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

Dentition and tooth replacement of <i>Dicraeosaurus hansemanni</i> (Dinosauria, Sauropoda, Diplodocoidea) from the Tendaguru Formation of Tanzania

<div><p>ABSTRACT</p><p>Computed tomographic scan data of three premaxillae, a maxilla, and a dentary of <i>Dicraeosaurus hansemanni</i> allow reconstruction of the tooth replacement pattern in this taxon. Four or five replacement teeth are present in each of the four tooth families of the premaxilla. The interalveolar septum is labially interrupted, and an alveolar trough is formed. In the maxilla, the number of replacement teeth decreases in a caudal direction from four to one per tooth family. The dentary bears 16 alveoli, and the number of replacement teeth decreases caudally from three to one per tooth family. Replacement rates are around 20 days for the premaxillary and rostral maxillary teeth of <i>Dicraeosaurus</i>, which confirms the presence of high tooth replacement rates in Diplodocoidea. Replacement teeth of the dentary are less than half as large as those of the upper jaw, and replacement rates are around 50 days for the rostral dentary teeth. Hypothetical reconstruction of Zahnreihen yields a potential z-spacing of 1 with simultaneous front-to-back tooth replacement. Most probably, the rostral-most teeth in <i>Dicraeosaurus</i> were used for food acquisition, whereas the more caudally positioned teeth served only as a guide and as a lateral limit for the food within the mouth. The teeth of the dentary were less prone to wear than those of the upper jaws. These findings are in agreement with the reconstructions of <i>Dicraeosaurus</i> as a selective mid-height browser.</p><p>SUPPLEMENTAL DATA—Supplemental materials are available for this article for free at <a href="http://www.tandfonline.com/UJVP" target="_blank">www.tandfonline.com/UJVP</a></p><p>Citation for this article: Schwarz, D., J. C. D. Kosch, G. Fritsch, and T. Hildebrandt. 2015. Dentition and tooth replacement of <i>Dicraeosaurus hansemanni</i> (Dinosauria, Sauropoda, Diplodocoidea) from the Tendaguru Formation of Tanzania. Journal of Vertebrate Paleontology. DOI: 10.1080/02724634.2015.1008134 .</p></div

Hyoid apparatus (A) and laryngeal cartilages (B) of the dhole.

<p>(A) Excised hyoid apparatus and larynx; overlying muscles partly reconstructed on the basis of macroscopic dissection. The thyrohyoid 'articulation' is established by a cartilaginous connection. (B) Left half of hyoid apparatus and laryngeal cartilages. The interarytenoid cartilage is intercalated between left and right arytenoid cartilage. A sesamoid cartilage supports the transverse arytenoid muscles at their dorsomedian fusion along the transverse furrow between the corniculate and medial processes of the arytenoid cartilages. Colours in (A): green = M. cricopharyngeus; blue = M. thyropharyngeus; red = M. thyrohyoideus; orange = termination of M. sternothyroideus; yellow = termination of M. sternohyoideus. ** in (B): thyrohyoid connection. (A) and (B): Left lateral view. Scale bar = 10 mm, respectively.</p

Spectrogram illustrating the acoustic similarity between the high-frequency squeaks of a dhole (A) and the whistles of a human (B).

<p>(A) A natural series of a captive male dhole. (B) A natural series of an adult male zoo visitor, imitating the dhole calls (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0146330#pone.0146330.s004" target="_blank">S4 Audio</a>). A 5 kHz high-pass filter was applied to remove background noise. Spectrogram settings as in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0146330#pone.0146330.g001" target="_blank">Fig 1</a>.</p

Lateral laryngeal ventricle (A) and larynx (B) in red fox.

<p>(A) Artificially inflated pharynx and laryngeal ventricle after removal of the left half of the thyroid cartilage. The thyroarytenoid muscle is not divided into a rostral ventricularis and a caudal vocalis muscle. Its wider ventral portion covers the ‘neck’ of the laryngeal ventricle rostrally. (B) Mucous membrane relief of the larynx including the vocal and vestibular folds in the red fox. In (A): * = cricothyroid articulation; ** = temporomandibular articulation. Left lateral view; in (B): Mediosagittal section of pharynx and larynx of an unpreserved specimen, right half, medial view. Scale = 50 mm in (A) and (B), respectively.</p

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

Intrinsic laryngeal muscles of the dhole (A) and position of lateral laryngeal ventricle (B).

<p>(A) Larynx after removal of the left cricothyroid muscle and the left half of the thyroid cartilage. Dorsal and lateral cricoarytenoid muscles and thyroarytenoid muscle exposed. The thyroarytenoid muscle is not divided into a rostral ventricularis and a caudal vocalis muscle. (B) Larynx after removal of its intrinsic muscles. Reconstruction of the thyroarytenoid muscle (black line, shaded in translucent red) shows how its wider ventral portion covers the ventral end of the cuneiform process and the ‘neck’ of the laryngeal ventricle rostrally. Contour of the cuneiform process indicated by faint black line. The vocal ligament marks position and angle of the medially located vocal fold. (A) and (B): Left lateral view. Scale bar = 10 mm.</p

Spectrogram illustrating high-frequency and low-frequency vocalization modes in domestic dog (A), dhole (B) and red fox (C).

<p>(A) Dog (7-kg dachshund): left–low-frequency whine; middle–high-frequency squeak; right–biphonic whine-squeak (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0146330#pone.0146330.s001" target="_blank">S1 Audio</a>). (B) Dhole: left–low-frequency yap; middle–high-frequency squeak; right–biphonic yap–squeak (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0146330#pone.0146330.s002" target="_blank">S2 Audio</a>). (C) Red fox–low-frequency whine (<a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0146330#pone.0146330.s003" target="_blank">S3 Audio</a>). Designations: f0 –low fundamental frequency; f1 and f2 –harmonics of f0; g0 –high fundamental frequency; g0–f0 and g0+f0 –the linear combinations of f0 and g0. The spectrogram was created at 22050 Hz sampling frequency, Hamming window, FFT 1024, frame 50%, overlap 93.75%.</p