Reinforcement of the larynx and trachea in echolocating and non‐echolocating bats

Abstract

The synchronization of flight mechanics with respiration and echolocation call emission by bats, while economizing these behaviors, presumably puts compressive loads on the cartilaginous rings that hold open the respiratory tract. Previous work has shown that during postnatal development of Artibeus jamaicensis (Phyllostomidae), the onset of adult echolocation call emission rate coincides with calcification of the larynx, and the development of flight coincides with tracheal ring calcification. In the present study, I assessed the level of reinforcement of the respiratory system in 13 bat species representing six families that use stereotypical modes of echolocation (i.e. duty cycle % and intensity). Using computed tomography, the degree of mineralization or ossification of the tracheal rings, cricoid, thyroid and arytenoid cartilages were determined for non‐echolocators, tongue clicking, low‐duty cycle low‐intensity, low‐duty cycle high‐intensity, and high‐duty cycle high‐intensity echolocating bats. While all bats had evidence of cervical tracheal ring mineralization, about half the species had evidence of thoracic tracheal ring calcification. Larger bats (Phyllostomus hastatus and Pterpodidae sp.) exhibited more extensive tracheal ring mineralization, suggesting an underlying cause independent of laryngeal echolocation. Within most of the laryngeally echolocating species, the degree of mineralization or ossification of the larynx was dependent on the mode of echolocation system used. Low‐duty cycle low‐intensity bats had extensively mineralized cricoids, and zero to very minor mineralization of the thyroids and arytenoids. Low‐duty cycle high‐intensity bats had extensively mineralized cricoids, and patches of thyroid and arytenoid mineralization. The high‐duty cycle high‐intensity rhinolophids and hipposiderid had extensively ossified cricoids, large patches of ossification on the thyroids, and heavily ossified arytenoids. The high‐duty cycle high‐intensity echolocator, Pteronotus parnellii, had mineralization patterns and laryngeal morphology very similar to the other low‐duty cycle high‐intensity mormoopid species, perhaps suggesting relatively recent evolution of high‐duty cycle echolocation in P. parnellii compared with the Old World high‐duty cycle echolocators (Rhinolophidae and Hipposideridae). All laryngeal echolocators exhibited mineralized or ossified lateral expansions of the cricoid for articulation with the inferior horn of the thyroid, these were most prominent in the high‐duty cycle high‐intensity rhinolophids and hipposiderid, and least prominent in the low‐duty cycle low‐intensity echolocators. The non‐laryngeal echolocators had extensively ossified cricoid and thyroid cartilages, and no evidence of mineralization/ossification of the arytenoids or lateral expansions of the cricoid. While the non‐echolocators had extensive ossification of the larynx, it was inconsistent with that seen in the laryngeal echolocators.

Selection on vocal output affects laryngeal morphology in rats

“…This prediction does not match the pattern of calcification we found in our rat larynges, which were mainly calcified in areas that can be under significant deformation pressure, specifically the specific areas of vocal fold attachment. Carter (2020) compared calcifications in the trachea and larynx across laryngeally echolocating bats and found that higher‐intensity vocalizing species tend to have a more mineralized thyroid cartilages than lower‐intensity species. Thyroid mineralization in the high line rats might help to facilitate and sustain USV production, similar to that observed in laryngeally echolocating bats.…”

The hyoid as a sound conducting apparatus in laryngeally echolocating bats

“…Although stylohyal morphology and its articulation with the tympanic bone show high similarity between different families of laryngeally echolocating bats (Carter, 2020; Sprague, 1943; Veselka et al, 2010), there is variation in the morphology of the more proximal elements of the anterior cornu of hyoid apparatus. For example, there is a tendency towards reduction of the hypohyal in length, with this reduction reaching its extreme in Eptesicus , Minipterus , and Kerivoula , where it is present as a slender fascial attachment of the anterior cornu to the basihyal (Sprague, 1943).…”

“…Laryngeally echolocating bats exhibit many adaptations associated with the production and reception of sophisticated call sequences. For example, echolocation is coupled with laryngeal cartilage that is structurally reinforced through extensive calcification or ossification, presumably in response to the increased mechanical demands during vocalization (Carter, 2020; Carter & Adams, 2014; Denny, 1976; Griffiths, 1978; Suthers, 2004). Additionally, the cochleae of laryngeally echolocating bats have enlarged basal turns relative to other mammals and internal adaptations that increase the stiffness of the basilar membrane, thereby increasing sensitivity to the higher frequencies associated with echolocation signals (Kössl & Vater, 1995; Vater & Kössl, 2011).…”

“…pusillus is indicated in orange, while the only part of the larynx that is calcified in A . jamaicensis is the cricoid (Carter 2020) and is not shown here. Points of view are from cranial (a), ventral (b), and lateral (c and d) aspects…”

“…The sinusoidal pressure applied to the laryngeal surface of the hyoid apparatus represents the pressure applied due to impact of the vibrating larynx against the hyoid during echolocation signal production. Based on µCT images on the necks of bats (Carter, 2020; Veselka et al, 2010), the laryngeal surface of the hyoid apparatus is in close proximity to the thyroid cartilage of the larynx and therefore this contact/collision was assumed to have no significant amounts of intervening soft tissue/damping. This sinusoidal pressure/impact is considered the excitation input and was modeled across the range of frequencies associated with the echolocation signals from both species.…”