Figure 5 - uploaded by Chelsie Snipes
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Ventral (A) and dorso-lateral (B) views of the geometry from the A. jamaicensis FE model. All fixed points are indicated with red triangles (A) with: four fixed supports on the ventral surface of the basihyal to model muscle attachments, two fixed supports on the ends of the thyrohyals to model their attachment to the larynx, and five fixed supports on the surface of the auditory bullae that closely articulates with the skull. TM displacement data were generated in the axis orthogonal to the plane of the TM, indicated by the blue axis on the triad (B). Bones are color coded as follows: fused basihyal and thyrohyals (blue), hypohyal (green), ceratohyal (purple), stylohyal (yellow), auditory bulla (orange), and intervening cartilaginous segments (grey).
Source publication
Synopsis
The hyoid apparatus in laryngeally echolocating bats is unique as it forms a mechanical connection between the larynx and auditory bullae, which has been hypothesized to transfer the outgoing echolocation call to the middle ear during call emission. Previous finite element modeling (FEM) found that hyoid-borne sound can reach the bulla at...
Contexts in source publication
Context 1
... connections were assigned as bonded (no sliding or separation between faces or edges), and a contact tool was used to ensure contacts had been assigned accurately by ANSYS. Similar to Snipes and Carter (2022) , a series of fixed supports were added to the tympanic bullae, basihyals, and thyrohyals to hold the model in space along surfaces that closely articulate with the surrounding anatomy ( Fig. 5 A). Due to the large number of muscle attachments on the basihyal, we added five fixed supports on its ventral surface of the basihyal which represent attachments of the geniohyoideus, hyoglossus, mandibulo-hyoid, and sterno-hyoideus ( Griffiths 1982Griffiths , 1994Griffiths et al. 1992 ). ...
Context 2
... intervening cartilage segments are gray. displacement values of the TM in the axis orthogonal to the plane of the TM ( Fig. 5 B) from 0-150 kHz ( Fig. 6 A). Additionally, when exposed to sound, a real TM does not displace as a rigid, piston-like unit but instead with spatial patterns ( Khanna andTonndorf 1972 , Cheng et al. 2019 ). ...
Citations
... Concerning the sound-producing organs of bats, a few studies have reported the musculoskeletal morphology of the hyolaryngeal apparatus in adults [26,40,[43][44][45][46][47][48][49]. Laryngeally echolocating bats possess hypertrophied intrinsic laryngeal muscles supported by reinforced cricoid, thyroid, and arytenoid cartilage [26,44,[50][51][52]. In particular, the cricothyroid muscle is a superfast muscle essential for the generation of high-frequency sounds in yangochiropterans [19]. ...
Background
The hyolaryngeal apparatus generates biosonar pulses in the laryngeally echolocating bats. The cartilage and muscles comprising the hyolarynx of laryngeally echolocating bats are morphologically modified compared to those of non-bat mammals, as represented by the hypertrophied intrinsic laryngeal muscle. Despite its crucial contribution to laryngeal echolocation, how the development of the hyolarynx in bats differs from that of other mammals is poorly documented. The genus Rhinolophus is one of the most sophisticated laryngeal echolocators, with the highest pulse frequency in bats. The present study provides the first detailed description of the three-dimensional anatomy and development of the skeleton, cartilage, muscle, and innervation patterns of the hyolaryngeal apparatus in two species of rhinolophid bats using micro-computed tomography images and serial tissue sections and compares them with those of laboratory mice. Furthermore, we measured the peak frequency of the echolocation pulse in active juvenile and adult individuals to correspond to echolocation pulses with hyolaryngeal morphology at each postnatal stage.
Results
We found that the sagittal crests of the cricoid cartilage separated the dorsal cricoarytenoid muscle in horseshoe bats, indicating that this unique morphology may be required to reinforce the repeated closure movement of the glottis during biosonar pulse emission. We also found that the cricothyroid muscle is ventrally hypertrophied throughout ontogeny, and that the cranial laryngeal nerve has a novel branch supplying the hypertrophied region of this muscle. Our bioacoustic analyses revealed that the peak frequency shows negative allometry against skull growth, and that the volumetric growth of all laryngeal cartilages is correlated with the pulse peak frequency.
Conclusions
The unique patterns of muscle and innervation revealed in this study appear to have been obtained concomitantly with the acquisition of tracheal chambers in rhinolophids and hipposiderids, improving sound intensity during laryngeal echolocation. In addition, significant protrusion of the sagittal crest of the cricoid cartilage and the separated dorsal cricoarytenoid muscle may contribute to the sophisticated biosonar in this laryngeally echolocating lineage. Furthermore, our bioacoustic data suggested that the mineralization of these cartilages underpins the ontogeny of echolocation pulse generation. The results of the present study provide crucial insights into how the anatomy and development of the hyolaryngeal apparatus shape the acoustic diversity in bats.
... Our study confirms that the shape of the stylohyal is a main difference in the anatomy of the hyoid apparatus between laryngeal echolocating bats and non-laryngeal echolocators (Figs 6, 8, 9;Tables 2, 3;Simmons et al. 2008, Veselka et al. 2010. In laryngeal echolocators, the paddle-shaped tip of the stylohyal is in contact or fused with the tympanic bone (Nojiri et al. 2021, Snipes andCarter 2023). Conversely, in non-bats and pteropodids, the stylohyal is similar to a thin drumstick and disconnected from the tympanic bone (Simmons et al. 2008, Veselka et al. 2010). ...
... We find that the thyrohyoid muscle originates from the caudal tip of the caudal thyroid cornu in non-bat mammals and pteropodids but that it originates more cranially, from the laminae, in most of the laryngeal echolocators. This difference correlates with the idea that the thyrohyoid muscle, not being an intrinsic laryngeal muscle, could play a role in laryngeal echolocation by pulling the basihyal into the thyroid for sound conduction through vibration (Novick and Griffin 1961, Griffiths 1983, Snipes and Carter 2023. However, the thyrohyoid varies in its insertion areas (basihyal or thyrohyal bones) in different families, so it is difficult to fully understand its implication in sound production. ...
Most of over 1400 extant bat species produce high-frequency pulses with their larynx for echolocation. However, the debate about the evolutionary origin of laryngeal echolocation in bats remains unresolved. The morphology of the larynx is known to reflect vocal adaptation and thus can potentially help in resolving this controversy. However, the morphological variations of the larynx are poorly known in bats, and a complete anatomical study remains to be conducted. Here, we compare the 3D laryngeal morphology of 23 extant bat species of 11 different families reconstructed by using iodine contrast-enhanced X-ray microtomography techniques. We find that, contrary to previously thought, laryngeal muscle hypertrophy is not a characteristic of all bats and presents differential development. The larynges of Pteropodidae are morphologically similar to those of non-bat mammals. Two morphotypes are described among laryngeal echolocating bats, illustrating morphological differences between Rhinolophoidea and Yangochiroptera, with the main variations being the cricothyroid muscle volume and the shape of the cricoid and thyroid cartilages. For the first time we detail functional specialization for constant frequency echolocation among Rhinolophoidea. Lastly, the nasal-emitting taxa representing a polyphyletic group do not share the same laryngeal form, which raises questions about the potential modular nature of the bat larynx.
Background
The hyolaryngeal apparatus generates biosonar pulses in the laryngeally echolocating bats. The cartilage and muscles comprising the hyolarynx of laryngeally echolocating bats are morphologically modified compared to those of non-bat mammals, as represented by the hypertrophied intrinsic laryngeal muscle. Despite its crucial contribution to laryngeal echolocation, how the development of the hyolarynx in bats differs from that of other mammals is poorly documented. The genus Rhinolophus is one of the most sophisticated laryngeal echolocators, with the highest pulse frequency in bats. The present study provides the first detailed description of the three-dimensional anatomy and development of the skeleton, cartilage, muscle, and innervation patterns of the hyolaryngeal apparatus in two species of rhinolophid bats using micro-computed tomography images and serial tissue sections and compares them with those of laboratory mice. Furthermore, we measured the peak frequency of the echolocation pulse in active juvenile and adult individuals to correspond to echolocation pulses with hyolaryngeal morphology at each postnatal stage.
Results
We found that the sagittal crests of the cricoid cartilage separated the dorsal cricoarytenoid muscle in horseshoe bats, indicating that this unique morphology may be required to reinforce the repeated closure movement of the glottis during biosonar pulse emission. We also found that the cricothyroid muscle is ventrally hypertrophied throughout ontogeny, and that the cranial laryngeal nerve has a novel branch supplying the hypertrophied region of this muscle. Our bioacoustic analyses revealed that the peak frequency shows negative allometry against skull growth, and that the volumetric growth of all laryngeal cartilages is correlated with the pulse peak frequency.
Conclusions
The unique patterns of muscle and innervation revealed in this study appear to have been obtained concomitantly with the acquisition of tracheal chambers in rhinolophids and hipposiderids, improving sound intensity during laryngeal echolocation. In addition, significant protrusion of the sagittal crest of the cricoid cartilage and the separated dorsal cricoarytenoid muscle may contribute to the sophisticated biosonar in this laryngeally echolocating lineage. Furthermore, our bioacoustic data suggested that the mineralization of these cartilages underpins the ontogeny of echolocation pulse generation. The results of the present study provide crucial insights into how the anatomy and development of the hyolaryngeal apparatus shape the acoustic diversity in bats.
