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.

The morphology of the stylohyal-tympanic bone articulation found in laryngeally echolocating bats is highly indicative of a function associated with signal production.One untested hypothesis is that this morphology allows the transfer of a sound signal from the larynx to the tympanic bones (auditory bulla) via the hyoid apparatus during signal production by the larynx. We used µCT data and finite element analysis to model the propagation of sound through the hyoid chain into the tympanic bones to test this hypothesis. We modeled sound pressure (dB) wave propagation from the basihyal to the tympanic bones, vibratory behavior (m) of the stylohyal-tympanic bone unit, and the stylohyal and tympanic bones when the stylohyal bone is allowed to pivot on the tympanic bone. Sound pressure wave propagation was modeled using the harmonic acoustics solver in ANSYS and vibratory behavior was modeled using coupled modal and harmonic response analyses in ANSYS. For both analyses (harmonic acoustics and harmonic response), the input excitation on the basihyal and thyrohyals was modeled as the estimated pressure (Pa) imposed by the collision of the vibrating thyroid cartilage of the larynx against these bones during signal production.Our models support the hypothesis that this stereotypical hyoid morphology found in laryngeally echolocating bats can transfer sound to the auditory bullae at an amplitude that is likely heard for the species Artibeus jamaicensis and Rhinolophus pusillus.

Echolocating bats have adaptations of the larynx such as hypertrophied intrinsic musculature and calcified or ossified cartilages to support sonar emission. We examined growth and development of the larynx relative to developing flight ability in Jamaican fruit bats to assess how changes in sonar production are coordinated with the onset of flight during ontogeny as a window for understanding the evolutionary relationships between these systems. In addition, we compare the extent of laryngeal calcification in an echolocating shrew species (Sorex vagrans) and the house mouse (Mus musculus), to assess what laryngeal chiropteran adaptations are associated with flight versus echolocation. Individuals were categorized into one of five developmental flight stages (flop, flutter, flap, flight, and adult) determined by drop-tests. Larynges were cleared and stained with alcian blue and alizarin red, or sectioned and stained with hematoxylin and eosin. Our results showed calcification of the cricoid cartilage in bats, represented during the flap stage and this increased significantly in individuals at the flight stage. Thyroid and arytenoid cartilages showed no evidence of calcification and neither cricoid nor thyroid showed significant increases in rate of growth relative to the larynx as a whole. The physiological cross-sectional area of the cricothyroid muscles increased significantly at the flap stage. Shrew larynges showed signs of calcification along the margins of the cricoid and thyroid cartilages, while the mouse larynx did not. These data suggest the larynx of echolocating bats becomes stronger and sturdier in tandem with flight development, indicating possible developmental integration between flight and echolocation. Anat Rec, 297:1270Rec, 297: -1277Rec, 297: , 2014. V C 2014 Wiley Periodicals, Inc.Key words: larynx; echolocation; Sorex vagrans; Artibeus jamaicensis; ontogenyDevelopmental calcification and ossification of the laryngeal cartilages is seen, to some degree, in a variety of mammal species (Harrison, 1995). In nonhominoid primates, young individuals showed no evidence of ossification, with the adults showing patchy patterns of ossification similar to that seen in humans (Harrison and Denny, 1983). The observed patchy areas of ossification were associated with intrinsic muscle attachment and increased tension relative to other areas of the larynx.

No abstract

Recent evidence has shown that the developmental emergence of echolocation calls in young bats follow an independent developmental pathway from other vocalizations and that adult-like echolocation call structure significantly precedes flight ability. These data in combination with new insights into the echolocation ability of some shrews suggest that the evolution of echolocation in bats may involve inheritance of a primitive sonar system that was modified to its current state, rather than the ad hoc evolution of echolocation in the earliest bats. Because the cochlea is crucial in the sensation of echoes returning from sonar pulses, we tracked changes in cochlear morphology during development that included the basilar membrane (BM) and secondary spiral lamina (SSL) along the length of the cochlea in relation to stages of flight ability in young bats. Our data show that the morphological prerequisite for sonar sensitivity of the cochlea significantly precedes the onset of flight in young bats and, in fact, development of this prerequisite is complete before parturition. In addition, there were no discernible changes in cochlear morphology with stages of flight development, demonstrating temporal asymmetry between the development of morphology associated with echo-pulse return sensitivity and volancy. These data further corroborate and support the hypothesis that adaptations for sonar and echolocation evolved before flight in mammals.