Bull bellows and bugles: a remarkable convergence of low and high-frequency vocalizations between male domestic cattle <i>Bos taurus</i> and the rutting calls of Siberian and North American wapiti

<p>Whereas low-frequency bellows (below 200 Hz) have been investigated in detail in both male and female domestic cattle (<i>Bos taurus</i>), male high-frequency bugle calls (over 800 Hz) have not been described so far in any large bovid species. In this study, high-frequency bugles and low-frequency bellows were recorded from three crossbred free-ranging domestic cattle bulls and analysed spectrographically. The maximum fundamental frequency of bellows was 113.6 Hz, whereas the maximum fundamental frequency of bugles was 958.4 Hz, ranging from 801 to 1125 Hz in different males. These amazingly high fundamental frequencies of bull bugles are comparable with those reported for Siberian wapiti <i>Cervus elaphus sibiricus</i>, but lower than reported values for some subspecies of North American wapiti <i>Cervus canadensis</i>. The similarity with both Siberian and North American wapiti was also observed in the production of bull biphonic bugles with two fundamental frequencies: the low and the high one. We suggest that bugles of domestic cattle bulls provide an excellent model for comparative research with cervid bugles concerning the mechanism of vocal production and the underlying anatomical and behavioural adaptations.</p

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

Koalas are characterised by a highly unusual vocal anatomy, with a descended larynx and velar vocal folds, allowing them to produce calls with 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. Second, three hyoid muscles have lost their connection to the hyoid skeleton. Third, the genioglossus and geniohyoid muscles have 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

Mucous membrane relief of the larynx including the vocal and vestibular folds in the dhole.

<p>The contour of the lateral laryngeal ventricle is indicated. The position of the ventricle is rostral to the vestibular fold and lateral to the cuneiform process. The red arrow points into the caudally directed entrance to the lateral laryngeal ventricle. Mediosagittal section of the formalin-fixed larynx of a two-years-old female, right half, medial view. White scale bar = 10 mm.</p

Extrinsic laryngeal muscles and ventral hyoid muscles of the dhole.

<p>The sternohyoid and sternothyroid muscles are fused between their joint origin from the sternal manubrium up to a tendinous inscription. At this point both muscles separate to reach their terminations on the basihyoid and on the thyroid cartilage, respectively. * = position of tendinous inscription. Left lateral view. Scale = 50 mm.</p

Gross morphology of the vocal apparatus, tongue and hyoid of an adult male dhole in near-natural position.

<p>Overlay reconstruction based on CT scans and macroscopic anatomical dissection. Skull, skeletal parts of the neck and thoracic inlet and contours of a typical head-and-neck posture of a live animal are provided in addition to facilitate an integrative view of the dhole vocal organs. Constrictor muscles of the pharynx removed. *** = lateral edge of neck musculature. Scale bar = 10 mm.</p

Potential Sources of High Frequency and Biphonic Vocalization in the Dhole (<i>Cuon alpinus</i>)

<div><p>Biphonation, i.e. two independent fundamental frequencies in a call spectrum, is a prominent feature of vocal activity in dog-like canids. Dog-like canids can produce a low (f0) and a high (g0) fundamental frequency simultaneously. In contrast, fox-like canids are only capable of producing the low fundamental frequency (f0). Using a comparative anatomical approach for revealing macroscopic structures potentially responsible for canid biphonation, we investigated the vocal anatomy for 4 (1 male, 3 female) captive dholes (<i>Cuon alpinus</i>) and for 2 (1 male, 1 female) wild red fox (<i>Vulpes vulpes</i>). In addition, we analyzed the acoustic structure of vocalizations in the same dholes that served postmortem as specimens for the anatomical investigation. All study dholes produced both high-frequency and biphonic calls. The anatomical reconstructions revealed that the vocal morphologies of the dhole are very similar to those of the red fox. These results suggest that the high-frequency and biphonic calls in dog-like canids can be produced without specific anatomical adaptations of the sound-producing structures. We discuss possible production modes for the high-frequency and biphonic calls involving laryngeal and nasal structures.</p></div

Right nasal cavity (A) and its flexible rostral portion (B) of an adult male dhole.

<p>(A) Middle nasal concha and nasal septum removed to expose the dorsal, the alar and the basal folds. ** = cut edge of the nasal septum. (B) Detail of (A). The arrow points to the flexible rostral portion of the nose, which can be variably constricted by differential action of the rostral nasal muscles. This will narrow particularly the space between the dorsal and the alar folds and, in concert with movements of the nostril wings, might influence nasal call characteristics. Mediosagittal section of the nasal region, right half, medial view. Scale bar = 10 mm in (A) and (B), respectively.</p

Intra-pharyngeal ostium in the dhole.

<p>During quiet respiration (not panting) and nasal call production the laryngeal entrance protrudes through the intra-pharyngeal ostium into the nasal portion of the pharynx. The intra-pharyngeal ostium is the sole connection between the ventral oral portion and the dorsal nasal portion of the pharynx. Mediosagittal section of pharynx and larynx of an unpreserved specimen, right half, medial view. Scale = 50 mm.</p

Mediosagittal section of the head and the region of the larynx of an adult male dhole.

<p>Illustrating the difference between nasal and oral vocal tract (vt) length including respective topographical relationships. The nasal vt is constantly longer than the oral vt in both adult male and adult female. The laryngeal entrance is depicted in a position for a nasal call. For production of an oral call, the soft palate is raised, the larynx slightly retracted and the epiglottis pulled ventrally to a position close to the root of the tongue, i.e. below the red line. Scale bar = 10 mm.</p