THE ANATOMICAL RECORD 290:716–733 (2007)

Sound Transmission in Archaic andModern Whales: Anatomical
Adaptations for Underwater Hearing
SIRPA NUMMELA,1,2* J.G.M. THEWISSEN,1 SUNIL BAJPAI,3
TASEER HUSSAIN,4 AND KISHOR KUMAR5
1
Department of Anatomy, Northeastern Ohio Universities College of Medicine, Rootstown, Ohio2
Department of Biological and Environmental Sciences, University of Helsinki,
Helsinki, Finland3
Department of Earth Sciences, Indian Institute of Technology, Roorkee,
Uttaranchal, India
4
Department of Anatomy, Howard University, College of Medicine, Washington, DC
5
Wadia Institute of Himalayan Geology, Dehradun, Uttaranchal, India

ABSTRACTThe 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 madeon 60 fossils of whole or partial skulls, isolated tympanics, middle ear
ossicles, and mandibles from all six archaeocete families. Fossil data werecompared with data on two families of modern mysticete whales and ninefamilies 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 lateralwall 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 bonyplate, 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, thetympanic 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 thegeneralized modern whale ear are evolutionarily stable configurations, twoends of a process where the cetacean mandible might have been a keystone
character. Anat Rec 290:716–733, 2007. Ó 2007 Wiley-Liss, Inc.

Key words: aquatic hearing; sensory systems;
mammal; archaeocete; cetacea; Eocene

Grant sponsor: Ella and Georg Ehrnrooth Foundation; Grant
sponsor: National Science Foundation; Grant sponsor: Department of Science and Technology, New Delhi, India.
*Correspondence to: Sirpa Nummela, Department of Biological and Environmental Sciences, University of Helsinki, P.O.
Box 65 (Viikinkaari 1), FI-00014 Helsinki, Finland.
E-mail: snummela@fastmail.fm
Ó 2007 WILEY-LISS, INC.

evolution;

Received 2 March 2007; Accepted 6 March 2007
DOI 10.1002/ar.20528
Published online in Wiley InterScience (www.interscience.wiley.
com).

ANATOMICAL ADAPTATIONS FOR UNDERWATER HEARING

Cetaceans descended from terrestrial mammals around50 million years ago (Thewissen et al., 2001; see also
review in Uhen, 2007, this issue). The cetacean sister groupis one of the artiodactyls (e.g., Luckett and Hong, 1998;
Milinkovitch et al., 1998; Gatesy and O’Leary, 2001; Gingerich et al., 2001; O’Leary, 2001; Thewissen et al., 2001;
Geisler and Uhen, 2003), and among the extant artiodactyls, hippopotamids are the most likely sister group of cetaceans (Nikaido et al., 1999; see also Fisher et al., 2007, thisissue). The order Cetacea can be characterized by theirears (Berta, 1994). The transition from land to water
involved a great number of changes in individual organsystems (see Berta et al., 2006). These different changes
happened in less than 10 million years (Thewissen andWilliams, 2002). The sound transmission mechanism
underwent pervasive anatomical changes that are wellunderstood functionally (Nummela et al., 2004a).
Early whale evolution is well documented in the fossil
record (see reviews by Fordyce and de Muizon, 2001; Thewissen and Williams, 2002). The Eocene cetacean families
Pakicetidae, Ambulocetidae, Remingtonocetidae, paraphyletic Protocetidae, Basilosauridae and paraphyletic
Dorudontidae represent respective higher branches on
the phylogenetic tree of Cetacea (O’Leary, 2001: Geisler
and Sanders, 2003; Geisler and Uhen, 2003).
Regarding pakicetids, Gingerich and Russell (1981)
and Gingerich et al. (1983) provided descriptions of thebraincase and the auditory region of Pakicetus inachus,
and analyzed pakicetid hearing mechanisms in air andwater. Their interpretation was that Pakicetus was
already specialized in aquatic hearing. Oelschläger(1986a,b, 1987, 1990) expanded this work and made further functional inferences. Thewissen and Hussain (1993)
described a Pakicetus incus, the oldest middle ear ossicle
known for cetaceans, and showed that the Pakicetus middle ear is land mammal-like and resembles the modern
artiodactyl incus in relative length of its crura. Luo(1998) and Luo and Gingerich (1999) studied the pakicetid ear structures, and added further details to thefunctional analyses of the transformation of the cetacean
basicranial structures during the evolution of whales.
Nummela et al. (2004a, 2006) provided detailed descriptions of the largest collection of cranial material of all
three pakicetid genera; the corresponding postcranial material is described by Madar (2007). Regarding ambulocetids, Thewissen et al. (1994, 1996) described this new
family while describing the genus Ambulocetus. Much of
the ear material of Ambulocetus is poorly preserved.
Kumar and Sahni (1986) described the ear region ofRemingtonocetus, within their new family Remingtonocetidae, making suggestions of the hearing mechanism of thisspecies. Nummela et al. (2004a) expanded the study of remingtonocetid ear and hearing, with new cranial material,
tympanic bullae, and all three auditory ossicles, and found
the remingtonocetids to be the first cetacean family with awhale hearing mechanism for underwater hearing. The
sound path from water to the inner ear passed through thelower jaw and mandibular fat pad to the tympanic plate, alateral wall of the tympanic bone, to the ossicular chain,and the oval window. This mechanism was fully functional,
although not yet very sophisticated.
The ear morphology of protocetids has been described
for Georgiacetus (Hulbert et al., 1998), Rodhocetus (Gingerich et al., 1994), Gaviacetus, Takracetus, and Dalanistes (Gingerich et al., 1995). Luo (1998), and Luo and

717

Gingerich (1999) described ear morphology of Gaviacetus
and Indocetus and discussed their function and hearing
abilities. Nummela et al. (2004a) described the hearing
function of protocetids, including Indocetus tympanic andmalleus. Geisler et al. (2005) described the ear structures
and the mandible for Carolinacetus. Regarding basilosaurids and dorudontids, Kellogg (1936) described theirauditory morphology in detail, but he did not address
functional aspects of the fossil whale ear.
The most explicit study of functional character transformations in early whales was by Lancaster (1990),
building on earlier work of Fleischer (1978). At the time
when Lancaster wrote his study, early cetacean ears withfunctional interpretations were only known for basilosaurids and dorudontids, and these Eocene whales were
included in the hypothetical transformation series he proposed for the whale ear. Lancaster determined that thelate Eocene whale ear was a highly derived hearing
mechanism capable of sound transmission underwater.
Uhen (1998, 2004), Luo (1998), Luo and Gingerich (1999),
and Nummela et al. (2004a) added functional interpretations based on the morphology of the lower jaw and theear region, which indicate that these animals heard wellin water, and had already relatively good directional
hearing, but did not yet echolocate.

SOUND TRANSMISSIONMECHANISMS IN MAMMALS
Although it has long been known that sound transmission through the cetacean ear differs from that of landmammals (e.g., Norris, 1968; Fleischer, 1978), the function of the middle ear was poorly understood until a generalized model for the hearing mechanism of modern
odontocetes (toothed whales, including dolphins and porpoises) was designed (Nummela et al., 1999a,b; Hemilä
et al., 1999, 2001). This study uses that model to evaluate
sound transmission pathways in the Eocene whale ear. It
will begin with a review of the acoustic differences
between air and water and explain why land mammalears do not function well in water. Then it will review thethree different sound transmission mechanisms found inland mammals and in whales: land mammal sound transmission, modern odontocete sound transmission, andbone conduction. After that, it will describe the morphology and interpret the function of the sound transmission
mechanisms found in Eocene archaeocete whales: pakicetids, ambulocetids, remingtonocetids, protocetids, basilosaurids, and dorudontids. The ancestral land mammal
ear and the modern odontocete ear represent evolutionarily stable configurations (Wagner and Schwenk, 2000),
and together they provide the endpoints of a continuum
that is an example of macroevolutionary change in mammalian evolution (Nummela et al., 2004a).

SOUNDWAVE PROPERTIESIN AIR AND WATERSound propagation in air and water differs due to differences in physical properties in these two media. Here,
we present a brief overview of basic acoustics as background for the functional discussion that follows. Soundvelocity c, sound wavelength k, and sound frequency f are
related to each other as: c ¼ k f.

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NUMMELA ET AL.

Sound velocity in air is approximately 340 m/s, but inwater it is nearly five times higher at 1,530 m/s (varying
slightly with changes in ambient conditions, e.g., temperature, salinity, pressure). The higher sound velocity inwater means that, for a given sound frequency, the wavelength is longer in water than in air. The ratio between
the frequency and the wavelength is inverse; when thesound frequency becomes higher, the wavelength becomesshorter, and vice versa. As shorter wavelengths give better spatial resolution, high frequencies are more suitablefor detecting small objects than are low frequencies, andare used by many animals in echolocation. However, highfrequencies do not carry very far; they attenuate rapidly.
Low frequencies have long wavelengths, attenuate more
slowly than high frequencies, and thus carry over longer
distances. They are more suitable for long-distance communication, whereas high frequencies are better suited
for short distances (see e.g., Richardson et al., 1995; Geisler, 1998).

ACOUSTIC IMPEDANCESound propagation in a particular medium can be characterized by its acoustic impedance. When sound moves
forward from one medium to another, the ratio between
the acoustic impedances of two media dictates how muchenergy will be reflected at the interface of these media.
The larger the ratio, the more energy will be reflected at
the interface.
The acoustic impedances of air and water differ greatly.
The characteristic acoustic impedance is: Z ¼ p/v ¼ q c,
where p is the sound pressure, v is the particle velocity, q is
the density of the medium, and c is the sound velocity inthat particular medium. The densities of air and water areapproximately 1.3 kg/m3 and 1,000 kg/m3, respectively,
and, as shown above, the sound velocity is approximately
five times larger in water than in air. The characteristic
acoustic impedance of air is Zair ¼ 400 Pas/m, and the characteristic acoustic impedance of water is Zwater ¼ 1,500
kPas/m. The specific acoustic impedance of the cochlea
filled with fluid is approximately one-tenth of the characteristic acoustic impedance of water, and thus Zc ¼ 150
kPas/m (see Hemilä et al., 1995). Hence, the specific impedance of the cochlea is much larger than the characteristic
acoustic impedance of air, but again only slightly smaller
than the characteristic acoustic impedance of water.
An equal sound pressure gives air molecules a larger
particle velocity than water molecules, resulting in lower
impedance of air than of water. To overcome an impedance difference between two media, and to decrease theamount of sound reflected at the interface, an impedance
matching device is needed. Such a mechanism adjusts thesound pressure and particle velocity, either by increasing
the sound pressure, and/or decreasing or increasing theparticle velocity between the outer medium and the cochlea (for more details, see the sections on land mammal
and modern odontocete hearing mechanisms).

DIRECTIONAL HEARINGThe ability to determine the direction from which asound is arriving is in general species-specific, and also
varies according to the sound frequency. For determining
the direction of the sound arrival, two different methods

can be used: the interaural time difference, and the interaural intensity difference (see e.g., Masterton et al., 1969;
Heffner, 2004). The interaural time difference is the time
between the arrival of the sound in left versus right ears.
When the sound arrives from front, or from behind, itreaches both ears simultaneously, but by turning thehead from one side to the other the animal can tellwhether the sound arrives from the front or from theback, by determining the time difference between arrivalof the sound at the left and right ears. Whether the interaural time difference can be used for determining thedirection of the sound depends on the size of the head, on
the direction of the incident sound, and on the frequency
of sound. If the interaural distance is large enough in
relation to the wavelength of the arriving sound, the animal can determine the direction of the sound on the basisof the interaural time difference (large enough phasedifference, however smaller than 2p).
However, when the size of the head is very small, thetime between the arrival of the sound in the left and rightears becomes absolutely very short, and no matter how
high frequencies are being heard, the central nervous system is not capable of detecting the differences in arrival
time. However, the sound intensity is generally larger inthe ear where the sound arrives first, and the interaural
intensity difference increases with the frequency. Hence,
directional hearing based on time difference may be goodeven at high sound frequencies, but when the sound ishigh enough, and the animal’s head is small, directional
hearing is based on intensity differences between the left
and right ear, provided that the high-frequency hearing
ability is good. This finding partly explains why it is advantageous for a small animal to hear very high frequencies.
Sound travels approximately five times faster in water
than in air and, at a given frequency, the wavelength inwater is five times longer. This reduces considerably theability to use the interaural time delay between the twoears for sound localization. However, even with thisincrease in velocity and wavelength, the high frequencies
that odontocetes use have short enough wavelengths inrelation to their large head. Hence, the high frequencies
together with a large head compensate for more than thefivefold increase in underwater sound velocity. Indeed,odontocetes are known to have very precise directional
hearing (see Supin et al., 2001), this being partly a prerequisite for their ability to echolocate.

INTENSITY VS. PRESSURE
In the field of acoustics, the sound pressure is of central
importance, because the sound loudness is measured
with pressure meters. However, as the perceived loudness
is roughly proportional to the logarithm of the rms (rootmean square) sound pressure p, the sound loudness,given in decibels dB, is usually expressed using soundpressure level Lp: Lp ¼ 20 dB log p/po.
The reference pressure value po used for sounds in air
is 20 mPa, and in water 1 mPa. When comparing hearing
sensitivity of different terrestrial or aquatic animals at
different frequencies, sound pressure levels are used.
The relevant quantity determining the sensitivity of thecochlea is the incident sound energy. Hence, sound intensity is used when comparing the hearing of a terrestrial
versus an aquatic animal. In the case of a plane wave, theANATOMICAL ADAPTATIONS FOR UNDERWATER HEARING
2

intensity I of the sound wave is: I ¼ p /Z, where Z is thecharacteristic acoustic impedance of the medium, Zair or
Zwater. The ratio Zwater/Zair is quite large, approximately
3,700. Hence, when comparing plane waves of equal intensities in air and water, the sound pressure in water islarger. Using the conventional reference pressure po valuesof 20 mPa (for air) and 1 mPa (for water), the waves haveequal intensities when the sound pressure level Lp of theaquatic wave is 61.8 dB larger than sound pressure level
Lp of the wave in air. Thus, a terrestrial animal and an
aquatic animal have equal sensitivities if the threshold Lp
value of the aquatic animal is 61.8 dB larger than thethreshold Lp of the terrestrial animal.

719

The basic function of the land mammal ear in hearing
is well understood over a wide range of frequencies (e.g.,
Henson, 1974; Fleischer, 1978; Fay, 1988; Geisler, 1998;
Rosowski and Relkin, 2001). Figure 1A shows a diagramof a generalized land mammal ear. Sound is collected by
the outer ear pinna, and travels through the external auditory meatus (EAM) to the tympanic membrane (TyMe),
where it sets up vibrations. In the middle ear cavity, thethree middle ear ossicles, malleus, incus, and stapes(Mal, Inc, Sta), form an ossicular chain between the tympanic membrane and the oval window (OvW) of the cochlea. The outermost ossicle, the malleus, is attached to the
tympanic membrane through its manubrium (Fig. 2A),
and the footplate of the stapes sits at the oval window.
Malleus and stapes are connected by the incus. The vibrations of the tympanic membrane are transmitted throughthe middle ear ossicles to the oval window, where themovements of the stapes footplate set the inner ear fluid
into motion. The tympanic bone (TyBo) and the periotic
bone (Per) have large contacts with each other (PeTy),

and the periotic is in close contact to the squamosum andother skull bones (Sk). As a result, the ear is not acoustically isolated from the skull and sound waves can travel
through the skull (see Bone Conduction below). The mandible (Man) is not involved in sound transmission.
When hearing in air, airborne sound is transmitted
from lower acoustic impedance of air (Zair ¼ 400 Pas/m) tomuch higher acoustic impedance of the inner ear fluid(Zc ¼ 150 kPas/m). In a land mammal ear, reflection ofsound is avoided by the insertion of the middle ear whichacts as an impedance-matching device between the air
and the inner ear.
The impedance matching in a land mammal ear isaccomplished by increasing the pressure p and by
decreasing the particle velocity v between the tympanic
membrane and the oval window (Z ¼ p/v, see above). The
pressure can be increased by transmitting sound from alarger to a smaller area. This is done with the help of
the tympanic membrane A1 and the oval window area A2.
The area ratio between these two is A1/A2. The particle
velocity can be decreased by having the malleus lever arm
l1 longer than the incus lever arm l2. With the lever ratio
l1/l2 > 1 between the malleus and the incus lever arms,
the particle velocity between the tympanic membrane andthe oval window is decreased. The product of the area ratio and the lever ratio, A1/A2 3 l1/l2, is called the geometric transformer ratio of the mammalian middle ear. With
this mechanical transformer, it is possible to minimize
reflection of sound energy at the tympanic membrane—inother words, the middle ear input impedance is matchedwith the input impedance of the cochlea.
In addition to the impedance matching function, themammalian middle ear also functions as an intensity amplifier. The intensity amplification is accomplished whenenergy is transferred from a larger to a smaller area, inthis case from the tympanic membrane to the oval window. In a land mammal ear, the area ratio between theFig. 1. A: Diagram of the land mammal ear. B: Diagram of themodern odontocete ear. For technical reasons, the mandibular foramen and the mandibular fat pad are shown on the lateral side of themandible, although they in reality are situated on the medial side.
Abbreviations in Figures 1 and 7: Coc, cochlea; Dom, dome-shaped
depression for periotic; EAM, external acoustic meatus; FaPa, mandibular fat pad; Inc, incus; Inv, involucrum; Mal, malleus; Man, mandi-ble; MeTy, medial synostosis between periotic and tympanic bone, incetaceans this synostosis is absent and is homologous to a gap
between these bones (‘‘MeTy’’); OvW, oval window; Per, periotic bone;
PeTy, joint between periotic and tympanic; Sin, air sinuses; Sk, skull;
Sta, stapes; TyBo, tympanic bone; TyMe, tympanic membrane; TyPl,
tympanic plate. Reprinted by permission from MacMillan Publishers
Ltd: Nature (Nummela et al., 2004a).

LAND MAMMAL EAR AND HEARING720

NUMMELA ET AL.

Fig. 2. Middle ear ossicles of fossil and modern mammals. A: Leftmalleus and incus of Sus scrofa. B: Left malleus and incus of Lagenorhynchus. C: Left malleus and incus of Lagenorhynchus in situ. D: Left incus ofPakicetus (H-GSP 91035). E: Left malleus and incus of Remingtonocetus(IITR-SB 2914). F: Left malleus and incus of Remingtonocetus in situ (IITRSB 2828). G: Right malleus of Indocetus (LUVP 11034). H: Right malleus
and incus of Basilosaurus, posterior view (LSUMG V1). I: Left incus ofBasilosaurus, posterior view (LSUMG V1). J: Left incus of Basilosaurus, anterior view (LSUMG V1). K: SEM photograph of the Pakicetus incus. L:

Right incus of Lagenorhynchus. M: Left ear of Remingtonocetus before
the tympanic bulla was removed, showing the ossicles in situ, lateral view.
N: Ventral view of the same ear, with tympanic membrane reconstructedin the middle ear cavity. Ossicles in A, B, D, E, and G are drawn perpendicular to the plane of the lever arms. Abbreviations: CrL, crus longum; Inc,
incus; Mal, malleus; Mn, manubrium; PrGr, processus gracilis; Sta, stapes;
TyMe, tympanic membrane; TyR, tympanic ring. Scale bar ¼ 5 mm in A–L;
2 cm in M,N. Adapted by permission from MacMillan Publishers Ltd: Nature (Thewissen and Hussain, 1993), and (Nummela et al., 2004a).

tympanic membrane and the oval window serves twofunctions: impedance matching and intensity amplification. Moving hardware models originally designed by
Tom Reuter and Simo Hemilä for the terrestrial mamma-

lian ear and the modern odontocete ear can be foundas video versions on the Web page for whale hearing:
http://www.neoucom.edu/DEPTS/ANAT/Thewissen/whale_
origins/index.html.

ANATOMICAL ADAPTATIONS FOR UNDERWATER HEARING

Fig. 3. Medial view of lower jaw showing the mandibular foramen
size. A: Right mandible of deer, Odocoileus. B: Left mandible of dolphin, Lagenorhynchus. Scale bar ¼ 5 cm.

MODERN ODONTOCETE EAR AND HEARINGThe modern odontocete ear is suitable for hearing
underwater sound (Reysenbach de Haan, 1957; Fleischer,
1978; see also Oelschläger, 1990; Ketten and Wartzok,
1990; Ketten, 1992, 2000). Figure 1B shows a diagram ofthe odontocete ear. Modern odontocetes have lost theirouter ear pinna, and the external auditory meatus is partially occluded and not functional in hearing. The mandible has a wide mandibular canal, which opens posteriorly
as a mandibular foramen on the medial side of the jaw(Fig. 3B). The mandibular canal is filled with a fat pad,an oily substance with a density close to that of sea water(Varanasi and Malins, 1971, 1972). Sound is collected by
the lateral mandibular wall (Norris, 1968), and guided
through the mandibular fat pad (FaPa) (Fig. 1B) up to
the tympanic plate (TyPl), and the lateral wall of the tympanic bone (TyBo), causing it to vibrate. Experimental
results support this mandibular sound route at higher
frequencies (e.g., Bullock et al., 1968; McCormick et al.,1970; Møhl et al., 1999). However, there is also evidence
showing that the head region close to the external auditory meatus is sensitive to lower-frequency sounds (Bullock et al., 1968; Popov and Supin, 1990; Supin et al.,2001).
When sound moves from the mandibular fat pad to thesmaller tympanic plate, the intensity is amplified, leading
to better sensitivity. In the middle ear cavity, the three
middle ear ossicles, malleus, incus, and stapes, form anossicular chain, as in the land mammal ear. The ossicular
chain is situated between the tympanic plate and the oval
window of the cochlea, the malleus is connected to the
tympanic plate with a bony ridge, the processus gracilis(Fig. 2B). The malleus has lost its manubrium, which inland mammals contacts the tympanic membrane. The
tympanic membrane is still left in the odontocete ear, inthe form of an elongated tympanic ligament, and it
attaches to the malleus with its medial tip (Fig. 2C). The
vibrations of the tympanic plate are transmitted throughthe middle ear ossicles to the oval window (Hemilä et al.,
1999; Nummela et al., 1999a), similarly to the land mammal ear. The anatomy of the tympanic bone is different
from that of other mammals; the lateral wall is thin, as inmammals in general, but the medial wall is a thick bulky
structure, called the involucrum (Inv). The contact
between the tympanic bone and the periotic bone (Per) is
reduced (PeTy), and thin bony ridges occur on the tympanic side (see computed tomography scans in Nummela
et al. 1999a). The whole tympanoperiotic complex ispachyosteosclerotic with a density higher than that foundin any other mammal: 2.7 g/cm3 (Giraud-Sauveur, 1969;

721

Lees et al., 1983; Nummela et al., 1999b). This bony complex is acoustically isolated from the skull through air
sinuses (Sin) between the periotic and the other skull
bones (Sk).
In an odontocete ear, waterborne sound is transmitted
from higher acoustic impedance of water (ZW ¼ 1,500
kPas/m) to lower acoustic impedance of the inner ear fluid(Zc ¼ 150 kPas/m). This is a rather small impedance mismatch, leading to an approximately 5 dB sound pressure
decrease. However, when the sound vibrations are transmitted from a large tympanic plate area to a smaller oval
window, the intensity is increased, which improves thehearing sensitivity, but also the pressure is increased andthis leads to a large impedance mismatch. Due to the thinbony ridges between the tympanic and the periotic, andalso due to the massive and dense periotic and involucrum, the vibration of the tympanic plate is approximately rotational. In this way, the tympanic plate forms alever, which reduces pressure and increases the particle
velocity. In the ossicular chain, the malleus head together
with the incus rotates as a pivot in the epitympanic
recess. Here again is a lever with the stapes footplate at
the oval window (OvW). This second lever also decreases
pressure and increases the particle velocity of the system.

HEARING THROUGH BONE-CONDUCTIONMECHANISM
In addition to the land mammal and the modern odontocete hearing mechanisms described above, a third
hearing mechanism can be described for mammals: boneconducted hearing (Lombard and Hetherington, 1993).
Bone conduction occurs when sound is transferred from asurrounding medium to the cochlea through vibrations of
the soft tissues and bony parts of the head directly,
instead of the air passage in the external auditory meatus, or the mandibular fat pad route. A common way to
divide between different types of bone conduction is tofocus on which anatomical components are mainly
involved: outer ear, middle ear, and inner ear; this gives
at least three different types of bone conduction (Tonndorf, 1968). Another way is to focus on function; two generally accepted mechanisms for bone-conducted hearing
are the compressional and the inertial bone conduction.
In the compressional model, a pressure differential develops across the cochlear partition of the inner ear. In theinertial model, relative motion between the ossicular
chain and the temporal bone leads to cochlear stimulationmuch the same way as in air-conducted hearing of landmammals. Both of these models eventually lead to displacement of the basilar membrane, which will create aneural impulse.
Barany (1938) has argued that, in the mammalian middle ear, bone conduction is minimized when the mass center point coincides with the rotational axis of the ossicular chain. This may be of importance when chewing creates a lot of noise, as in terrestrial herbivore mammals.
However, bone conduction becomes a useful hearing
mechanism in a habitat where the density of the surrounding medium is similar to the density of the body tissues. This means similar impedances, and that soundvibrations can easily penetrate the body tissues, with little attenuation. The density of water is close to the density of soft body tissues, and in water most animals hearthrough bone conduction, at least to some degree. A nota-

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ble exception is the Odontoceti (toothed whales), whichhave air cushions that isolate the ears effectively fromthe skull.
The movement of the inner ear fluid in the cochlea
caused by bone conduction can even be enhanced by morphological changes in the middle ear ossicles, by moving
the mass center point away from the rotation axis, which
results in different phases of vibration between theossicles and the inner ear fluid. This kind of enhancement
has evolved in modern mammals, e.g. in phocids and odobenids, in which the incus is inflated (Repenning, 1972;
Nummela, 1995), and in some fossorial insectivores androdents where the malleus is inflated (Cooper, 1928; Stroganov, 1945; Fleischer, 1973; Mason and Narins, 2001;
Willi et al., 2006). A disadvantage of bone conduction isthat directional hearing is poor when the whole headvibrates, and there is no interaural time or intensity difference available. This is a well-known phenomenon forhuman divers, too. When an animal’s head is underwater, bone conduction can only be prevented by isolating
the ears from the skull, as is the case in the modern odontocete ear.
In this study, the evolution of underwater hearing incetaceans is described using fossils. Previous studies ofthis evolutionary pattern (Fleischer, 1978; Lancaster,
1990; Thewissen and Hussain, 1993) were hampered by
the paucity of Eocene whale ear ossicles and the lack ofan understanding of the function of the middle ear inmodern whales. We here use the functional model of
Hemilä et al. (1999, 2001), and Nummela et al. (1999a,b),
and expand on the analysis of Nummela et al. (2004a) tobuild a comprehensive evolutionary model of evolving
sound transmission mechanisms during the period whencetaceans became aquatic. Our study does not address
the functional changes in the inner ear (but see Ketten,
1992, 2000; Parks et al., 2007, this issue), and leaves
open the question of the origin of low-frequency hearing
in mysticetes.

MATERIALS AND METHODS
Fossil material was studied for all six archaeocete families. The material consists of whole or partial skulls,
isolated tympanics, middle ear ossicles, and mandibles.
Mandibles from modern cetaceans were also studied.
Comparative data on modern mammalian ears is basedon Nummela (1995) and Nummela et al. (1999b, 2004a),
as well as new measurements (Table 1). The analysis presented here for the pakicetid hearing mechanisms isbased on a large collection of cranial material of
pakicetids described by Nummela et al. (2004a, 2006);
descriptions for mandibles can be found in Thewissen andHussain (1998). All the fossil cetacean material studied islisted in Appendix 1.

Parameters Measured
The bicondylar width was measured for our sample ofarchaeocetes and some modern cetaceans. Data for some
additional modern cetaceans were kindly provided by
Terry Lancaster and Mark Uhen. Table 1 lists morphometric data for fossil and modern cetaceans. The
bicondylar width was used to estimate the body mass fordifferent species. Body size is of great importance as
many variables in the skull scale with it. Body size wasestimated following Marino et al. (2004) who found thatthe bicondylar width correlated strongly with body mass.
Bicondylar width could not be measured on the specimens of the protocetids Indocetus and Babiacetus. Therefore, bicondylar width was estimated for these taxa by
scaling cheektooth/bicondylar width relations in the
protocetid Georgiacetus (Hulbert et al., 1998).
Measurements were made of the minimum thickness of
the lateral mandibular wall along the transect that was
located at three quarters of the foraminal length, measured from the posterior end of the foramen (thickness T3
in Nummela et al., 2004b, and in Table 1). Minimum
thickness for mandible was determined by running aclosed Dyer gauge caliper vertically along this transect
and recording the true minimum value of transect. Measurements were also made of the height of the mandibularforamen along this same transect (H3 in Table 1). Additionally, measurements were taken of the bicondylar
width and the mandibular foramen height for five noncetacean mammals: the black bear (Ursus americanus),
horse (Equus caballus), one-humped camel (Camelus
dromedarius), pronghorn antelope (Antilocapra americana), and goat (Capra sp.).
The tympanic membrane and the tympanic plate area
were determined using a method described by Nummela(1995) and Nummela et al. (1999b), respectively. A Dyer
gauge caliper (301-204) was used to measure thickness ofthe tympanic plate. Tympanic plate thickness is the minimum thickness of this plate as determined by measuring
at least five representative areas. The tympanic plate
thickness could not be measured for the Gaviacetus bulla,as the plate is badly eroded on both sides.
Ossicular mass is a variable of great importance inacoustic studies. Because the specific weight of bone may
change during fossilization, a range for the ossicularmass was calculated by determining the volume of thefossil ossicle and multiplying it by the minimum andmaximum specific weights known for mammalian bone(land mammals, 2.0 g/cm3, and odontocetes, 2.7 g/cm3;
Giraud-Sauveur, 1969; Nummela et al., 1999b; see also de
Buffrénil et al., 2004). The minimum and maximum mass
values received are both given in Table 1.

RESULTS
The auditory anatomy of the families of archaic
cetaceans is described in this section with a focus on comparing the functional components of hearing, not on morphological details. The sound path of the Eocene cetaceanfamilies is presented, starting with the mandible andmandibular fat pad (if present), the tympanic and periotic
bones, tympanic membrane and/or tympanic plate, andthe middle ear ossicles. Expanding on the quantitative
analysis on ear ossicle parameters by Nummela et al.
(2004a), metric data on these listed elements are summarized in Table 1, and performed as bivariate plots in
Figures 4–6. The plots cover the functionally most important aspects of mandibular, tympanic, and middle ear
ossicle morphology.

Pakicetids
The mandibular foramen in the lower jaw of pakicetids
is small (Fig. 4A), and indicates that no mandibular fat
pad was present in the alveolar canal of these earliest

TABLE 1. Morphometric data for cetaceans

ARCHAEOCETI
Pakicetidae
Pakicetus attocki
Ichthyolestes pinfoldi
Ambulocetidae
Ambulocetus natans
Remingtonocetidae
Remingtonocetus
Protocetidae
Babiacetus
Indocetus ramani
Basilosauridae
Basilosaurus cetoides
Dorudontidae
Zygorhiza
MYSTICETIBalaenidae
Balaena glacialis
Balaena mysticetus
Balaenopteridae
Megaptera novaeangliae
Balaenoptera borealis
Balaenoptera physalus
Balaenoptera musculus
ODONTOCETI
Physeteridae
Physeter catodon
Kogiidae
Kogia breviceps
Ziphiidae
Ziphius cavirostris
Hyperoodon ampullatus
Mesoplodon europaeus
Mesoplodon bidens
Platanistidae
Platanista gangetica
Iniidae
Inia geoffrensis
Pontoporiidae
Pontoporia blainvillei
Monodontidae
Delphinapterus leucas
Monodon monoceros
Delphinidae
Steno bredanensis
Tursiops truncates
Stenella attenuate
Stenella frontalis
Delphinus delphis
Lagenorhynchus albirostris
Lagenorhynchus acutus
Lagenorhynchus obliquidens
Lagenorhynchus australis
Lissodelphis borealis
Grampus griseus
Feresa attenuate
Pseudorca crassidens
Orcinus orca
Globicephala melas
Phocoenidae
Neophocaena phocaenoides
Phocoena phocoena
Phocoenoides dalli

A1 (mm2)

M (mg)I (mg)

MþI (mg)

TPT (mm)

T3 (mm)

H3 (mm)BCW (mm)

350 (41.82)–––

20–271
–

–
–

0.88
–

1.51
1.45

6.88
7.8

50.4
42.48

–

–

–

–

–

2.4

48.9

76.48

1.2

1.6

–

82.76

1

922 (83.78)––

200–270–1225–
144–1941

–
–

–
–

–
1.07

3.76
2.8

54.8
–

128
70.12

2295

340–4601

160–2161

500–6761

1.94

–

–

144.8

1580

176–3731

120–1621

396–5351

1.55

3.15

101

119

5887
6071

1331
918

516
407

1847
1317

3.08
3.13

–
–

–
–

–
–

5383
5132
6508
5979

2012
2133
3077
2303

549
850
1230
894

2561
2983
4307
3197

2.21
2.54
2.45
2.23

–
–
–
–

–
–
–
–

–
282
–
435

1605

400

324

724

1.23

–

–

–

–

–

–

–

–

0.74

47.5

92.75

–
1286
–
750

–
351
–
156

–
122
–
64

–
473
–
220

–
1.77
–
1.08

1.33
1.35
1.51
1.15

66.5
103
81
57.8

158.1
205
113.2
103.7

930

278

54.2

332.2

1.364

0.3

25

–

522

158

34.8

192.8

0.955

2.0

44.5

79.5

–

–

–

–

–

0.94

24.5

61.5

525
662

204
260

50.5
62.1

254.5
322.1

0.762
0.866

1.84
1.03

54.37
66.65

142.5
151.9

505
539
–
318
348
446
336
–
–
–
546
–
741
1828
625

143
203
–
76.3
92.8
134
92.3
–
–
–
204
–
326
757
187

32.7
48.8
–
19.1
21.5
38.9
22.1
–
–
–
52.1
–
89.6
213
55.2

175.7
251.8
–
95.4
114.3
172.9
114.4
–
–
–
256.1
–
415.6
970
242.2

0.744
0.77
–
0.638
0.511
0.656
0.57
–
–
–
0.72
–
1.022
1.232
0.8

1.94
2.03
1.13
2.26
1.14
1.53
1.24
0.99
1.13
0.95
2.38
1.15
2.8
5.48
1.5

38.4
57.6
32
38.64
26.72
45.28
27.87
38.5
36.95
28.29
61.5
41.03
57.83
139
82.95

96.74
115.5
78.26
95.06
88.94
96.45
83.84
91.78
82.37
83.11
100.5
81.16
151.7
206
173.6

–
333
–

–
58.9
–

–
14.9
–

–
73.8
–

–
0.609
–

0.57
0.57
0.57

23.91
29.5
38

74.58
64.36
81.3

a
Due to possible changes during the fossilization process, minimum and maximum mass values were received for fossil
cetacean ossicles; see Materials and Methods.
Data partly collected from: Nummela et al. (1999b, 2004a,b).
A1 Sound input area; tympanic plate area, for Pakicetus and Remingtonocetus, also the tympanic membrane area is given
in parentheses.
M Malleus mass.
I Incus mass.
MþI Malleus þ Incus combined mass.
TPT Tympanic plate thickness.
T3 Minimum thickness of the lateral mandibular wall (see Materials and Methods).
H3 Height of the mandibular foramen (see Materials and Methods).
BCW Bicondylar width.

724

NUMMELA ET AL.

Fig. 4. Variation of the mandibular foramen height and the mandibular lateral wall thickness at theposterior part of the mandible in archaeocetes and modern odontocetes. A: Mandibular foramen heightvs. bicondylar width. B: Lateral wall thickness of the mandible vs. bicondylar width. Odontocete data
points clustered within the circle. Symbol chart applies to Figures 4–6.

Fig. 5. Variation of the area and thickness of the sound input area of the tympanic bulla, the tympanic
plate in archaeocetes and modern odontocetes. A: Tympanic plate area vs. bicondylar width. B: Tympanic
plate thickness vs. bicondylar width. For symbols, see Figure 4A.

whales. The mandibular foramen height of Pakicetus andIchthyolestes, rather than following the other cetaceans,
falls within a group of noncetaceans including: the pronghorn antelope (Antilocapra americana), the goat (Caprasp.), the black bear (Ursus americanus), the horse (Equus
caballus), and the one-humped camel (Camelus dromedarius), the three first-mentioned being closest to the
pakicetids (Fig. 4A). The lateral mandibular wall is also
relatively thick (Fig. 4B). In the absence of a mandibular

fat pad as a sound channel to the ear, the lateral mandibular wall could not function as a sound receiver in pakicetid hearing in water.
In all cetaceans, including pakicetids, the tympanic
bulla has a thick medial part, the involucrum, and amuch thinner lateral wall. The area of the lateral tympanic wall does not as such deviate from the fossil ormodern whales (Fig. 5A). The absolute thickness of thislateral wall falls in the same range as that of the smallest

ANATOMICAL ADAPTATIONS FOR UNDERWATER HEARING

725

Fig. 6. Variation of middle ear ossicular mass along the soundinput area in different mammals. For sound input area, we used the
tympanic membrane area for land mammals, seals, pakicetids, andremingtonocetids, and the tympanic plate area for remingtonocetids,
protocetids, basilosaurids, and dorudontids. The phocids form theirown group by having more massive ossicles than the land mammals,
especially the incus. A: Combined mass of malleus and incus vs.
sound input area. Remingtonocetus is shown twice, with its ossicularmass plotted against the tympanic membrane area (hearing in air) andthe tympanic plate area (hearing in water). B: Malleus mass vs. soundinput area. C: Incus mass vs. sound input area. The Remingtonocetus
could not be included in B and C, because its malleus and incus are
not separated from each other. Abbreviated names for the different
genera are used, their family level shown by symbols as indicated in
Figure 4A. Additionally, following Geisler et al. (2005), Gaviacetus isregarded to be a protocetid. Adapted by permission from Macmillan
Publishers Ltd: Nature (Nummela et al., 2004a).

odontocetes measured, but when body size is taken into
account, the lateral tympanic wall of pakicetids is relatively thick. However, its thickness can be seen to coincide along the thickness line for the Eocene cetaceans(Fig. 5B).
The tympanic bone makes contact with the periotic
bone, which is firmly attached to the skull, with no space

for air sinuses isolating it acoustically from the surrounding skull bones. In the holotype braincase of Pakicetus
inachus (Gingerich and Russell, 1981), the involucrum of
the tympanic bone does contact the basioccipital due to a
deformation (Nummela et al., 2006).
The skull morphology reveals that the external auditory meatus was present and patent. On the medial side

726

NUMMELA ET AL.

Fig. 7. A: Diagram of the pakicetid ear. The malleus is supposed to have been of land mammal type,and its position is shown with a dotted line. B: Diagram of the remingtonocetid/protocetid ear. For abbreviations, see Figure 1. Adapted by permission from Macmillan Publishers Ltd: Nature (Nummela et al.,2004a).

of the lateral wall of the tympanic bulla, the shape of the
tympanic ring suggests that the tympanic membrane
attaching to the ring in life was of the land mammal type.
One ossicle, the incus, is preserved for Pakicetus. The
incus is relatively heavy in relation to the sound input
area, but still clusters with modern land mammals (Fig.
6C). The Pakicetus incus resembles that of artiodactylswith its crus breve as long as the crus longum (Fig. 2;
Doran, 1879; Fleischer, 1973; Thewissen and Hussain,1993). Generally, the shape of the incus and of the tympanic ring are of land mammal type and indicate that themalleus was of land mammal type too, attaching to the
tympanic membrane with its manubrium.
A diagram of the pakicetid ear function is presented in
Figure 7A. Results suggest that these earliest whales
probably used normal land mammal hearing in air, wheresound vibrations reached the tympanic membrane
through the external auditory meatus, and were transmitted further by the ossicular chain to the cochlea. Pakicetids most likely used bone conduction for hearing inwater, given the close contact between the periotic bone
and the skull, and the relatively massive incus. The lackof a mandibular fat pad and the close connection between
the periotic and the skull indicate that the lateral tympanic wall was not functionally significant in their hearing mechanism in water, and the modern odontocete
hearing mechanism was not present. Directional hearing
in water was poorly developed.

Ambulocetids
The Ambulocetus head and mandible are massive. The
mandibular foramen is large enough to place the Ambulocetus among the modern odontocetes (Fig. 4A), and thelateral mandibular wall is relatively thick, at the upper
end of modern odontocetes, but well among the other
Eocene whales (Fig. 4B). These results suggest that a fat
pad was present for sound transmission through thelower jaw to the tympanic bone, although a thick mandibular wall suggests low sensitivity in hearing.
The tympanic bulla has a thick and massive involucrum on its medial side and a thin tympanic plate laterally. In the only known specimen with ears (Thewissen

et al., 1996), the lower jaw and the auditory bulla have abony contact unlike any other cetacean. Nothing is knownof the tympanic membrane and the ear ossicles of Ambulocetus.
The contact between the auditory bulla and the lower
jaw suggests that hearing of Ambulocetus was mainly
through bone conduction in water and that it lacked thespecial modern odontocete hearing mechanism. On land,
Ambulocetus may also have relied on substrate-borne
vibration (Thewissen et al., 1996), by pushing the headagainst the ground. In water, sound could travel directlyfrom the surrounding water through the tissues to reachthe ear. Most likely their hearing was in the lowfrequency range; frequencies of around 440 Hz are known
to propagate best in soil (Heth et al., 1986).

Remingtonocetids
The lower jaw of Remingtonocetus has a large mandibular foramen (Thewissen and Bajpai, 2001a). The lateralmandibular wall is thinner than in pakicetids and ambulocetids, placing remingtonocetids among the modern
cetaceans, and indicating synapomorphism between remingtonocetids and later cetaceans in this respect (Fig.
4B).
The external auditory meatus was present. The tympanic bone has a thick medial involucrum and a thin lateral tympanic plate. The tympanic contacts the periotic,
which is surrounded by some air sinuses, but still has
close contact to the skull. This finding was also noticed by
Sahni and Mishra (1972, 1975) in Remingtonocetus,
which was originally identified by them as a protocetid
but later reinterpreted (Kumar and Sahni, 1986; Williams, 1998). The tympanic plate area of Remingtonocetus
is similar in size to archaeocetes, being larger than inmodern odontocetes (Fig. 5A). The tympanic plate thickness shows the same pattern; it is larger than in modern
odontocetes, but does not separate remingtonocetids fromother archaeocetes (Fig. 5B).
The tympanic ring on the medial side of the tympanic
plate and the parts of the plate just lateral to the ring areof land mammal type. This, and the presence of the external auditory meatus, suggest that the sound path forANATOMICAL ADAPTATIONS FOR UNDERWATER HEARING

727

Fig. 8. A generalized phylogeny for the cetaceans discussed inthis study, listing the characters relevant to hearing during the evolution of whales. Different sound transmission mechanisms used in air
and water by different cetacean taxa are shown in boxes above thecladogram. The cetacean sister group is here indicated as ‘‘land mammals,’’ they used the generalized mammalian sound transmission system. Adapted with permission from Macmillan Publishers Ltd: Nature(Nummela et al., 2004).

air-conducted hearing was still present. The ear ossicles
resemble the modern cetacean ossicles morphologically incertain respects. The malleus has a large head and it has
lost the manubrium, but has a well-developed processus
gracilis, which makes a bony connection to the tympanic
plate of the tympanic bulla (Fig. 2). The malleus shapeindicates that the tympanic membrane was an elongatedligament that attached laterally to the tympanic ringinside the auditory bulla, and medially to the malleus
with its tip. The crus breve and crus longum of the incus
are similar in length. Overall remingtonocetid ossicles
look like modern odontocete ossicles but minor morphological differences do exist. The ossicular chain is notreoriented. The incus is still relatively large (Fig. 2),
unlike in modern odontocetes, where the incus is verysmall in relation to the malleus.
Possible similarities between the remingtonocetid ear,the land mammal ear, and the odontocete ear were studied using both the tympanic membrane area and the tympanic plate area in the analysis with the middle ear
ossicles (Fig. 6). The ossicular mass (malleus þ incus)
related to the tympanic membrane area in Remingtonocetus resembles that of modern phocids (Fig. 6A), who haveenlarged middle ear ossicles, and deviate from the general mammalian pattern in this respect (Repenning,
1972; Nummela, 1995). The extra mass of the ossicles
most likely helped bone-conducted hearing underwaterby increasing the mass inertia of the ossicles and also by
moving the rotational axis and the mass center point
apart from each other. These features suggest an
increased phase difference between the vibration of theossicles and the vibration of the inner ear fluid. The ossicular mass related to the tympanic plate area is similar in
Remingtonocetus and modern odontocetes (Fig. 6A), leading to a functional interpretation that the remingtonocetids had a fully aquatic ear.
A diagram interpreting the function of the remingtonocetid/protocetid hearing mechanisms is presented in Figure 7B. In air, a land mammal hearing mechanism wasstill present, and sound reached the inner ear throughthe external auditory meatus, the tympanic membrane,
and the ossicular chain. Under water, the modern odontocete sound transmission mechanism was used, with thesound path passing from the lower jaw fat pad to the tympanic plate, and to the middle ear ossicles. The partial
connection of the periotic with the skull did not allow
fully developed directional hearing in water.

Protocetids
Protocetids have a wide mandibular foramen (Fig. 4A),
suggesting the presence of a mandibular fat pad. The lateral wall is thicker than in modern odontocetes, but in accordance with archaeocetes (Fig. 4A). These two features of728

NUMMELA ET AL.

the lower jaw indicate that the lower jaw with its fat pad
was a functional path in sound transmission underwater.
An external auditory meatus is present in protocetids.
The tympanic bone has a thick medial involucrum and athin lateral tympanic plate. The tympanic makes contacts
with the periotic, which is surrounded by air sinuses, but
still has close contact to the skull. This arrangement
allows for directional hearing to some degree in protocetids. The tympanic plate area of Indocetus is larger thanin modern odontocetes, as is typical of archaeocetes (Fig.
5A). The tympanic plate is also slightly thicker than inmodern odontocetes, but similar to that of other archaeocetes (Fig. 5B). Bajpai and Thewissen (1998) noticed thatthe shape of the tympanic bulla of remingtonocetids isclearly different from that of protocetids. The most prominent difference between remingtonocetids and protocetids
is that, in protocetids, the periotic is more detached fromthe skull through the surrounding air sinuses. The tympanic and periotic are still in contact with the skull
through the basioccipital (Luo and Gingerich, 1999).
A tympanic ring was not identified for the tympanic
membrane in the auditory bulla of Indocetus or Gaviacetus. However, the shape of malleus suggests that the
tympanic membrane was an elongated conical ligament,
similar to remingtonocetids (Fig. 2). The Indocetus malleus is of the modern odontocete type in the lack of amanubrium, and in being attached to the tympanic bullaby the processus gracilis. The shape of the malleus head
and the joint facet show that the ossicular chain has reoriented with respect to the position found in remingtonocetids, although it has not yet reached the orientation of
the modern odontocete ossicular chain. No incus is available for this group. The mass of the malleus related to the
tympanic plate area shows that Indocetus and Gaviacetus
are placed among the modern cetaceans (Fig. 6B).
In air, protocetids used the land mammal hearing
mechanism, as suggested by the presence of the external
auditory meatus and the connections of the periotic to theskull. Under water, they could hear through the modern
odontocete hearing mechanism with their modern whaleear. The bony connection between the ear and the skull,
however, indicates that they could not echolocate. Figure
7B describes with a diagram the hearing mechanism of
remingtonocetids and protocetids.

Basilosaurids and Dorudontids
The mandibular foramen height in the dorudontid
Zygorhiza is only slightly larger that the foramen heightin modern odontocetes (Fig. 4A). The lateral mandibularwall of Zygorhiza is thicker than in modern odontocetes,
but is closer to the regression of odontocetes than to thatof other archaeocetes (Fig. 4B).
The external auditory meatus is still present in theskull, as in all other Eocene archaeocetes, but its orientation differs from remingtonocetids and protocetids. In
basilosaurids and dorudontids, the external auditory meatus is oriented posterolaterally (see also Luo and Gingerich, 1999), whereas in remingtonocetids and protocetids it
is oriented laterally. The contact of the tympanoperiotic
complex is more derived than in earlier archaeocetes. The
tympanic plate area is clearly larger in basilosaurids anddorudontids than in modern odontocetes, following thepattern in other Eocene archaeocetes (Fig. 5A). The
tympanic plate thickness in basilosaurids and dorudon-tids (Fig. 5B) is also similar to that of other Eocene
archaeocetes.
The specimens studied did not display a tympanic ringfor the possible tympanic membrane inside the auditory
bulla, but this finding may be due to the quality of thematerial. The malleus and incus, especially of Zygorhiza,
resemble those of modern delphinids and are clearly different from those of remingtonocetids and protocetids(Fig. 2). This finding suggests that the ossicular chain
was similar to its position in modern odontocetes, that is,
it rotated medioanteriorly, and the tympanic membrane
apparently was an elongated conical ligament. Still, thejoint facets are relatively larger in basilosaurids anddorudontids than in modern odontocetes, occupying
approximately half of the malleolar head length (see also
Lancaster, 1990). The incus is relatively larger than inmodern odontocetes. However, when plotting the ossicular mass against the sound input area, both Zygorhiza
and Basilosaurus are placed among all other cetaceans,
both extinct and modern (Fig. 6).
The footplate area for the stapes of Basilosaurus is 9.47mm2 and is an estimate for oval window area (A2, seeabove). With this one example, it seems that the area ratio, the tympanic plate area divided by the oval window
area, in Basilosaurus is similar to that reported for modern cetaceans by Nummela et al. (1999b).
Basilosaurids and dorudontids hardly used their hearing in air. The strongly reduced contact of the tympanoperiotic complex from the skull suggests that underwater
hearing had become the main function of the middle ear.
It is unclear what the highest frequencies were that theseanimals were able to hear; the thickness values of the lateral mandibular wall and of the tympanic plate area do
not indicate a very sensitive mechanism.

DISCUSSION
During the Eocene, radical changes took place in theear anatomy and function of archaeocetes as they
adapted to life in water. The modern odontocete ear capable of hearing underwater evolved in less than 10 million
years. Our results show that the aquatic ear evolved
while hearing on land was still needed, with the origin of
remingtonocetids.
The cladogram in Figure 8 shows the characters thatare critical for the evolution of an aquatic ear in cetaceans, and the time of appearance of these characters
during the Eocene. All the listed characters are necessary
for the proper function of the modern odontocete ear.
Even so, some of these characters reached their modern
state without known intermediates, whereas others
underwent gradual changes.
In a modern odontocete ear, relative vibrations between
different parts in the tympanoperiotic complex are of crucial importance for the function of this aquatic ear. The
degree of the contacts between the tympanic and periotic
dictates how these two bones can vibrate in relation toeach other. The contacts between the tympanic and periotic bones are reduced already in pakicetids, although toa modest degree. These contacts are further reduced during the Eocene in remingtonocetids and protocetids, inwhich the first aquatic ear can be found, and in basilosaurids and dorudontids, in which the contacts are still
reduced, and close to the odontocete ear.

ANATOMICAL ADAPTATIONS FOR UNDERWATER HEARING

In water, sound penetrates the body tissues easily due
to the small impedance difference. This means that soundcan reach the two cochleae almost simultaneously, thus
precluding sophisticated directional hearing. In pakicetids, the tympanoperiotic complex is in close contact tothe skull. This finding does not affect hearing in air andis a great advantage for hearing through bone conduction
in water. However, bone conduction precludes directional
sensitivity, as the ears have to be isolated from each otherto accomplish this.
One character of the modern aquatic ear already present since the earliest fossil cetaceans is the typicallycetacean anatomy of the tympanic bulla, with a thickmedial part, the involucrum, and a thin lateral wall.
The tympanic bone, with a thick medial involucrum anda thin lateral tympanic plate, is of functional importancefor the vibration modes of the tympanic. However, it isplausible that the thick involucrum present in pakicetids
and ambulocetids had an important functional role inenhancing the stimulus while hearing through bone conduction under water. The thin lateral wall of the tympanic bone is a plesiomorphic character among mammals in general, but the involucrum is an apomorphy. It
is the combination of these that led to the modern cetacean hearing mechanism, although its functional significance in aquatic hearing is evident first in remingtonocetids.
The contacts between the tympanic and periotic, andthe acoustic isolation of the whole tympanoperiotic complex from the skull become further reduced in remingtonocetids and protocetids, compared with pakicetids andambulocetids. This enables the tympanic plate to vibrate
more freely, consistent with its active role as a soundreceiving area between the lower jaw and the ossicular
chain, and improves the directional hearing of cetaceans.
However, both these characters evolve further in basilosaurids and dorudontids, where the contacts between the
tympanic and periotic become thinner, and the sinuses
around the ear complex increase in size. This change
underwent gradual evolution, where full isolation, as
seen in modern odontocetes, was not yet reached during
the Eocene.
The thin lateral wall of the tympanic, together with the
thick medial part, becomes functional in an aquatic ear inremingtonocetids. This takes place simultaneously withthe changes in the middle ear structures, the tympanic
membrane, and the middle ear ossicles. The tympanic
membrane elongates into a conical structure, which thenoften is called the tympanic ligament. The middle ear
ossicles, while still forming the ossicular chain, change intheir anatomy so that the ossicular chain becomesslightly rotated, the malleus head enlarges, and its manubrium shrinks to a tiny process to which the tip of the
tympanic ligament attaches. The malleus develops a bony
contact to the tympanic plate through its anterior process, the processus gracilis, and vibrations from the tympanic plate can now be transferred to the ossicular chain
as in an odontocete ear. Additionally, the mandibularforamen in remingtonocetids is large enough to house amandibular fat pad, a structure that, in an aquatic ear, isa functional analogue to the outer ear of land mammals;
the sound vibrations received by the lower jaw can be
guided to the tympanic plate of the tympanic bulla. Thisis even more prominent in Carolinacetus, the basalmost
cetacean of North America; it has an extremely deep729

mandibular fossa, apparently housing a large mandibular
fat pad (Geisler et al., 2005).
Evolution of the lower jaw and the fat pad as a soundpath to the ear was fast and proceeded to its full capacity
as soon as this evolutionary invention was available (seereview in Uhen, 2007, this issue). However, in some otherrespects, plesiomorphic characters were retained throughthe Eocene. For example, all Eocene archaeocetes were
diphyodont and heterodont (Uhen, 1998).
The evolution of the tympanic plate of the aquatic ear
is more gradual. The plate area is still relatively large
and thick compared with the modern odontocetes. A large
area collects more energy, but a thinner tympanic plate
can vibrate at higher sound frequencies. Also, Ketten(1992) found the Zygorhiza to have a mixed high- andlow-frequency ancestral type of basilar membrane.
Apparently, high-frequency hearing improved during
the Eocene, and this finding can be tied to the evolutionof echolocation; decrease of mass enables the system totransmit higher frequencies, which are useful in echolocation. However, based on cranial and cochlear anatomy
of archaeocetes as well as fossil odontocetes and mysticetes, Fleischer (1976) suggested that echolocation firstevolved among fossil odontocetes, and that no archaeocetes had the ability to echolocate. This is inconsistent
with the findings of Uhen (1998) that basilosauroids did
not yet show any telescoping of the skull. Directional
hearing improved with better isolation of the ears, which
is of great importance in developing echolocation ability.
In general, the tympanic plate area and thickness
increased in the archaeocetes throughout the Eocene, butthen decreased between archaeocetes and the modern
odontocetes. While a larger tympanic plate area improves
the signal-to-noise ratio, hence improving the hearing
sensitivity, a thinner and a smaller tympanic plate has asmaller mass, enabling transmission of higher frequencies. This is relevant for the evolution of echolocation inwhales. Characteristic of the anatomical adaptations forunderwater hearing is that during their evolutionary history, cetaceans kept the inner ear relatively unchanged(Ketten, 1992, 2000), while they totally reorganized thesound transmission through the outer and middle ear.

ACKNOWLEDGMENTS
We thank the guest editor, Joy Reidenberg, and associate editor, Jeffrey Laitman, for inviting us to contributeto this special issue of The Anatomical Record. We also
thank Jun Ebersole (McWane Center, Birmingham, AL),James Mead, Charles Potter, and David Bohaska(National Museum of Natural History, Smithsonian Institution), Roger Birkhead and Jennifer Styrsky (Auburn
University Museum of Paleontology), Judie Schiebout(Louisiana State University Museum of Geology), andHans J. Baagøe and Mogens Andersen (ZoologicalMuseum University of Copenhagen) for access to theircollections and loan of material under their care. Brooke
Garner, Amy Maas, and Lauren Stevens are thanked fortheir technical assistance with the fossils, and Mary Elizabeth Filon for her artwork. We thank Tom Reuter andSimo Hemilä for designing the hardware models for different mammalian ears, and Rey Notareschi for his
expertise in video film techniques. We are indebted toAnnalisa Berta, Jason Kosove, Terry Lancaster, Winston
Lancaster, and Mark Uhen for helping us collect more

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NUMMELA ET AL.

data, and to Simo Hemilä for many critical comments for
improving this manuscript. S.N. was funded by the Ellaand Georg Ehrnrooth Foundation, J.G.M.T. by the
National Science Foundation, and S.B. by the Department of Science and Technology of India.

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APPENDIX 1Specimens studied for this research are catalogued in
the collections of the following institutions:
AUMP — Auburn University, Museum of Paleontology,
Auburn, Alabama (see RMM)
H-GSP — Howard University, Geological Survey ofPakistan.
IITR-SB (previously RUSB) — Indian Institute of Technology, Roorkee, India.
LSUMG — Louisiana State University, Museum of
Geoscience, Baton Rouge, Louisiana
LUVP — Lucknow University, Vertebrate Palaeontology Laboratory, India.
NMNH (USNM) – National Museum of Natural History, Smithsonian Institution, Washington, DC.

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RMM — McWane Center, Birmingham, Alabama
VPL — Vertebrate Palaeontology Laboratory, Panjab
University, Chandigarh, India.
ZMUC — Zoological Museum University of Copenhagen, Denmark. The research presented here was basedon study of six families of fossil cetaceans, pakicetids,
ambulocetids, remingtonocetids, protocetids, dorudontids, and basilosaurids. We here present a list of fossil
cetacean specimens studied.
CETACEA
Pakicetidae
Ichthyolestes pinfoldi
H-GSP 18391 (field number 92003), left tympanic withinvolucrum, lateral plate, sigmoid process, anterior
process, and tympanic ring (described by Thewissen
and Hussain, 1998; Luo, 1998; Luo and Gingerich,1999).
H-GSP 30181, right tympanic bulla, rostrolateral parts
missing.
H-GSP 30223, left tympanic bulla.
H-GSP 30459, right tympanic bulla, dorsolateral parts
missing.
H-GSP 91047, right mandible fragment with mandibular foramen (described by Thewissen and Hussain,1998).
H-GSP 96254, cf. Ichthyolestes, juvenile. Braincase andorbital regions with sagittal and nuchal crests, butlacking basicranium and squamosal.
H-GSP 96283, left tympanic with involucrum and fragment of tympanic plate.
H-GSP 96407, left temporal region with periotic andcochlea preserved in part as endocast, external auditory meatus and epitympanic recess.
H-GSP 96431, fragment of left basicranium, which
includes periotic with promontorium and oval andround windows, and tympanic with involucrum and lateral plate.
H-GSP 96623, partial skull with right ear region. Periotic with promontorium and epitympanic recess. Squamosal with external auditory meatus, anterior facet,and mastoid process (briefly described by Nummela
et al., 2006).
H-GSP 98134, skull including braincase and both ear
regions with promontorium, oval and round windows,
external auditory meatus (briefly described by Thewissen et al., 2001).
Nalacetus ratimitus
H-GSP 30325, right tympanic bulla, medial part (involucrum).
H-GSP 96384, left tympanic, part of lateral wall missing.
H-GSP 96385, left tympanic, part of ventrolateral wall
missing, but with internal cast.
H-GSP 96386, braincase with left squamosal and ear
region, promontorium, epitympanic recess, and external auditory meatus.
H-GSP 98140, internal cast of tympanic bulla.
Pakicetus attocki
H-GSP 1649, mandible (holotype, see West, 1980).
H-GSP 30386, left tympanic with involucrum and lateral plate.
H-GSP 91034, right mandible with mandibular foramen (described by Thewissen and Hussain, 1993,
1998).

H-GSP 91035, left tympanic with involucrum, lateralplate, and tympanic ring; left incus.
H-GSP 92100, left tympanic with involucrum, lateralplate, and anterior process.
H-GSP 96192, left tympanic with involucrum and partsof lateral plate.
H-GSP 96231, skull including braincase and right ear
region with promontorium, oval and round windows,
external auditory meatus (briefly described by Thewissen et al., 2001).
H-GSP 96344, left tympanic with involucrum and lateral plate (published with transposed numbers as HGSP 96334 by Luo, 1998; Luo and Gingerich, 1999).
Pakicetidae indet.
H-GSP 30119, left tympanic with involucrum and lateral plate.
H-GSP 30120, left tympanic with involucrum and partsof the lateral plate.
H-GSP 30142, right tympanic with involucrum and lateral plate.
H-GSP 30150, right tympanic with involucrum andparts of the lateral plate.
H-GSP 30198, pakicetid n. sp. Right tympanic bulla,caudal and caudomedial parts missing.
H-GSP 30379, right tympanic with lateral plate.
H-GSP 30387, right tympanic with involucrum and lateral plate.
H-GSP 30389, left tympanic with involucrum and lateral plate.
H-GSP 30398, unassociated parts of tympanic bulla.
H-GSP 30424, right tympanic with involucrum and lateral plate.
H-GSP 96506, left tympanic with involucrum and lateral plate.
H-GSP 96541, right tympanic with involucrum, lateralplate missing, but with internal cast.
H-GSP 98138, right tympanic with involucrum and lateral plate.
H-GSP 98141, right tympanic with involucrum and lateral plate.
H-GSP 98143, internal cast of left tympanic bulla.
H-GSP 98199, right tympanic with involucrum andparts of the lateral plate.
H-GSP 98220, right tympanic bulla, rostral and dorsal
parts missing.
Ambulocetidae
Ambulocetus natans
H-GSP 18507, skull, partly damaged and mediolaterally compressed, right tympanic with fragments ofdentary and basioccipital, left tympanic with parts ofmandibular condyle, left posterior mandible (thisspecimen described in detail by Thewissen et al.,1996).
Remingtonocetidae
Remingtonocetus sp.
RUSB 2521, left and right mandible with mandibularforamen (dental morphology published by Thewissen
and Bajpai, 2001b).
RUSB 2592, left mandible with mandibular foramen(dental morphology published by Thewissen and Bajpai, 2001b).
RUSB 2781, right ear region with parts of squamosal, periotic, parietal, supra- and exoccipital, including the external

ANATOMICAL ADAPTATIONS FOR UNDERWATER HEARING

auditory meatus. The promontorium with oval and roundwindows, epitympanic recess, and internal auditory.
RUSB 2828, braincase, left tympanic with involucrum,
tympanic plate, and sigmoid process; promontorium;
the ossicles in situ: malleus with gonial process, incus
with short and long processes, and stapes.
RUSB 2914, left tympanic with involucrum, tympanic
plate, sigmoid process, posterior process and tympanic
ring; malleus with gonial process; incus with long andshort processes found in anatomical contact.
Andrewsiphius sp.
RUSB 2786, right ear region with parts of squamosal,
periotic, parietal, supra- and exoccipital; promontorium
with oval and round windows, epitympanic recess, andexternal auditory meatus.
Protocetidae
Indocetus ramani
LUVP 11034, right tympanic with involucrum, lateralplate, and sigmoid process; right periotic withpromontorium, oval and round windows, facial canal,internal auditory meatus; right malleus with joint facet
for the incus, but gonial process missing (described by
Sahni and Mishra, 1975; Kumar and Sahni, 1986; Williams, 1998; Luo, 1998; Luo and Gingerich, 1999; Thewissen and Bajpai, 2001a; Spoor et al., 2002).
Babiacetus
RUSB 2512, right mandible, posterior part with M1-M2,
and mandibular foramen.

733

Gaviacetus
RUSB 2870, left tympanic with involucrum and lateralplate, left malleus with partly broken joint facet for theincus, gonial process missing.
Basilosauroidea
Dorudontidae
Zygorhiza kochii
LSUMG V160A, left tympanic with involucrum andtympanic plate, left incus with short and long processes(described by Lancaster, 1990).
RMM 2739, left tympanic bulla and left malleus(described by Lancaster, 1990 as AUMP 2368).
USNM 4680, right tympanic bulla (described by Kellogg, 1936).
USNM 4748, right tympanic bulla (described by Kellogg, 1936).
USNM 11962, skull (holotype), right and left tympanics, right and left mandibles (described by Kellogg,
1936).
Basilosauridae
Basilosaurus cetoides
LSUMG V1, right malleus with gonial process, rightand left incus with long and short processes, right stapes (described by Lancaster, 1990).
RMM 2740, left tympanic bulla.
USNM 4677, left tympanic bulla, dorsal and lateralparts missing (described by Kellogg, 1936:24).
USNM 6125, left tympanic bulla (described by Kellogg,
1936:24).