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The hyoid as a sound conducting apparatus in laryngeally echolocating bats
Abstract
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 (FEA) 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.
... The cochlea, which transmits sound signals to the cerebral system in vertebrates, is one of the most iconic organs because it is markedly enlarged in laryngeally echolocating bats [32]. In addition, laryngeally echolocating bats possess a fully ossified stylohyal attached to the ectotympanic bone, which improves their sensitivity to ongoing signals [34,42]. The morphology and development of these features have been well-documented in the context of the evolutionary origins of laryngeal echolocation in bats [31, 32, 35-38, 41, 42]. ...
... In mice, the basihyal was the only hyoid component to ossify at birth (Fig. 9G), whereas in horseshoe bats, all bony elements in the hyoid apparatus were already ossified (Fig. 9A). In laryngeally echolocating bats, the stylohyal bone is articulated with an ectotympanic [34], which possibly facilitates the transmission of the ongoing signal into the inner ear through bone conduction [42]. A recent biomechanical analysis revealed that the closer the bony element was to the basihyal bone, the higher the sound pressure is (Snipes and Carter [42]). ...
... In laryngeally echolocating bats, the stylohyal bone is articulated with an ectotympanic [34], which possibly facilitates the transmission of the ongoing signal into the inner ear through bone conduction [42]. A recent biomechanical analysis revealed that the closer the bony element was to the basihyal bone, the higher the sound pressure is (Snipes and Carter [42]). The ongoing echolocation pulse, which is produced in the larynx, transfers to the thyrohyal and basihyal regions and subsequently propagates into the ceratohyal, epihyal, stylohyal, and ectotympanic regions. ...
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.
... Concerning the sound-producing organs of bats, a few studies have reported the 107 musculoskeletal morphology of the hyolaryngeal apparatus in adults [26,40,[42][43][44][45][46][47][48]. Laryngeally 108 echolocating bats possess hypertrophied intrinsic laryngeal muscles supported by reinforced 109 cricoid, thyroid, and arytenoid cartilage [26,43,49]. ...
... Biosonar sound requires rotation of the thyroid cartilage to increase the tension of the vocal folds 388 with the superfast muscle [19]. Acoustic response analyses have revealed that the bony connection 389 between the stylohyal and ectotympanic transfers sound signals at the most susceptible amplitude 390 to the auditory bullae [40,48]. Thus, as a result of the release from the tight connection, the hyoid 391 complex and laryngeal cartilage might become mutually movable, providing higher flexibility for 392 bone conduction and thyroid rotation, respectively. ...
... In mice, the basihyal was the only hyoid component to ossify at birth 512 (Fig. 7G), whereas in horseshoe bats, all bony elements in the hyoid apparatus were already 513 ossified (Fig. 7A). In laryngeally echolocating bats, the stylohyal bone is articulated with an 514 ectotympanic [32], which possibly facilitates the transmission of the ongoing signal into the inner 515 ear through bone conduction [40]. A recent biomechanical analysis revealed that the closer the 516 bony element was to the basihyal bone, the higher the sound pressure is (Snipes and Carter, 2022). ...
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.
... Finite-element (FE) modeling of this connection between larynx and ear indicates that sound can be effectively transmitted from the laryngeal surface of the hyoid to the auditory bullae in Artibeus jamaicensis (a low duty cycle [LDC]/frequency modulated [FM] echolocator) and Rhinolophus pusillus (a high duty cycle [HDC]/narrow band [NB] echolocator) ( Snipes and Carter 2022 ). Here, duty cycle refers to the length of time in a call sequence in which there is out going Fig. 1 Volume-rendered lateral and ventral views of the cranium (brown), trachea/larynx (gray), and hyoid apparatus from R. f er rumequinum. ...
... The LDC echolocator ( A. jamaicensis ) has stylohyals that wrap around the lateral side of the bullae, while the HDC echolocator ( R. pusillus ) has stylohyals that wrap around the medial rim of the bullae ( Fig. 2 ). Snipes and Carter (2022) did not include a tympanic membrane (TM) in their FE models but instead used the vibration of the bulla as evidence that sound likely moved into the inner ear via bone conduction or a rocking motion of the bulla/TM unit in the lateral-medial plane, which presumably sets the ear ossicles into motion. In that study, we modeled varying levels of constraint (0, 1, 3, and 5 fixed points) on the basihyal to evaluate the effect of muscle attachments and found differences in the performance of our R. pusillus and A. jamaicensis models. ...
... In that study, we modeled varying levels of constraint (0, 1, 3, and 5 fixed points) on the basihyal to evaluate the effect of muscle attachments and found differences in the performance of our R. pusillus and A. jamaicensis models. As basihyal constraint was increased, the displacement of the bulla in the A. jamaicensis model quickly dropped below the assigned threshold of 2.9e-11 m; and conversely, the bulla of the R. pusillus model exhibited displacement peaks above the assigned threshold at all levels of constraint ( Snipes and Carter 2022 ). These results lead us to con-sider whether HDC echolocators could use vibration of the bulla and bone conduction to transfer sound into the inner ear. ...
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 an amplitude likely heard by echolocating bats; however, that study did not model how or if the signal could reach the inner ear (or cochlea). One route that sound could take is via stimulation of the eardrum—similarly to that of air-conducted sound. We used micro computed tomography (μCT) data to build models of the hyoid apparatus and middle ear from six species of bats with variable morphology. Using FEM, we ran harmonic response analyses to measure the vibroacoustic response of the tympanic membrane due to hyoid-borne sound generated during echolocation and found that hyoid-borne sound in all six species stimulated the eardrum within a range likely heard by bats. Although there was variation in the efficiency between models, there are no obvious morphological patterns to account for it. This suggests that hyoid morphology in laryngeal echolocators is likely driven by other associated functions.
... There has been considerable debate over whether early chiropterans could echolocate, laryngeally or otherwise (Fenton 2010;Simmons et al. 2008Simmons et al. , 2010Snipes and Carter 2021;Thiagavel et al. 2018;Veselka et al. 2010) and the fossil record is understandably mute regarding the evolution of cartilaginous structures like the scutulum and pinna, let alone the Tp (Simmons et al. 2008(Simmons et al. , 2010. Genome-based phylogenetics has suggested that the non-echolocating pteropodids and the highly sophisticated OWNE are closely related to each other within the Yinpterochiroptera (Eick, Jacobs, and Matthee 2005; Hutcheon and Kirsch 2006;Springer et al. 2001;Teeling et al. 2002). ...
The external ear in eutherian mammals is composed of the annular, auricular (pinna), and scutellar cartilages. The latter extends between the pinnae, across the top of the head, and lies at the intersection of numerous auricular muscles and is thought to be a sesamoid element. In bats, this scutulum consists of two distinct regions, (1) a thin squama that is in contact with the underlying temporalis fascia and (2) a lateral bossed portion that is lightly tethered to the medial surface of the pinna. The planar size, shape, and proportions of the squama vary by taxa, as does the relative size and thickness of the boss. The origins, insertions, and relative functions of the auricular muscles are complicated. Here, 30 muscles were tallied as to their primary attachment to the pinnae, scutula, or a pre-auricular musculo-aponeurotic plate that is derived from the epicranius. In contrast to Yangochiroptera, the origins and insertions of many auricular muscles have shifted from the scutulum to this aponeurotic plate, in both the Rhinolophidae and Hipposideridae. We propose that this functional shift is a derived character related primarily to the rapid translations and rotations of the pinna in high-duty-cycle rhinolophid and hipposiderid bats.
... It is also known that bats' larynges are disproportionally large compared to other mammals of similar size due to sexual dimorphism in Pteropodidae (Langevin and Barclay 1990). Despite some recent focus on the larynx (Carter andAdams 2014, 2016;Carter 2020;Nojiri et al. 2021a;Snipes and Carter 2022), we suggest that further research is needed to unravel the extent and patterning of variation in this organ as it relates to echolocation capability in bats. We hypothesise that despite a highly similar laryngeal morphology inside Orders of non-bat mammals, a variety of laryngeal forms will be observed among laryngeal echolocating bats, and these specialized laryngeal features will relate to the laryngeal echolocation strategies. ...
Laryngeal echolocation in bats could have evolved following two scenarios: a single origin from a common ancestor or an independent acquisition inside the two clades Yinpterochiroptera and Yangochiroptera. Later, some members of Yinpterochiroptera possibly lost their ability to echolocate. In bats, the larynx produces vocalizations for communication and, in most species, for echolocation. Here, we describe how comparative chiropteran laryngeal morphology is a novel area of research that could improve the understanding of echolocation and may help resolve the evolutionary history of bats. This review provides morphological descriptions and comparisons of the bat larynx and bioacoustics interpretations. We discuss the importance of understanding: (1) laryngeal sound production so it may be linked with the evolution of the chiropteran auditory system; and (2) the evolution of laryngeal morphology to understand the ecological and behavioural aspects of bat biology. We find that a strong phylogenetic signal is potentially the main source explaining macroevolutionary variation in laryngeal form among bats. We predict that the three parameters of sound production in echolocation (frequency, intensity, and rate of calls) are independently modulated by different laryngeal components, but this hypothesis remains understudied in terms of species diversity.
This study describes variation patterns in the constant frequency of echolocation calls emitted at rest and when not flying ("resting frequency" RF) of the least horseshoe bat, Rhinolophus pusillus, on a broad geographical scale and in response to local climatic variables. Significant differences in RF were observed among populations throughout the species range in Mainland China, and this variation was positively and significantly related to climate conditions, especially environmental humidity, but the variability was only weakly associated with geographical distance. Sex dimorphism in the RF of R. pusillus may imply that female and male might keep their frequencies within a narrow range for sex recognition. Moreover, bats adjusted resting frequency to humidity, which may imply partitioning diet by prey size or the influence of rainfall noise. The results indicate that bats adjust echolocation call frequency to adapt to environmental conditions. Therefore, environmental selection shape the diversity of echolocation call structure of R. pusillus in geographically separated populations, and conservation efforts should focus on changes in local climate and effects of environmental noise.
Echolocation is an active form of orientation in which animals emit sounds and then listen to reflected echoes of those sounds to form images of their surroundings in their brains. Although echolocation is usually associated with bats, it is not characteristic of all bats. Most echolocating bats produce signals in the larynx, but within one family of mainly non-echolocating species (Pteropodidae), a few species use echolocation sounds produced by tongue clicks. Here we demonstrate, using data obtained from micro-computed tomography scans of 26 species (n = 35 fluid-preserved bats), that proximal articulation of the stylohyal bone (part of the mammalian hyoid apparatus) with the tympanic bone always distinguishes laryngeally echolocating bats from all other bats (that is, non-echolocating pteropodids and those that echolocate with tongue clicks). In laryngeally echolocating bats, the proximal end of the stylohyal bone directly articulates with the tympanic bone and is often fused with it. Previous research on the morphology of the stylohyal bone in the oldest known fossil bat (Onychonycteris finneyi) suggested that it did not echolocate, but our findings suggest that O. finneyi may have used laryngeal echolocation because its stylohyal bones may have articulated with its tympanic bones. The present findings reopen basic questions about the timing and the origin of flight and echolocation in the early evolution of bats. Our data also provide an independent anatomical character by which to distinguish laryngeally echolocating bats from other bats.
Echolocation call intensity was measured in the laboratory for five species of British insectivorous bats in free flight and in the hand. All species showed similar call intensities of between 80 and 90 dB peSPL (peak equivalent SPL) at 1 m during flight except Plecotus auritus, whose call intensity was between 68 and 77 dB peSPL at 1 m. Calls from stationary bats were about 13 dB less intense than calls during flight. A method is proposed to measure the root mean square (rms) amplitude of echolocation calls and, hence, to calculate the energy flux density of the call.
The constant−frequency calls of Rhinolophus hipposideros have energy flux densities approximately ten times higher than those of bats using frequency−modulated calls as a result of their longer durations and lower crest factors. It is argued that the low−intensity calls of P. auritus allow it to approach tympanate moths more closely before triggering their escape response.
Vocal signals play a very important role in the life of both birds and echolocating bats, but these two unrelated groups of flying vertebrates have very different vocal systems. They nevertheless must solve many of the same problems in producing sound. This brief review examines avian and microchiropteran motor mechanisms for: 1) coordinating the timing of phonation with the vocal motor pattern that controls its acoustic properties, and 2) achieving respiratory strategies that provide adequate ventilation for pulmonary gas exchange, while also facilitating longer duration songs or trains of sonar pulses.
The fact that vibration of the skull causes a hearing sensation has been known since the 19th century. This mode of hearing was termed hearing by bone conduction. Although there has been more than a century of research on hearing by bone conduction, its physiology is not completely understood. Lately, new insights into the physiology of hearing by bone conduction have been reported. Knowledge of the physiology, clinical aspects, and limitations of bone conduction sound is important for clinicians dealing with hearing loss and is the purpose of this review.
The data were compiled from the published literature in the areas of clinical bone conduction hearing, bone conduction hearing aids, basic research on bone conduction physiology, and recent research on bone conduction hearing from our laboratory.
Five factors contributing to bone conduction hearing have been identified: 1) sound radiated into the external ear canal, 2) middle ear ossicle inertia, 3) inertia of the cochlear fluids, 4) compression of the cochlear walls, and 5) pressure transmission from the cerebrospinal fluid. Of these five, inertia of the cochlear fluid seems most important. Bone conduction sound is believed to reflect the true cochlear function; however, certain conditions such as middle ear diseases can affect bone conduction sensitivity, but less than for air conduction. The bone conduction route can also be used for hearing aids; since the bone conduction route is less efficient than the air conduction route, bone conduction hearing aids are primarily used for hearing losses where air conduction hearing aids are contraindicated.
Bats (Chiroptera) represent one of the largest and most diverse radiations of mammals, accounting for one-fifth of extant species. Although recent studies unambiguously support bat monophyly and consensus is rapidly emerging about evolutionary relationships among extant lineages, the fossil record of bats extends over 50 million years, and early evolution of the group remains poorly understood. Here we describe a new bat from the Early Eocene Green River Formation of Wyoming, USA, with features that are more primitive than seen in any previously known bat. The evolutionary pathways that led to flapping flight and echolocation in bats have been in dispute, and until now fossils have been of limited use in documenting transitions involved in this marked change in lifestyle. Phylogenetically informed comparisons of the new taxon with other bats and non-flying mammals reveal that critical morphological and functional changes evolved incrementally. Forelimb anatomy indicates that the new bat was capable of powered flight like other Eocene bats, but ear morphology suggests that it lacked their echolocation abilities, supporting a 'flight first' hypothesis for chiropteran evolution. The shape of the wings suggests that an undulating gliding-fluttering flight style may be primitive for bats, and the presence of a long calcar indicates that a broad tail membrane evolved early in Chiroptera, probably functioning as an additional airfoil rather than as a prey-capture device. Limb proportions and retention of claws on all digits indicate that the new bat may have been an agile climber that employed quadrupedal locomotion and under-branch hanging behaviour.
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 (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 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. 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. Mineralization patterns are discussed with regard to echolocation ability.
Mysticetes are known to emit sounds of low and even very low frequencies, down to the famous 20-Hz-signals. Because the mammalian ear is generally rather insensitive to low frequencies, the problem arises how these animals manage to hear them. Several mechanisms have been proposed, including the detection of resonances of the lungs. It is the purpose of this presentation, however, to show that the cetacean ear is structurally specialized for the detection of low frequencies.
This is a comprehensive and accessible overview of what is known about the structure and mechanics of bone, bones, and teeth. In it, John Currey incorporates critical new concepts and findings from the two decades of research since the publication of his highly regarded The Mechanical Adaptations of Bones. Crucially, Currey shows how bone structure and bone's mechanical properties are intimately bound up with each other and how the mechanical properties of the material interact with the structure of whole bones to produce an adapted structure. For bone tissue, the book discusses stiffness, strength, viscoelasticity, fatigue, and fracture mechanics properties. For whole bones, subjects dealt with include buckling, the optimum hollowness of long bones, impact fracture, and properties of cancellous bone. The effects of mineralization on stiffness and toughness and the role of microcracking in the fracture process receive particular attention. As a zoologist, Currey views bone and bones as solutions to the design problems that vertebrates have faced during their evolution and throughout the book considers what bones have been adapted to do. He covers the full range of bones and bony tissues, as well as dentin and enamel, and uses both human and non-human examples. Copiously illustrated, engagingly written, and assuming little in the way of prior knowledge or mathematical background, Bones is both an ideal introduction to the field and also a reference sure to be frequently consulted by practicing researchers.
Despite all other craniodental adaptations, the head of most bats must function as an ultrasonic emitter and receiver. Not all echolocation calls are ultrasonic, but all either are emitted from an open mouth (oral-emission) or are forced through the confines of the nasal passages (nasal-emission), and some nasal-emitting bats alternate between modes as the situation demands. The conspicuous baffles that surround the nostrils of nasal-emitting bats are not ornamental structures; rather, these noseleaves serve several important acoustic functions and are considered to be the earmark of nasal-emitting bats. For many readers, the difference between oral-and nasal-emission is viewed as a simple character state, most likely tied to the vagaries of foraging ecology in some tangential manner. However, Pedersen and Timm (Evolutionary history of bats: fossils molecules and morphology. Cambridge University Press, Cambridge, pp 470-499, 2012) reviewed a considerable volume of literature discussing how the advent of nasal-emitting bats required a dramatic redesign of the microchiropteran rostrum and skull base during development. Nasal-emission is therefore a key innovation responsible for two of the most dramatic morphological radiations in the Chiroptera-phyllostomid and rhinolophid + hipposiderid bats. Herein, we summarize and update that review and then discuss recent advances in the numerical analysis of form and function in regard to the beamforming function of noseleaves (Müller, J Acoust Soc Am 128:1414-1425, 2010). © 2013 Springer Science+Business Media New York. All rights are reserved.
The mammalian cochlea must extract loudness and frequency information about different and overlapping acoustic events from a single input channel. Unlike the visual system, where input from different spatial sources is separated early and distributed in parallel channels, all input to the cochlea converges in the middle ear to induce movement at the membrane of the oval window. The oval window acts as a point source of mechanical waves dissipating in the fluid-filled spaces of the cochlea. It is now left to the organ of Corti to filter relevant information from the total input. Because this is a difficult task, it is no wonder that the acquisition of highly developed cochleae that are able to analyze low-level signals at many different frequencies is a relatively recent step in animal evolution, one that is confined to higher vertebrates. The high-frequency hearing capabilities of reptiles and birds are restricted to frequencies below about 12 kHz (for review, see Manley 1990). As a specific mammalian adaptation, the middle ear and the cochlea have an extended sensitivity in the high-frequency range. For processing of high frequencies, the cochlea has developed macro- and micromechanical specializations and employs active processes that enhance frequency tuning and sensitivity.
The laryngeal musculature and laryngeal cartilages associated with sound production and amplification in Mormoops megalophylla and Pteronotus davyi are described and compared with homologous structures in eight species of phyllos-tomatid bats. Certain specialized structures observed in the mormoopid larynges resemble a variable Helmholtz resonating amplifier. This type of amplifier is theoretically capable of 1) varying the amplitude of a constant-frequency pulse, and 2) maintaining a constant amplitude during a frequency change within a pulse.
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, 2014. © 2014 Wiley Periodicals, Inc.
A long-standing question in bat biology is if the evolution of echolocation and flight are associated or if they evolved independently, and if so, which evolved first. We seek to use ontogeny as a surrogate for understanding linkages between flight evolution and echolocation in bats. To do this we quantify the onset of recognizable sonar calls in newborn Artibeus jamaicensis and the tempo of growth and development across several different postnatal flight stages. By dropping individuals from a perch beginning on day 1 postpartum, we recorded vocalizations and quantified their flight ability into five developmental stages (flop, flutter, flap, flight and adult). One-day-old individuals were capable of emitting sonar-like frequency-modulated (FM) calls during free-fall that were not significantly different from adult sonar calls in high and low frequency (kHz). However, bandwidth (kHz) did increase significantly with age as did sweep rate (kHz ms−1), whereas call duration significantly decreased. Few bats older than 18 days emitted communication calls as they fell and measured parameters of communication calls did not change significantly with age. Our data support the hypothesis that communication and sonar calls are discrete and independently derived at birth and thus have different evolutionary pathways as well.
We behaviorally determined the audiograms of three Common vampire bats (Phyllostomidae, Desmodus rotundus), a species specialized to exist exclusively on blood. The bats were trained to respond to pure tones in a conditioned suppression/avoidance procedure for a blood reward and a mild punisher for failures to detect the tones. Common vampire bats have a hearing range from 716 Hz to 113 kHz at a level of 60 dB. Their best hearing is at 20 kHz where they are slightly more sensitive than other bats, and they have a second peak of good sensitivity at 71 kHz. They have unusually good sensitivity to low frequencies compared to other bats, but are less sensitive to low frequencies than most mammals. Selective pressures affecting high-frequency hearing in bats and mammals in general are discussed.
Mechanical loads play a pivotal role in the growth and maintenance of bone and joints. Although loading can activate anabolic genes and induce bone remodeling, damping is essential for preventing traumatic bone injury and fracture. In this study we investigated the damping capacity of bone, joint tissue, muscle, and skin using a mouse hindlimb model of enhanced loading in conjunction with finite element modeling to model bone curvature. Our hypothesis was that loads were primarily absorbed by the joints and muscle tissue, but that bone also contributed to damping through its compression and natural bending. To test this hypothesis, fresh mouse distal lower limb segments were cyclically loaded in axial compression in sequential bouts, with each subsequent bout having less surrounding tissue. A finite element model was generated to model effects of bone curvature in silico. Two damping-related parameters (phase shift angle and energy loss) were determined from the output of the loading experiments. Interestingly, the experimental results revealed that the knee joint contributed to the largest portion of the damping capacity of the limb, and bone itself accounted for approximately 38% of the total phase shift angle. Computational results showed that normal bone curvature enhanced the damping capacity of the bone by approximately 40%, and the damping effect grew at an accelerated pace as curvature was increased. Although structural curvature reduces critical loads for buckling in beam theory, evolution apparently favors maintaining curvature in the tibia. Histomorphometric analysis of the tibia revealed that in response to axial loading, bone formation was significantly enhanced in the regions that were predicted to receive a curvature-induced bending moment. These results suggest that in addition to bone's compressive damping capacity, surrounding tissues, as well as naturally-occurring bone curvature, also contribute to mechanical damping, which may ultimately affect bone remodeling and bone quality.
Duty cycle describes the relative 'on time' of a periodic signal. In bats, we argue that high duty cycle (HDC) echolocation was selected for and evolved from low duty cycle (LDC) echolocation because increasing call duty cycle enhanced the ability of echolocating bats to detect, lock onto and track fluttering insects. Most echolocators (most bats and all birds and odontocete cetaceans) use LDC echolocation, separating pulse and echo in time to avoid forward masking. They emit short duration, broadband, downward frequency modulated (FM) signals separated by relatively long periods of silence. In contrast, bats using HDC echolocation emit long duration, narrowband calls dominated by a single constant frequency (CF) separated by relatively short periods of silence. HDC bats separate pulse and echo in frequency by exploiting information contained in Doppler-shifted echoes arising from their movements relative to background objects and their prey. HDC echolocators are particularly sensitive to amplitude and frequency glints generated by the wings of fluttering insects. We hypothesize that narrowband/CF calls produced at high duty cycle, and combined with neurobiological specializations for processing Doppler-shifted echoes, were essential to the evolution of HDC echolocation because they allowed bats to detect, lock onto and track fluttering targets. This advantage was especially important in habitats with dense vegetation that produce overlapping, time-smeared echoes (i.e. background acoustic clutter). We make four specific, testable predictions arising from this hypothesis.
Arising from: N. Veselka et al. Nature 463, 939-942 (2010); Veselka et al. reply
Echolocation of bats is a fascinating topic with an ongoing controversy regarding the signal processing that bats perform on the echo. Veselka et al. found that bats that use the larynx for producing the echolocating ultrasound have a stylohyal bone that connects the larynx to the auditory bulla. I propose that the stylohyal bone is used for heterodyne detection of Doppler-shifted echoes. This would allow very precise frequency resolution and phase-sensitive analysis of the returning echoes for determining the velocity of echolocated objects like insects.
This review addresses the functional organization of the mammalian cochlea under a comparative and evolutionary perspective. A comparison of the monotreme cochlea with that of marsupial and placental mammals highlights important evolutionary steps towards a hearing organ dedicated to process higher frequencies and a larger frequency range than found in non-mammalian vertebrates. Among placental mammals, there are numerous cochlear specializations which relate to hearing range in adaptation to specific habitats that are superimposed on a common basic design. These are illustrated by examples of specialist ears which evolved excellent high frequency hearing and echolocation (bats and dolphins) and by the example of subterranean rodents with ears devoted to processing low frequencies. Furthermore, structural functional correlations important for tonotopic cochlear organization and predictions of hearing capabilities are discussed.
Thesis (Ph. D.)--University of Massachusetts, 1981.
VESPERTILIONID bats produce FM echolocation pulses which sweep through a broad ultrasonic range1,2. Neurophysiological3,4 and behavioural5 evidence indicates that Myotis lucifugus, the most intensively studied of the vespertilionids, is maximally sensitive to the frequencies of its cries. The small size and mass of the middle ear structures in Microchiroptera6 suggest that the transduction system is specialized for the reception of ultrasound. It is obvious that the bat middle ear must respond to high ultrasonic frequencies, but it is not known how efficient the middle ear is, or whether this is achieved by tuned resonances or by a broad-band response. We have used the Mössbauer technique to investigate the contribution of the tympanic membrane to this high-frequency sensitivity. Although our primary interest was in the high-frequency response, we examined a broad range from 1 to 100 kHz.
Bats use echolocation to exploit a variety of habitats and food types. Much research has documented how frequency-time features of echolocation calls are adapted to acoustic constraints imposed by habitat and prey but emitted sound intensities have received little attention. Bats from the family of Phyllostomidae have been categorised as low intensity (whispering) gleaners, assumed to emit echolocation calls with low source levels (approximately 70 dB SPL measured 10 cm from the bat's mouth). We used a multi-microphone array to determine intensities emitted from two phyllostomid bats from Panamá with entirely different foraging strategies. Macrophyllum macrophyllum hunts insects on the wing and gaffs them with its tail membrane and feet from or above water surfaces whereas Artibeus jamaicensis picks fruit from vegetation with its mouth. Recordings were made from bats foraging on the wing in a flight room. Both species emitted surprisingly intense signals with maximum source levels of 105 dB SPL r.m.s. for M. macrophyllum and 110 dB SPL r.m.s. for A. jamaicensis, hence much louder than a ;whisper'. M. macrophyllum was consistently loud (mean source level 101 dB SPL) whereas A. jamaicensis showed a much more variable output, including many faint calls and a mean source level of 96 dB SPL. Our results support increasing evidence that echolocating bats in general are much louder than previously thought. We discuss the importance of loud calls and large output flexibility for both species in an ecological context.
Echolocating bats use different information-gathering strategies for hunting prey in open, uncluttered environments, in relatively
open environments with some obstacles, and in densely cluttered environments. These situations differ in the extent to which
individual targets such as flying insects can be detected as isolated objects or must be separated perceptually from backgrounds.
Echolocating bats also differ in whether they use high-resolution, multidimensional images of targets or concentrate specifically
on one particular target dimension, such as movement, to detect prey.
The acoustic vibrations of the eardrum at the umbo and of the stapes have been measured in the greater horseshoe bat. The displacement amplitude response of the eardrum shows a second-order low-pass characteristic, typical of a lumped mass and stiffness system with a resonance frequency of about 55 kHz. The effective mass was calculated to be about 8 micrograms, and the specific stiffness 40 X 10(6) dyne/cm3, which is one hundred times greater than guinea pig. The measured level ratio appears to be greater (3X - 5X) than the geometric ratio (2X) probably due to flexing of the manubrium. The umbo-stapes phase lag exceeds 1 cycle at high frequencies, suggesting a system of at least four reactances. This is not consistent with the relatively slight change in lever ratio with frequency. One possibility for reconciling the two results is that the distributed mass and stiffness of the ossicles act as a transmission line for transverse vibrations. There is no evidence for a sharply peaked middle-ear response (although it is more sharply tuned than some species), nor for resonant absorption by the cochlea in the region of 83 kHz - the 'constant' frequency of this bat. The eardrum shows theoretically optimal matching to the air at 55 kHz and is reasonably efficient from 15 kHz to at least 110 kHz.
The wide range of dietary niches filled by modern mammals is reflected in morphological diversity of the feeding apparatus. Despite volumes of data on the biomechanics of feeding, the extent to which the shape of mammal skulls reflects stresses generated by feeding is still unknown. In addition to the feeding apparatus, the skull accommodates the structural needs of the sensory systems and brain. We turned to bats as a model system for separating optimization for masticatory loads from optimization for other functions. Because the energetic cost of flight increases with body mass, it is reasonable to suggest that bats have experienced selective pressure over evolutionary time to minimize mass. Therefore, the skulls of bats are likely to be optimized to meet functional demands. We investigate the hypothesis that there is a biomechanical link between biting style and craniofacial morphology by combining biting behavior and bite force data gathered in the field with finite-element (FE) analysis. Our FE experiments compared patterns of stress in the craniofacial skeletons within and between two species of bats (Artibeus jamaicensis and Cynopterus brachyotis) under routine and atypical loading conditions. For both species, routine loading produced low stresses in most of the skull. However, the skull of Artibeus was most resistant to loads applied via its typical biting style, suggesting a mechanical link between routine loading and skull form. The same was not true of Cynopterus, where factors other than feeding appear to have had a more significant impact on craniofacial morphology.
Phylogenetic systematics of slit‐faced bats (Chiroptera, Nycteridae) based on hyoid and other morphology
- Griffiths T.A.
Griffiths, T.A. (1994) Phylogenetic systematics of slit-faced bats
(Chiroptera, Nycteridae) based on hyoid and other morphology.
American Museum Novitiates, 3090, 1-17.
The auditory bulla in some fossil mammals with a general introduction to this region of the skull
- Klaauw C.J.V.D.
Klaauw, C.J.V.D. (1931) The auditory bulla in some fossil mammals with
a general introduction to this region of the skull. Bulletin of the
American Museum of Natural History, 62, article 1.
Comparative anatomy of the larynx
- S P Denny
Denny, S.P. (1976) Comparative anatomy of the larynx. In: Hinchcliffe,
R. & Harrison, D.F.N. (Eds.) The scientific basis of otolaryngology.
London: Heinemann, pp. 536-545.
Vocal mechanisms in birds and bats: a comparative view. Anais Da Academia Brasileira De Ciências
- R A Suthers
Suthers, R.A. (2004) Vocal mechanisms in birds and bats: a comparative view. Anais Da Academia Brasileira De Ciências, 76,
247-252.