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.     

Ossicular density in golden moles (Chrysochloridae)

The densities of middle ear ossicles of golden moles (family Chrysochloridae, order Afrosoricida) were measured using the buoyancy method. The internal structure of the malleus was examined by high-resolution computed tomography, and solid-state NMR was used to determine relative phosphorus content. The malleus density of the desert golden mole Eremitalpa granti (2.44 g/cm³) was found to be higher than that reported in the literature for any other terrestrial mammal, whereas the ossicles of other golden mole species are not unusually dense. The increased density in Eremitalpa mallei is apparently related both to a relative paucity of internal vascularization and to a high level of mineralization. This high density is expected to augment inertial bone conduction, used for the detection of seismic vibrations, while limiting the skull modifications needed to accommodate the disproportionately large malleus. The mallei of the two subspecies of E. granti, E. g. granti and E. g. namibensis, were found to differ considerably from one another in both size and shape.     

Functional and systematic implications of the ear in golden moles (Chrysochloridae)

Golden moles (Chrysochloridae) are fossorial mammals known to have unusual mallei. The aim of this study was to describe and quantify aspects of the auditory morphology of golden moles in order to determine their systematic and functional implications. Observations were made on skeletal material as well as histological sections. The results of this study do not support the separation of the genus Calcochloris from Amblysomus . It was found that the morphology shared by all the studied genera is indicative of specialization for hearing low frequency sound. The tympanic membrane to stapes footplate ratios, ossicular lever arm ratios and incudomallear joint morphology suggest low frequency specializations in genera with small mallear heads and high frequency specializations in genera with large mallear heads. However, the size and degree of trabeculation of the tympanic cavity are not consistent with this result. It is proposed that all golden moles are low frequency hearers with differences in their range of sensitivity according to how much time they spend foraging above ground.     

Convergence vs. Specialization in the ear region of moles (mammalia)

We investigated if and how the inner ear region undergoes similar adaptations in small, fossorial, insectivoran‐grade mammals, and found a variety of inner ear phenotypes. In our sample, afrotherian moles (Chrysochloridae) and the marsupial Notoryctes differ from most other burrowing mammals in their relatively short radii of semicircular canal curvature; chrysochlorids and fossorial talpids share a relatively long interampullar width. Chrysochlorids are unique in showing a highly coiled cochlea with nearly four turns. Extensive cochlear coiling may reflect their greater ecological dependence on low frequency auditory cues compared to talpids, tenrecids, and the marsupial Notoryctes. Correspondingly, the lack of such extensive coiling in the inner ear of other fossorial species may indicate a greater reliance on other senses to enable their fossorial lifestyle, such as tactile sensation from vibrissae and Eimer's organs. The reliance of chrysochlorids on sound is evident in the high degree of coiling and in the diversity of its mallear types, and may help explain the lack of any semiaquatic members of that group. The simplest mallear types among chrysochlorids are not present in the basal‐most members of that clade, but all extant chrysochlorids investigated to date exhibit extensive cochlear coiling. The chrysochlorid ear region thus exhibits mosaic evolution; our data suggest that extensive coiling evolved in chrysochlorids prior to and independently of diversification in middle ear ossicle size and shape. J. Morphol. 276:900–914, 2015. © 2015 Wiley Periodicals, Inc.     

Iridescent colour production in hairs of blind golden moles (Chrysochloridae)

Relative to other metazoans, the mammalian integument is thought to be limited in colour. In particular, while iridescence is widespread among birds and arthropods, it has only rarely been reported in mammals. Here, we examine the colour, morphology and optical mechanisms in hairs from four species of golden mole (Mammalia: Chrysochloridae) that are characterized by sheens ranging from purple to green. Microspectrophotometry reveals that this colour is weak and variable. Iridescent hairs are flattened and have highly reduced cuticular scales, providing a broad and smooth surface for light reflection. These scales form multiple layers of light and dark materials of consistent thickness, strikingly similar to those in the elytra of iridescent beetles. Optical modelling suggests that the multi-layers produce colour through thin-film interference, and that the sensitivity of this mechanism to slight changes in layer thickness and number explains colour variability. While coloured integumentary structures are typically thought to evolve as sexual ornaments, the blindness of golden moles suggests that the colour may be an epiphenomenon resulting from evolution via other selective factors, including the ability to move and keep clean in dirt and sand.     

A phylogenetic estimate for golden moles (Mammalia,Afrotheria, Chrysochloridae)

Background  

Golden moles (Chrysochloridae) are small, subterranean, afrotherian mammals from South Africa and neighboring regions. Of the 21 species now recognized, some (e.g., Chrysochloris asiatica, Amblysomus hottentotus) are relatively common, whereas others (e.g., species of Chrysospalax, Cryptochloris, Neamblysomus) are rare and endangered. Here, we use a combined analysis of partial sequences of the nuclear GHR gene and morphological characters to derive a phylogeny of species in the family Chrysochloridae.     

Ontogenetic and phylogenetic transformations of the ear ossicles in marsupial mammals

This study is based on the examination of histological sections of specimens of different ages and of adult ossicles from macerated skulls representing a wide range of taxa and aims at addressing several issues concerning the evolution of the ear ossicles in marsupials. Three-dimensional reconstructions of the ear ossicles based on histological series were done for one or more stages of Monodelphis domestica, Caluromys philander, Sminthopsis virginiae, Trichosurus vulpecula, and Macropus rufogriseus. Several common trends were found. Portions of the ossicles that are phylogenetically older develop earlier than portions representing more recent evolutionary inventions (manubrium of the malleus, crus longum of the incus). The onset of endochondral ossification in the taxa in which this was examined followed the sequence; first malleus, then incus, and finally stapes. In M. domestica and C. philander at birth the yet precartilaginous ossicles form a supportive strut between the lower jaw and the braincase. The cartilage of Paauw develops relatively late in comparison with the ear ossicles and in close association to the tendon of the stapedial muscle. A feeble artery traverses the stapedial foramen of the stapes in the youngest stages of M. domestica, C. philander, and Sminthopsis virginiae examined. Presence of a large stapedial foramen is reconstructed in the groundplan of the Didelphidae and of Marsupialia. The stapedial foramen is absent in all adult caenolestids, dasyurids, Myrmecobius, Notoryctes, peramelids, vombatids, and phascolarctids. Pouch young of Perameles sp. and Dasyurus viverrinus show a bicrurate stapes with a sizeable stapedial foramen. Some didelphids examined to date show a double insertion of the Tensor tympani muscle. Some differences exist between M. domestica and C. philander in adult ossicle form, including the relative length of the incudal crus breve and of the stapes. Several differences exist between the malleus of didelphids and that of some phalangeriforms, the latter showing a short neck, absence of the lamina, and a ventrally directed manubrium. Hearing starts in M. domestica at an age in which the external auditory meatus has not yet fully developed, the ossicles are not fully ossified, and the middle ear space is partially filled with loose mesenchyme. The ontogenetic changes in hearing abilities in M. domestica between postnatal days 30 and 40 may be at least partially related to changes in middle ear structures.     

Chromosomal evolution and distribution of telomeric repeats in golden moles (Chrysochloridae, Mammalia)

Golden moles (Chrysochloridae) are small, subterranean mammals endemic to sub-Saharan Africa that together with tenrecs constitute one of six orders in Afrotheria. Here we present a comprehensive karyotypic comparison among six species/subspecies of golden moles based on G-banding and chromosome painting. By expanding the species representation to include a further five species recently published in a companion paper, we were able to map the distribution of telomeric repeats in ten species/subspecies that are representative of six of the nine currently recognized genera. We conclude that: (i) the monophyly of Amblysomus is supported by the amplification of heterochromatin in several pericentric regions and one intrachromosomal rearrangement; (ii) A. hottentotus meesteri groups as sister to a clade that contains A. h. hottentotus, A. h. longiceps, A. h. pondoliae and A. robustus, an association that is underpinned by a shared intrachromosomal rearrangement and the detection of telomeric sequences in the centromeres of all chromosomes of the three A. hottentotus subspecies and A. robustus but, importantly, not in those of A. h. meesteri. These findings indicate an absence of gene flow suggesting that A. h. meesteri should be elevated to specific status. We hypothesize that the lack of gene flow may, in part, reflect hybrid dysgenesis resulting from abnormal meiotic segregation as a consequence of differences in the nature of the centromeric specific satellites; (iii) chromosomes 7 and 13 of Chrysochloris asiatica are fused in both Calcochloris obtusirostris and Eremitalpa granti, but that the position of the centromere in the fused chromosome differs in each species. This suggests that rather than being indicative of common ancestry, the fusion is more likely a convergent character which has arisen independently in each lineage. Furthermore our painting data show two centromeric shifts that are probably autapomorphic for C. obtusirostris. Finally, we conclude that (iv) golden moles are characterized by strong karyotypic conservatism but in marked contrast to the constrained rates of change exhibited by most species, A. robustus is unique in that three autapomorphic fissions define its evolutionary history, and hence the more extensive reshuffling of its genome.     

Atmospheric air vs. normal middle ear gas: Effects on in vitro growth and collagen synthesis in normal middle ear fibroblasts

Summary The present study was undertaken to quantitate the effects of atmospheric air and normal middle ear gas on cultured fibroblasts obtained from normal rabbit middle ear mucosa. The cells were exposed to three different gas compositions: 7% O₂:5% CO₂:88% N₂, 21% O₂:5% CO₂:74% N₂, and 75% O₂:5% CO₂:20% N₂. The growth was monitored by measuring the total content of cell protein, the amount of DNA, and the cell division activity. The activity of the synthetic apparatus was determined by the collagen synthesis. For comparison, rabbit skin fibroblasts were grown under identical conditions. The results demonstrated significantly higher replication rate of middle ear fibroblasts at 7% oxygen than at atmospheric air whereas the collagen synthesis was significantly lower at 7%. Furthermore, the responses varied significantly between rabbit middle ear and rabbit skin fibroblasts. Thus the present study substantiates the hypothesis of an influence of atmospheric air on the middle ear mucosa which might be of importance, e.g., in relation to insertion of ventilation tubes or longstanding perforations of the tympanic membrane in otitis media.     

Acoustic communication and burrow acoustics are reflected in the ear morphology of the coruro (Spalacopus cyanus, Octodontidae), a social fossorial rodent

We studied the middle and inner ears of seven adult coruros (Spalacopus cyanus), subterranean and social rodents from central Chile, using free-hand dissection and routine staining techniques. Middle ear parameters that were focused on here (enlarged bullae and eardrums, ossicles of the "freely mobile type") are believed to enhance hearing sensitivity at lower frequencies. The organ of Corti was of a common mammalian type and revealed three peaks of higher inner hair cell densities. Based on a position frequency map, frequencies were assigned to the respective peaks along the basilar membrane. The first peak at around 300-400 Hz is discussed with respect to the burrow acoustics, while the peak around 10-20 kHz is probably a plesiomorphic feature. The most pronounced peak at around 2 kHz reflects the frequency at which the main energy of vocal communication occurs. The morphology of the ear of the coruro corresponds to the typical pattern seen in subterranean rodents (low frequency and low-sensitivity hearers), yet, at the same time, it also deviates from it in several functionally relevant features.     

Scaling of the marsupial middle ear and its functional significance

The marsupial middle ear performs an anatomical impedance matching for acoustic energy travelling in air to reach the cochlea. The size of the middle ear sets constraints for the frequencies transmitted. For generalized placental mammals, it has been shown that the limit for high-frequency hearing can be predicted on the basis of middle ear ossicle mass, provided that the ears fulfil requirements of isometry. We studied the interspecific size variation of the middle ear in 23 marsupial species, with the following measurable parameters: skull mass, condylobasal length, ossicular masses for malleus, incus and stapes, tympanic membrane area, oval window area, and lever arm lengths for malleus and incus. Our results show that the middle ear size grows with negative allometry in relation to body size and that the internal proportions of the marsupial middle ear are largely isometric. This resembles the situation in placental mammals and allows us to use their isometric middle ear model to predict the high-frequency hearing limit for marsupials. We found that the isometry model predicts the high-frequency hearing limit for different marsupials well, indicating that marsupials can be used as auditory models for general therian mammalian hearing. At very high frequencies, other factors, such as the inner ear, seem to constrain mammalian hearing.     

Study of age-related changes in Middle ear transfer function

Abstract

Osteoporosis (OP) is common with advancing age. Several studies have shown a strong correlation between OP and otosclerosis. However, no studies have investigated OP of the malleus, incus or stapes in the human middle ear, its effect on middle ear transfer function. Here, we investigate whether these three ossicles develop OP, and how this affects middle ear transfer function. The effect of OP on middle ear transfer function was investigated in simulations based on a finite element (FE) method. First, the FE model used in our previous study was refined, and optimized by introducing viscoelastic properties to selected soft tissues of the middle ear. Then, the FE model was used to simulate OP of the three ossicles and assess its influence on middle ear transfer function. Other possible age-related changes, such as stiffness of the joints or ligaments in the middle ear, were also investigated. The results indicated that OP of the ossicles could increase the high frequency displacement of both the umbo and stapes footplate (FP). However, the stiffness of the middle ear soft tissue can lead to the decrease of middle ear gain at lower frequencies. Furthermore, loosening of these joints or ligaments could increase displacement of the umbo and stapes FP. In conclusion, although age-related hearing loss is most commonly conceived of as sensorineural hearing loss (SNHL), we found that age-related changes may also include OP and changes in joint stiffness, but these will have little effect on middle ear transfer function in elderly people.     

The influence of muscles activation on the dynamical behaviour of the tympano-ossicular system of the middle ear

The human ear is a complex biomechanical system and is divided into three parts: outer, middle and inner ear. The middle ear is formed by ossicles (malleus, incus and stapes), ligaments, muscles and tendons, which transfers sound vibrations from the eardrum to the inner ear, linking with mastoid and Eustachian tube. In this work, a finite element modelling of the tympano-ossicular system of the middle ear was developed. A dynamic study based on a structural response to harmonic vibrations, for a sound pressure level (SPL) of 110, 120 and 130 dB SPL applied in the eardrum, is presented. The connection between the ossicles is made using a contact formulation. The model includes the different ligaments considering its hyperelastic behaviour. The activation of the muscles is based on the constitutive model proposed by previous work. The harmonic responses of displacement and pressure obtained on the stapes footplate, for a frequency range between 100 Hz and 10 kHz, are obtained simulating the muscle activation. The results are compared considering the passive and active states. The results are discussed and they are in accordance with audiological data published with reference to the effects of the middle ear muscles contraction.     

Morphometrics of human auditory ossicles from Antinoe Necropolis (Egypt)

Historical evidence suggests that the Christian Coptic population of Antinoe necropolis, probable descendants of Dynastic Egyptians, may reflect admixture from Greek and Roman populations. Within the anthropological surveys on Antinoe skeletal remains (A.D. 300–600), a sample of auditory ossicles was compared with a Dynastic Egyptian sample (“G. Marro” osteological collection), from Asiut and Gebelen Univariate and multivariate statistical analyses were applied, to this end. The auditory ossicles are generally larger in the Coptic group; in both groups shape measurements have a high variability, while size measurements are relatively invariable. Univariate variances are homogeneous but the means are significantly different. This suggests genetic changes, but identical patterns of variation. The stepwise discriminant functions analysis and the Generalized Distance, suggesting a biological heterogeneity in the Antinoe sample in spite of some similarity of the two groups, tend to support this. Further analyses of the auditory ossicles in Greek and Roman populations are however needed to confirm the gene flow hypothesis in the Antinoe population, suggested by historical data.     

Locomotory activity in the Namib Desert golden mole Eremitalpa granti namibensis (Chrysochloridae)

Eremitalpa granti namibensis is a small, blind, subterranean insectivore endemic to the Namib Desert sand dunes. Unlike other subterranean mammals which seldom leave their burrow systems, the Namib mole forages extensively on the dune surface for its insectivorous prey. Activity phasing in this atypical mole was examined in the field and in the laboratory. Free-living moles were almost exclusively nocturnal, while moles kept in the laboratory were active day and night. These findings are discussed in relation to prey availability, predator pressure and avoidance of diurnal extremes. Light and temperature appeared to be important cues for daily onset and cessation of activity.     

Water metabolism in the Namib Desert golden mole, Eremitalpa granti namibensis (Chrysochloridae)

1. Laboratory and field studies of energy and water metabolism employing isotopic dilution methods examined the ability of Namib Desert moles to survive on an insect diet without drinking water. 2. Water independence is achieved through efficient renal function while low rates of energy usage and torpor are further effective in reducing overall water requirements.     

Evolution of the amphibian tympanic ear and the origin of frogs

Recent anurans plus all but the most primitive temnospondyl labyrinthodont amphibians are proposed as a monophyletic taxon, based on shared stapedial characters which are derived with respect to all other tetrapods. Within temnospondyls, the mostly Lower Permian dissorophoids are proposed as most closely related to Recent anurans, based on interpretation of the dissorophoid dorsal quadrate process and the anuran tympanic annulus as sequential steps in a character transformation series. The otic features described here reinforce the concept of the amphibian tympanic ear as a prior "invention" with no genealogical relationship to amniote tympanic ears.     

The epithelium of the middle ear in the guinea pig

Summary An electron microscopic study of aldehyde and osmium fixed normal guinea pig middle ear epithelium was made. Numerous branching microvilli occur between the cilia of the ciliated cells. The granules of the secretory cells are always surrounded by a membrane, and they vary in their content of electron dense substance. Half desmosomes are frequent in basal cells. The squamous epithelial cells of the bulla contain few microvilli and pinocytoric invaginations. In the basal part of the squamous epithelium dilations of the intercellular clefts often occur. The luminal part of the intercellular clefts are closed by multiple tight junctions.