laryngeal entrance.
Figure 5
Figure 5
Dissection stage at which full retraction of the ventral hyoid parts and the larynx down into the thoracic inlet were simulated. Maximal extension of the pharynx; the hyoid ligament, and the genioglossolaryngeal muscle are exposed. Scale bar: 10 mm.
Figure 6
Figure 6
The excised soft palate of an adult male koala: dorsal view with part of right lateral wall of nasopharynx (A), and ventral view (B). A prominent feature of the dorsal surface is the narrow median trench passing caudally into the IPO. A prominent feature of the ventral surface is the IPO with the large VVFs protruding into the laryngopharynx. The asterisk marks a steel pin inserted into the right blind space lateral to the VVFs. Scale bar: 10 mm.
Figure 7
Figure 7
Upper panel: Histological sections of the male VVFs. The cornifying stratified squamous epithelium and the underlying, parallel network of elastic fibres (black) and collagenous fibres (pink) of the upper intermediate layer (A); high density of thicker bundles of collagenous fibres in the lower intermediate layer (B); longitudinally oriented large bundle of elastic fibres, parallel to the free edge of the VVFs in the lower intermediate layer (C); longitudinal muscle fibre bundles of the deep layer near the laterodorsal base of the VVFs (D). (A, B, D) Transverse sections, (C) sagittal section. (A, C, D) Elastica van Gieson staining, (D) Masson/Goldner Trichrome staining. In each sub‐figure the arrow points towards the highlighted feature. Lower panel: Histological sections of the female VVFs. The cornifying stratified squamous epithelium and the upper intermediate layer of collagenous and elastic fibres (A). the mostly longitudinally arranged muscle fibre bundles, collagenous and elastic fibres inside the VVF stand out against the mostly transversely oriented thick muscular bundles of the soft palate in the region of the VVFs (B). Detail of the deepest layer of the VVF (C), illustrating the scaffolding of collagenous and elastic fibres interspersed with muscle fibre bundles and mucinous glands; soft palate immediately caudal to the VVFs containing transversely arranged larger bundles of elastic fibres (D). (A, D) Transverse sections; (B, C) sagittal sections. (A, B, C, D) Elastica van Gieson staining. In each sub‐figure the arrow points towards the highlighted feature.
Figure 8
Figure 8
CT‐based 3D reconstruction of the hyoid apparatus in an adult male koala. The position of the left hyoid ligament is indicated by the yellow bar. The left clavicle, ribs and shoulder girdle have been removed virtually to expose the in situ position of the hyoid apparatus and larynx. The white asterisk marks the cartilaginous connection between the hyoid apparatus and the larynx. The black asterisk marks the cartilaginous longitudinal ventral fusion of thyroid and cricoid cartilages that is typical for marsupials. The resting position of the larynx is approximately at the level of the cervical vertebrae 4–6.
Figure 9
Figure 9
Superficial muscular triangle covering the ventrolateral neck region, consisting of the two bellies of the digastric muscle rostrally, the sternohyoid muscle ventrally, and the V‐shaped omohyoid muscle laterally. A tendinous intersection links these three muscles. Position of lower jaw indicated by white contour. In the koala, the omohyoid and sternohyoid muscles have completely lost their connection to the hyoid apparatus. The three muscles are laterally flanking the pharynx, the ventral hyoid parts, the larynx, trachea and oesophagus. Scale bar: 10 mm.
Figure 10
Figure 10
Intra‐thoracic origin of the sternohyoid and sternothyroid (strap) muscles in a female (A) and a male (B) adult koala. (A) Resting position of the larynx. (B) The neck has been extended and the larynx pulled caudally (red arrows) to simulate its retraction down into the thoracic entrance. The origins of the two muscles extend down to the level of the 3rd and 4th costal cartilage. The sternohyoid muscle courses ventrally, contacting the inner thoracic wall, and is covered dorsally by the sternothyroid muscle. In situ, the intrathoracic portions of both muscles are covered by a sheath of connective tissue. The sternothyroid muscle is the main retractor of the larynx and the sternohyoid muscle, due to its tendinous connection to the digastric and omohyoid muscles, guides the extensive up‐and‐down movements of the larynx, the ventral hyoid parts and the pharynx during bellow production. Scale bars: 10 mm.
Figure 11
Figure 11
The hyocephalic muscle in an adult female koala. Left lateral view. The hyocephalic muscle (probably emerging from the fusion of the stylohyoid muscle rostrally, the caudal stylopharyngeal muscle (middle), and the hyopharyngeal muscle caudally) originates from the cerato‐, basi‐ and thyrohyoid and rostrodorsally from the thyroid cartilage, and mainly terminates on the base of the skull, caudally adjacent to the attachment of the hyoid ligament. As a result of this topographical relationships, the hypocephalic muscle can assist in protraction of the larynx subsequent to momentary retraction during bellow production. Scale bar: 10 mm.
Figure 12
Figure 12
Right half of the larynx of an adult male koala (A) and an adult female koala (B). Medial view. Dissection photo, showing the mucous membrane relief of the laryngeal cavity, including the laryngeal vocal fold (LVF), and the relative positions of the laryngeal cartilages. The thyroid and cricoid cartilages are ventrally fused by a longitudinal cartilaginous keel (A). Translucent specimen (B) prepared by using the Spalteholz technique (Spalteholz, 1914; Peters, 1961; Piechocki, 1967). +, rostral horn; o,  caudal horn of thyroid cartilage; *, fusion of thyroid and cricoid cartilage. Scale bars: 10 mm.
Figure 13
Figure 13
Undulating nerves supplying the musculature of the pharynx, which is subjected to considerable length changes during extensive rostrocaudal excursions of the ventral hyoid parts and the larynx. The undulating nerve branches are ensheathed by flexible hose‐like connective tissue tubes (three red arrows), which facilitate stretching and rewinding. Asterisks mark two steel pins used for separating the nerves. Left lateral view. Scale bar: 10 mm.
Figure 14
Figure 14
Reconstruction of the vocal anatomy of an adult male koala in six layers while producing the very low frequencies during the nasal inhalatory sections of the final stage of bellow vocalisations. The larynx is maximally retracted down into the thoracic inlet; the hyoid ligament is maximally extended and the sternothyroid muscle maximally contracted. Left lateral view. Parotidoauricularis muscle terminates on sternal manubrium (A); Y‐shaped tendinous intersection connects digastric, omohyoid and sternohyoid muscle, the latter with intrathoracic origin (B); the genioglossolaryngeal muscle terminates on pharynx wall, thyrohyoid and thyrohyoid membrane (C); the geniohyoid muscle is markedly elongated and kept in place by passing through an arch formed by the hyoglossus muscle and the rostral branch of the Y‐shaped tendinous intersection; the stylohyoid muscle connects the thyrohyoid to the skull base; the sternothyroid muscle has an intrathoracic origin (D); the hyopharyngeus muscle and the caudal constrictors of the pharynx connect the thyrohyoid and the larynx to the pharynx; first and second rib removed (E); nasal and oral vocal tract, naso‐ and oropharynx and soft palate maximally extended; VVFs opposite to the laryngeal entrance; complete (longitudinally compressed) trachea from the larynx to the bifurcation; first rib removed (F).

Similar articles

Cited by

References

    1. Allen CD, de Villiers DL, Manning BD, et al. (2010) Seasonal reproduction in wild and captive male koala (Phascolarctos cinereus) populations in south‐east Queensland. Reprod Fertil 22, 695–709. - PubMed
    1. Berillis P (2013) The role of collagen in the aorta's structure. Open Circ Vasc J 6, 1–8.
    1. Chan RW, Fu M, Young L, et al. (2007) Relative contributions of collagen and elastin to elasticity of the vocal fold under tension. Ann Biomed Eng 35, 1471–1483. - PubMed
    1. Charlton B (2015) The acoustic structure and information content of female koala vocal signals. PLoS ONE 10, e0138670. - PMC - PubMed
    1. Charlton BD, Ellis WAH, McKinnon AJ, et al. (2011a) Perception of male caller identity in koalas (Phascolarctos cinereus): acoustic analysis and playback experiments. PLoS ONE 6, e20329. - PMC - PubMed

Publication types

MeSH terms

LinkOut - more resources