Sirpa Nummela

Scaling of the mammalian middle ear

This study considers the general question how animal size limits the size and information receiving capacity of sense organs. To clarify this in the case of the mammalian middle ear, I studied 63 mammalian species, ranging from a small bat to the Indian elephant. I determined the skull mass and the masses of the ossicles malleus, incus and stapes (M, I and S), and measured the tympanic membrane area, A1. The ossicular mass (in mg) is generally negatively allometric to skull mass (in g), the regression equation for the whole material (excluding true seals) being y = 1.373 x(0.513). However, for very small mammals the allometry approaches isometry. Within a group of large mammals no distinct allometry can be discerned. The true seals (Phocidae) are exceptional by having massive ossicles. The size relations within the middle ear are generally rather constant. However, the I/M relation is slightly positively allometric, y = 0.554 x(1.162). Two particularly isometric relations were found; the S/(M + I) relation for the ossicles characterized by the regression equation y = 0.054 x(0.993), and the relation between a two-dimensional measure of the ossicles and the tympanic membrane ares, (M + I)2/3 /A1. As in isometric ears the sound energy collected by the tympanic membrane is linearly related to its area, the latter isometry suggests that, regardless of animal size, a given ossicular cross-sectional area is exposed to a similar sound-induced stress. Possible morphological middle ear adaptations to particular acoustic environments are discussed.

What middle ear parameters tell about impedance matching and high frequency hearing

Acoustic energy enters the mammalian cochlea aided by an anatomical impedance matching performed by the middle ear. The purpose of this paper is to analyse the functional consequences of changes in scale of the middle ear when going from the smallest mammals to the largest. Our anatomical measurements in mammals of different sizes ranging from bats to elephants indicate that middle ear proportions are largely isometric. Thus the calculated transformer ratio is basically independent of animal size, a typical value lying between 30 and 80. Similarly, the calculated specific acoustic input impedance of the inner ear is independent of animal size, the average value being about 140 kPa s/m. We show that if the high frequency hearing limit of isometric ears is limited by ossicle inertia, it should be inversely proportional to the cubic root of the ossicular mass. This prediction is in reasonable agreement with published audiogram data. We then present a three-parameter model of the middle ear where some obvious deviations from perfect isometry are taken into account. The high frequency hearing limits of different species generally agree well with the predictions of this simple model. However, the hearing limits of small rodents clearly deviate from the model calculation. We interpret this observation as indicating that the hearing limit towards very high frequencies may be set by cochlear transduction mechanisms. Further we discuss the exceptional high frequency hearing of the cat and the amphibious hearing of seals.

Eocene evolution of whale hearing

The origin of whales (order Cetacea) is one of the best-documented examples of macroevolutionary change in vertebrates. As the earliest whales became obligately marine, all of their organ systems adapted to the new environment. The fossil record indicates that this evolutionary transition took less than 15 million years, and that different organ systems followed different evolutionary trajectories. Here we document the evolutionary changes that took place in the sound transmission mechanism of the outer and middle ear in early whales. Sound transmission mechanisms change early on in whale evolution and pass through a stage (in pakicetids) in which hearing in both air and water is unsophisticated. This intermediate stage is soon abandoned and is replaced (in remingtonocetids and protocetids) by a sound transmission mechanism similar to that in modern toothed whales. The mechanism of these fossil whales lacks sophistication, and still retains some of the key elements that land mammals use to hear airborne sound.

Sound Transmission in Archaic and Modern Whales: Anatomical Adaptations for Underwater Hearing

The whale ear, initially designed for hearing in air, became adapted for hearing underwater in less than ten million years of evolution. This study describes the evolution of underwater hearing in cetaceans, focusing on changes in sound transmission mechanisms. Measurements were made on 60 fossils of whole or partial skulls, isolated tympanics, middle ear ossicles, and mandibles from all six archaeocete families. Fossil data were compared with data on two families of modern mysticete whales and nine families of modern odontocete cetaceans, as well as five families of noncetacean mammals. Results show that the outer ear pinna and external auditory meatus were functionally replaced by the mandible and the mandibular fat pad, which posteriorly contacts the tympanic plate, the lateral wall of the bulla. Changes in the ear include thickening of the tympanic bulla medially, isolation of the tympanoperiotic complex by means of air sinuses, functional replacement of the tympanic membrane by a bony plate, and changes in ossicle shapes and orientation. Pakicetids, the earliest archaeocetes, had a land mammal ear for hearing in air, and used bone conduction underwater, aided by the heavy tympanic bulla. Remingtonocetids and protocetids were the first to display a genuine underwater ear where sound reached the inner ear through the mandibular fat pad, the tympanic plate, and the middle ear ossicles. Basilosaurids and dorudontids showed further aquatic adaptations of the ossicular chain and the acoustic isolation of the ear complex from the skull. The land mammal ear and the generalized modern whale ear are evolutionarily stable configurations, two ends of a process where the cetacean mandible might have been a keystone character. Anat Rec, 290:716–733, 2007.

Scaling of the cetacean middle ear

Functionally interesting dimensions of the tympano-periotic complex were measured and compared in 18 odontocete and six mysticete species, ranging from small porpoises to the blue whale. We determined (i) the masses of the tympanic and periotic bones (T and P) and of the ossicles malleus, incus, and stapes (M, I and S), (ii) the volume occupied bythe tympanic bone (V), (iii) the areas of the tympanic plate and oval window (A1 and A2), (iv) the thickness of the tympanic plate (D), and (v) the densities of the ossicles (dM, dI, and dS). In most cases, roughly isometric scaling was found in both toothed and baleen whales. P is isometric to T, and the tympanic bone is structurally isometric in all species studied, although not within mysticetes as a group, shown by the isometric relations of V to T, of T(2/3) to A1, and of D to square root(A1). The essentially isometric scaling of the tympanic bone provides a basis for the functional models described by Hemilä et al. (1999). The relation of S to M+I is also isometric, but the relation of M+I+S to T is negatively allometric, as is the relation of A2 to A1, both with slopes close to 2/3. The possible functional implication of this allometry is unknown. The mean ossicular density is 2.64 g/cm3 for odontocetes, and 2.35 g/cm3 for mysticetes. The highly mineralized and convex tympanic plate provides cetaceans with a uniquely large and stiff sound collecting area.

A model of the odontocete middle ear

The high acoustic sensitivity of the bottlenose dolphin is physically defined and related to the anatomy of the middle ear. The paper presents a conceptual and parametric analysis of the demands imposed by this high sensitivity upon the middle ear mechanisms: the head and the middle ear structures must collect sound energy from a large area and concentrate it onto the oval window. Assuming that the specific input impedance of the mammalian cochlea is relatively constant, and smaller than the characteristic acoustic impedance of water, we find that the impedance matching task of the cetacean middle ear is very different from that of terrestrial mammals: instead of a large pressure amplification, cetaceans need amplification of particle velocity. Our mechanical four-bone model of the odontocete middle ear is based on the anatomy of the tympano-periotic complex and consists of four rigid bone units (tympanic bone, the malleus-incus complex, stapes, periotic bone) connected through elastic junctions. The velocity amplification is brought about by lever mechanisms and elastic couplings. The model produced velocity amplifications ranging from 7- to 23-fold when provided with middle ear parameters from the six odontocete species for which audiograms are available. The model reproduces the complete audiograms of these six species fairly well for frequencies up to about 100-120 kHz.

The anatomy of the killer whale middle ear (Orcinus orca).

The paper first reviews our present understanding of the functional morphology of the odontocete (toothed whale) ear. The tympano-periotic complex forming the ear region consists of a ventral bowl-shaped tympanic bone in direct contact with the surrounding soft tissues and the incident sound, and a dorsal periotic bone containing the inner ear. Apparently sound brings the tympanic bone, and especially its thin tympanic plate, into vibration. The ossicles in the air-filled middle ear cavity form a bridge from the tympanic plate to the periotic bone connecting the vibrating plate to the oval window and the inner ear. Our computer tomography (CT) sections and camera lucida drawings reveal two hitherto unknown features of the odontocete ear, both of them of potential relevance to sound reception and impedance matching. (1) It is well known that, in addition to the ossicular chain, two other bone structures connect the tympanic to the periotic bone. We show that the most delicate parts of these extra-ossicular connections consist of thin and folded bony sheets which apparently allow compliance in the tympano-periotic bone contacts and enable plate vibration in relation to the periotic bone. (2) The round head of the malleus, in combination with a fitting round depression on the periotic side, seems to form a joint. We propose that this (hypothetical) joint, together with the adjacent structures, forms a lever producing an amplification of the vibration velocity at the level of the oval window.

CRANIAL ANATOMY OF PAKICETIDAE (CETACEA, MAMMALIA)

Abstract The skulls and isolated tympanics are described for the earliest whales, pakicetids, from the H-GSP Locality 62 in the Ganda Kas area in Northern Pakistan. Currently three pakicetid genera are known: Pakicetus, Ichthyolestes, and Nalacetus. Ichthyolestes is smaller than the two other genera. Nalacetus and Pakicetus are similar in size, but morphologically different. Pakicetids have a nasal opening at the tip of the rostrum. Their palate retains an incisive foramen. This study reveals three characters of the cranial anatomy useful for systematic analyses. In pakicetids the orbits are orientated dorsally, and there is no supraorbital shield. The dorsal orientation of the orbits is diagnostic for the family, and the lack of supraorbital shield distinguishes pakicetids, ambulocetids, and remingtonocetids from the other Eocene archaeocetes. The intertemporal region of the pakicetid skull is very narrow, a feature that also occurs in many other Eocene cetaceans. The tympanic, which is the most abundant cranial bone (more than 30 specimens) in the pakicetid collections from H-GSP Locality 62, can be used to distinguish the species of pakicetids. In Ichthyolestes, the tympanic bulla is of the same absolute size as in Pakicetus, hence relatively larger, and the tympanic bulla of Nalacetus is larger than either of these. Morphologically, the tympanic bullae differ between the genera, and on the basis of these morphologies it is possible to recognize a fourth species of pakicetid at this locality.

Modeling whale audiograms: effects of bone mass on high-frequency hearing

In a previous paper (Hemilä et al., Hear. Res. 133 (1999) 82-97) we have presented a mechanical model, based on species-specific anatomical data, for the toothed whale middle ear. For five odontocete species of six we found that the model quite well predicted published behavioral audiograms. Here we report that new published data indicate that the audiogram of the sixth and deviating species, the killer whale Orcinus orca, was from a specimen with deficient high-frequency hearing. A new published killer whale audiogram is similar to other odontocete audiograms and does fit our four-bone model. With certain general conditions, a model with isometric (middle) ears results in uniform audiograms for different species, when presented in a log-log plot; with larger ears the audiogram curves are just moved towards lower frequencies. The audiograms coincide in case all frequencies are scaled by a factor 1/m3, where m is the mass of the ear ossicles. Odontocete ears are isometric enough to show that the corresponding audiograms are indeed similar after such mass scaling. Specifically, this scaling factor can be used to predict the high-frequency hearing limits of all odontocete species. Our anatomical data and models support the notion that ossicular mass is a crucial factor limiting high-frequency hearing in both terrestrial mammals and toothed whales.

Exploring the mammalian sensory space: co-operations and trade-offs among senses

The evolution of a particular sensory organ is often discussed with no consideration of the roles played by other senses. Here, we treat mammalian vision, olfaction and hearing as an interconnected whole, a three-dimensional sensory space, evolving in response to ecological challenges. Until now, there has been no quantitative method for estimating how much a particular animal invests in its different senses. We propose an anatomical measure based on sensory organ sizes. Dimensions of functional importance are defined and measured, and normalized in relation to animal mass. For 119 taxonomically and ecologically diverse species, we can define the position of the species in a three-dimensional sensory space. Thus, we can ask questions related to possible trade-off vs. co-operation among senses. More generally, our method allows morphologists to identify sensory organ combinations that are characteristic of particular ecological niches. After normalization for animal size, we note that arboreal mammals tend to have larger eyes and smaller noses than terrestrial mammals. On the other hand, we observe a strong correlation between eyes and ears, indicating that co-operation between vision and hearing is a general mammalian feature. For some groups of mammals we note a correlation, and possible co-operation between olfaction and whiskers.