Matthew J. Mason

Middle ear structures in fossorial mammals: a comparison with non‐fossorial species

A large data set, comprising certain measurements of middle ear structures in mammals, was compiled both from measurements made by the author and from the literature. Parameters of the middle ear apparatus believed to be important to audition were compared between fossorial and non-fossorial species, in an attempt to identify general trends among fossorial groups. Although their tympanic membranes are not of unusual size, many fossorial mammals possess enlarged stapes footplate areas, resulting in low anatomical area ratios. Low anatomical lever ratios are also common, and the reduction or loss of middle ear muscles seems to be a consistent trend. These characteristics might be associated with poor sensitivity to airborne sound. Other features of the middle ear apparatus are more variable both between and within fossorial families. The middle ear ossicles of fossorial rodents, talpid moles and some golden moles were not found to differ in mass from those of non-fossorial mammals of similar body size. The similar ossicular morphologies of these animals suggest convergent adaptation towards a subterranean environment, but the middle ear structure alone does not seem to explain the restricted hearing range observed in certain of these species. Some genera of golden moles possess extraordinarily hypertrophied auditory ossicles, which, relative to body mass, are the largest of all mammals for which data are available. These ossicles seem to be adaptations towards a form of inertial bone conduction, used for the detection of substrate vibrations. In stark contrast, the marsupial mole Notoryctes has particularly small ossicles. The unusual middle ear structures of this animal may well be degenerate.

A bony connection signals laryngeal echolocation in bats

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.

Morphology of the middle ear of golden moles (Chrysochloridae)

The middle ear structures of nine species of golden moles (family Chrysochloridae) were examined under the light microscope. Auditory structures of several of these species are described here for the first time in detail, the emphasis being on the ossicular apparatus. Confirming previous observations, some golden moles (e.g. Amblysomus species) have ossicles of a morphology typical of mammals, whereas others ( Chrysospalax , Chrysochloris , Cryptochloris and Eremitalpa species) have enormously hypertrophied mallei. Golden moles differ in the nature and extent of the interbullar connection, the shape of the tympanic membrane and that of the manubrium. The stapes has an unusual orientation, projecting dorsomedially from the incus. It has been proposed that hypertrophied ossicles in golden moles are adapted towards the detection of seismic vibrations. The functional morphology of the middle ear apparatus is reconsidered in this light, and it is proposed that adaptations towards low-frequency airborne hearing might have predisposed golden moles towards the evolution of seismic sensitivity through inertial bone conduction. The morphology of the middle ear apparatus sheds little light on the disputed ordinal position of the Chrysochloridae.

Pathways for Sound Transmission to the Inner Ear in Amphibians

The role of the tympanic ear in tetrapods is fairly well understood: it has to cope with demands including impedance matching, sound localization, and protection from high sound levels and static pressures. Adaptations in frogs and other tetrapods might well be analogous rather than homologous (Lombard and Bolt 1979), allowing one to examine critically assumptions about what is required of an ear. Indeed, many amphibians lack a tympanic ear altogether yet are still capable of hearing in air. Hetherington and Lindquist (1999) suggest that audition in early tetrapods might have involved the lung.

Bone conduction and seismic sensitivity in golden moles (Chrysochloridae)

Some genera of golden moles are known to possess enormously hypertrophied auditory ossicles. These structures have been implicated as potentially mediating a form of inertial bone conduction, used by the golden mole to detect seismic vibrations. A simple model of ossicular inertial bone conduction, based on an existing model of the human middle ear from the literature, was used in an attempt to examine vibrational sensitivity in these animals. Those golden moles with hypertrophied ossicles are predicted to possess a sensitive inertial bone conduction response at frequencies below a few hundred hertz, whereas species lacking these middle ear adaptations are predicted to have a far less sensitive response in this ecologically important frequency range. An alternative mode of inertial bone conduction in golden moles, potentially conferring sensitivity to vertically-polarized seismic vibrations such as Rayleigh waves, is proposed. Certain behaviours of golden moles described in the literature are interpreted as augmenting seismic sensitivity.

Evolution of the middle ear apparatus in talpid moles

The middle ear structures of eight species of mole in the family Talpidae (Mammalia: Eulipotyphla) were studied under light and electron microscopy. Neurotrichus, Parascalops, and Condylura have a simple middle ear cavity with a loose ectotympanic bone, ossicles of a “microtype” morphology, and they retain a small tensor tympani muscle. These characteristics are ancestral for talpid moles. Talpa, Scalopus, Scapanus, and Parascaptor species, on the other hand, have a looser articulation between malleus and ectotympanic bone and a reduced or absent orbicular apophysis. These species lack a tensor tympani muscle, possess complete bullae, and extensions of the middle ear cavity pneumatize the surrounding basicranial bones. The two middle ear cavities communicate in Talpa, Scapanus, and Parascaptor species. Parascaptor has a hypertrophied malleus, a feature shared with Scaptochirus but not found in any other talpid genus. Differences in middle ear morphology within members of the Talpidae are correlated with lifestyle. The species with middle ears closer to the ancestral type spend more time above ground, where they will be exposed to high‐frequency sound: their middle ears appear suited for transmission of high frequencies. The species with derived middle ear morphologies are more exclusively subterranean. Some of the derived features of their middle ears potentially improve low‐frequency hearing, while others may reduce the transmission of bone‐conducted noise. By contrast, the unusual middle ear apparatus of Parascaptor, which exhibits striking similarities to that of golden moles, probably augments seismic sensitivity by inertial bone conduction. J. Morphol.

Seismic sensitivity in the desert golden mole (Eremitalpa granti): A review

Behavioral and anatomical studies relating to possible seismic sensitivity in the desert golden mole (Eremitalpa granti) are reviewed. Field studies in the Namib desert have shown that isolated hummocks of dune grass generate low-frequency vibrations, distinct from the background noise at a distance of many meters. The golden mole apparently uses these cues to orient itself toward the hummocks and the prey species within. An analysis of middle ear morphology suggests that the massive malleus of the golden mole is adapted toward a form of inertial bone conduction, suitable for the detection of seismic cues obtained in this manner. The significance of seismic sensitivity in this golden mole is briefly discussed.

THE MIDDLE EAR APPARATUS OF THE TUCO-TUCO CTENOMYS SOCIABILIS (RODENTIA, CTENOMYIDAE)

Abstract Despite much recent interest in the middle ear and hearing of subterranean mammals, there is very little information in the literature regarding the middle ear apparatus of tuco-tucos (Rodentia: Ctenomyidae). In this study, the middle ear apparatus of Ctenomys sociabilis was dissected and is described for the first time. The middle ear structures of this species proved to be very similar to those of other caviomorph rodents; for example, in the bullet-shaped malleus head and in the fusion of the malleus and incus. The caviomorphs represent a rather conservative group in this respect. The m. stapedius is not present in C. sociabilis—loss of middle ear muscles is a common trend among fossorial mammals, but this particular feature has been reported in many other members of the superfamily Octodontoidea. Although the middle ear apparatus of C. sociabilis includes features consistent with the fossorial paradigm, some of which might be interpreted as low-frequency adaptations, it is not obviously specialized relative to other caviomorphs in this respect.

Mechanics of the frog ear

The frog inner ear contains three regions that are sensitive to airborne sound and which are functionally distinct. (1) The responses of nerve fibres innervating the low-frequency, rostral part of the amphibian papilla (AP) are complex. Electrical tuning of hair cells presumably contributes to the frequency selectivity of these responses. (2) The caudal part of the AP covers the mid-frequency portion of the frogs auditory range. It shares the ability to generate both evoked and spontaneous otoacoustic emissions with the mammalian cochlea and other vertebrate ears. (3) The basilar papilla functions mainly as a single auditory filter. Its simple anatomy and function provide a model system for testing hypotheses concerning emission generation. Group delays of stimulus-frequency otoacoustic emissions (SFOAEs) from the basilar papilla are accounted for by assuming that they result from forward and reverse transmission through the middle ear, a mechanical delay due to tectorial membrane filtering and a rapid forward and reverse propagation through the inner ear fluids, with negligible delay.

Middle Ear Structures of Octodon degus (Rodentia: Octodontidae), in Comparison with Those of Subterranean Caviomorphs

Abstract By comparison with murine rodents such as rats, the middle ear structures of many subterranean mammals appear to be enlarged and thus adapted toward low-frequency sound transmission. However, comparison with closely related terrestrial outgroups has not always been undertaken, and apparent specializations in some cases might reflect phylogeny rather than habitat. Examination of the middle ear of the nonsubterranean degu (Octodon degus) under light microscopy revealed a septated middle ear cavity, a circular tympanic membrane lacking a pars flaccida, a malleus with elongated head, synostosed with the incus, a typically bicrurate stapes, and no stapedius muscle. Many of these features are shared with closely related, subterranean octodontoids in the genera Ctenomys (tuco-tucos) and Spalacopus (coruro). Caviomorph rodents in general share a very similar middle ear morphology, regardless of habitat, which suggests that sensitive low-frequency hearing is plesiomorphic for this group, rather than being specifically associated with a subterranean lifestyle.