3.
14 Underwater Hearing
A N Popper, University of Maryland, College Park, MD, USA
D R Ketten, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
ª 2008 Elsevier Inc. All rights reserved.
3.14.1 The Origins of Vertebrate Underwater Hearing
3.14.2 The Evolution of Vertebrate Hearing in Water
3.14.3 The Inner Ear of Fishes
3.14.4 Hearing Capabilities of Fishes
3.14.5 Marine Mammals
3.14.5.1 Marine Mammal Auditory Systems
3.14.5.2 Marine Mammal Audiometrics
References
Glossary
audiogram A graph of hearing ability conventionally
displayed as frequency in hertz or kilohertz (abscissa)
versus sensitivity expressed as sound pressure level
or intensity measured in decibels (ordinate).
bony fishes All fishes with skeletons made of
bone. This is the largest of all vertebrate groups and
includes most of the species commonly thought of
as fishes such as goldfish, tuna, etc.
cartilaginous fishes Sharks, skates, and rays.
The skeleton in these species is made of very
dense cartilage rather than bone.
Cetacea The name of the taxonomic order
encompassing all whales, dolphins, and porpoises
derived from the Latin word for whale, cetus. There
are two suborders: Mysticeti (baleen whales) and
Odontoceti (toothed whales) (see below).
cochlea The snail-shaped canals and sensory
organs of the inner ear that provide hearing by
transforming sound energy into neural impulses.
decibel (dB) A unit of measurement based upon
the logarithm of the ratio of pressure versus an
arbitrary reference pressure. For sound measure-
ments, the decibel scale usually represents sound
pressure level (SPL), but it may also be used as a
measure of intensity (pressure squared). The refer-
ence pressures used are different for air (20 mPa)
and underwater (1 mPa) sound measurements;
therefore, the decibel level of a sound is properly
stated in the form of n dB re n mPa. Two sounds that
are perceived as equally loud may have different
decibel values based on the reference pressures
used in the measurements. Two sounds with equal
227
227
228
228
230
230
232
235
intensity would have a 100 dB re 20 mPa in air but a
decibel value in water of approximately 160 dB re
1 mPa.
echolocation The ability to image features of the
environment including size, shape, and location of
an object by analyzing echoes from a self-
generated sound. Bats and toothed whales have
the best known animal echolocation or biosonar.
end organ The sensory regions of the inner ear,
particularly the otolithic receptors and the recep-
tors of the semicircular canals.
hertz A unit of sound frequency equal to 1 cycle
s 1 (see also kHz).
impedance A complex ratio of power versus flow
properties, describing effectively the resistance or
efficiency of transfer. Acoustic impedance can be
thought of as the impact of the medium on sound
transmission.
inner ear The combined organs of hearing and
balance, the cochlea and vestibular system.
infrasonic Frequencies below 20 Hz, the lower
extreme of human hearing.
kilohertz (kHz) Equals 1000 Hz (or 1000 cycles s 1).
lagena One of the end organs of the ear in fishes. It
is also present in all nonmammalian terrestrial
vertebrates.
lamprey A group of primitive vertebrates that do
not have a lower jaw. Lampreys represent the most
primitive group of vertebrates.
mandible Lower jaw bone.
masking The impact of one sound on the ability to
detect another sound.
225
226 Underwater Hearing
middle ear The chamber and structures that
amplify sound and connect the outer ear and inner
ear. A form of middle ear is found in all terrestrial
vertebrates.
Mysticetis The suborder of baleen-bearing or
moustached whales comprising all great whales
such as blue, finback, right, and humpback whales.
Baleen is a series of horny overlapping plates with
feathered edges that mysticetes use in lieu of teeth
for straining food. Mysticetes have not been shown
to echolocate.
octave An octave is broadly defined as a doubling
of frequency. Thus, a one octave shift from 500 Hz
is 1000 Hz; from 3000 Hz it is 6000 Hz. Adult
humans have on typically an eight-octave func-
tional hearing range of 32 Hz to 16 kHz.
octavolateralis system The term that refers to the
combined ear and lateral line system of fishes.
Odontoceti The suborder of cetaceans compris-
ing the toothed whales, such as sperm whales,
dolphins, and porpoises. All odontocetes are
believed to echolocate (to use sound for imaging
the environment).
ossicles The bones that act as levers in the middle
ear to amplify and transduce sound energy
impinging on the tympanum or eardrum into
mechanical forces driving the inner ear responses.
otoconia Calcium carbonate crystals found in the
otolithic organs of terrestrial vertebrates, cartilagi-
nous fishes, and primitive bony fishes. The crystals
are embedded in a gelatinous matrix.
otolith Calcium carbonate structures found in the
saccule, lagena, and utricle of most bony fishes.
The otolith is several times denser than the rest of
the fish body. Relative motion between the otolith
and the sensory epithelium results in stimulation of
the sensory hair cells. The saccular otolith has
growth rings that can be visualized to determine
fish age.
otolithic organs A general term for the saccule,
lagena, and utricle of the inner ear. Each has a
sensory epithelium and an overlying calcium car-
bonate mass (otoconia or otolith, depending on the
species). Relative motion between the mass and
the sensory epithelium causes excitation of the
sensory hair cells.
Otophysi A group of fishes that includes goldfish,
catfish, and carp. All members of this mostly
freshwater group of fishes have a series of bones,
the Weberian ossicles, which connect the swim
bladder to the inner ear.
pinna The outer ear flap in most mammals,
including humans. The pinnae assist with focusing
sound and localization, the ability to detect the
direction of a sound.
Pinnipedia The marine mammal order comprised
of seals, sea lions, and walruses.
rorquals A type of baleen whale that feeds on
small fish and zooplankton by lunge-feeding.
saccule One of the regions of the ear. In fishes the
saccule is generally considered to be the major
auditory end organ but it may also be used to
determine head position relative to gravity. In ter-
restrial vertebrates and all mammals, the saccule,
along with the utricle, provides information about
head position relative to gravity and helps the ani-
mal maintain eye position as head position
changes.
semicircular canals Fluid filled canals of the res-
tibular system of the inner ear. Motion of these
fluids excite cells that detect angular acceleration
of the head. Feedback from the canals affects eye
movements.
sensory hair cells The fundamental cell of the
inner ear and lateral line of vertebrates. These cells
detect mechanical motion and convert that motion
to a signal that can stimulate the nerves that carry
information to the brain.
sound localization Determination of the position
of a sound source compared to the position of an
animal based on differences in its intensity and
arrival times between ears or receptors.
swim bladder An air chamber in the abdominal
cavity of most bony fishes that is used to adjust
buoyancy so that the animal can maintain its posi-
tion in the water column without expenditure of
energy. The swim bladder in some fishes is used in
sound production and in sound detection.
ultrasonic Sounds above 20 kHz, which is the
upper extreme of human hearing.
utricle One of the regions of the inner ear. In fishes
the utricle is involved in both hearing and determi-
nation of head position relative to gravity. In
terrestrial vertebrates and all mammals, the utricle
is primarily a receptor for determination of head
position relative to gravity and helps the animal
maintain eye position as the head changes
position.
vestibular system The part of the inner ear, that
determines the position and acceleration of the
head relative to gravity, commonly thought of as the
balance system. The vestibular system includes the

sensory organs of the saccule and utricule plus the
semicircular canals.
Weberian ossicles A series of bones between
the swim bladder and inner ear of Otophysan
fishes that appears to enhance hearing by serving
3.14.1 The Origins of Vertebrate
Underwater Hearing
The vertebrate ear and hearing evolved in aquatic
animals. Although there is no evidence as to when the
first vertebrates were able to hear, it is likely this
occurred several hundred million years ago.
Once vertebrates came onto land, they had to
develop an array of new mechanisms to enable use of
their fluid-filled and water-adapted inner ears for
detection of airborne sounds. The problem that ter-
restrial vertebrates had to overcome was the difference
in impedance between the fluids of the inner ear that
had evolved to detect sound in water and the impe-
dance of sound in air. Without special structures for
capture, transduction, and amplification, the sound
energy in air would not be efficiently transferred to
the fluids of the inner ear. As a consequence, airborne
sound would be largely undetectable. This need to
accommodate the impedance mismatch of air and
water led to the evolution of the middle ear present
in virtually all terrestrial vertebrates.
Conversely, there was also a readaptation when air-
adapted vertebrates once again entered the water. Air-
adapted ears of land animals (including human divers)
function poorly in water because they are not adapted
to the higher pressures and faster sound speeds in water
(approximately 1550 m s 1 in water versus 330 m s 1 in
air) that are critical elements for discriminating
between sounds and determining the position of a
sound source in the space. Consequently, aquatic ver-
tebrates have two levels of adaptation: the original
water-derived ear of fishes and a range of partial to
full remodifications of an air-to-water ear in animals
that have returned to the marine environment.
3.14.2 The Evolution of Vertebrate
Hearing in Water
The earliest vertebrates were jawless species resem-
bling the modern-day lamprey. Lampreys, like their
vertebrate ancestors, have a very recognizable ear with
Underwater Hearing 227
as an acoustic coupling device between the
pressure-receiving swim bladder and the saccule
of the inner ear in a way that is functionally ana-
logous to the middle ear of terrestrial
vertebrates.
sensory cells and other structures similar to those of
modern vertebrates. However, because the ear com-
prises both the vestibular and auditory senses, it is not
clear whether the earliest ears were primarily for hear-
ing or for detecting acceleration and head position.
Even if ears did not originally arise for hearing,
they likely subsumed this role very early in the evolu-
tion of vertebrates because there were considerable
selective pressures favoring sound detection (van
Bergeijk, W. A., 1967; Wever, E. G., 1974; Fay, R. R.
and Popper, A. N., 2000). In effect, hearing is likely to
have arisen because other senses available to the ear-
liest vertebrates, including vision, touch, and olfaction,
function effectively only over short ranges. For exam-
ple, vision can only function when there is sufficient
light to excite photoreceptors in the eye (Fay, R. R.
and Popper, A. N., 2000) and light does not penetrate
very far into the ocean. In contrast to light, sound
travels well in water, and the ocean is filled with
sounds (Wenz, G. M., 1964) that can provide animals,
through hearing, with a broader range of information
about the environment at greater distances from the
receiver than virtually any other sense.
Animals just detect presence of sound to use it
effectively. Particularly for survival, the animal needs
to be able to determine the direction and, ideally, the
relative distance of sounds and to determine which are
biologically relevant (e.g., predator, prey, mate, or
competitor) in the presence of other sounds. Thus, it
is possible to hypothesize that very early in the evolu-
tion of hearing, vertebrates developed mechanisms
that would enabled them to localize sound sources,
discriminate among signals, and detect signals in the
presence of masking noise. This implies that in addi-
tion to evolving an ear, they also had to evolve the
mechanisms for analyzing multiple features of sounds
(e.g., Fay, R. R. and Popper, A. N., 2000).
It is likely also that use of sound for communica-
tion among animals of the same species, such as for
mating, evolved later than hearing per se. Although
data are limited, it is known that sharks and rays use
sound to detect possible prey, but there is no evi-
dence that any member of this very successful
228 Underwater Hearing

vertebrate group uses sound for communication
(Myrberg, A. A., 2001). Similarly, although goldfish
have excellent hearing (Fay, R. R., 1988), no one has
yet detected that goldfish producing sounds. Marine
mammals by contrast employ complex signals not
only for communication but, in some cases, for
sophisticated acoustic imaging called echolocation
or biosonar as discussed below.
3.14.3 The Inner Ear of Fishes
The ears of cartilaginous fishes (sharks and rays) and of
bony fishes resemble those of terrestrial vertebrates
(Figure 1). All vertebrate ears (other than jawless fishes)
have three semicircular canals that are used for deter-
mination of angular acceleration. They also have
(a)
m
o roles vary among the more then 25 000 extant species
l
o in goldfish and related species (e.g., most catfish),
s
(b) o whereas in a few species the utricle has a major role
several otolithic end organs, two of which, the saccule
and utricle, are found in all vertebrates. The third end
organ, the lagena, is found in all vertebrates except
mammals but may have given rise to the cochlea
(Wever, E. G., 1974). The function of the otolithic
end organs in terrestrial animals is to determine head
motion relative to gravity. For fishes, however, these
organs provide vestibular functions as well as hearing
(Platt, C., 1983; Popper, A. N. et al., 2003).
Fish hearing involves the use of sensory hair cells
that are virtually the same as those found in terrestrial
vertebrates (Coffin, A. et al., 2004). In cartilaginous
fishes (sharks and rays), terrestrial vertebrates, and
more primitive bony fishes (e.g., sturgeon and lung-
fish), the sensory epithelium containing the sensory
cells is overlain by a mass of calcium carbonate crystals
(otoconia) embedded in a gelatinous matrix. In the
majority of bony fishes, however, the calcium carbo-
nate fuses into a single dense structure, the otolith.
Hearing by fishes results when a sound field impinges
on the body and moves tissues more readily than the
denser otoliths. Because the ciliary bundles on the hair
cells are mechanically coupled to the otoliths, the
relative motion between the fish’s body and the otolith
results in bending of the ciliary bundles and stimula-
tion of the hair cells, leading to detection of sound (or
body motion in water).
The precise role of each of the end organs in fish
hearing is not known, and it is likely that the specific
of fish (Popper, A. N. et al., 2003). For example, the
saccule is thought to be the major auditory end organ
in hearing, as discussed below.

3.14.4 Hearing Capabilities of Fishes

Hearing has been measured in cartilaginous and bony

fishes. These measures include both the range of
l
frequencies detectable and the lowest sound levels
m that are detected at each frequency. While limited,
o these data show that cartilaginous fishes are able to
o
s detect sounds up to about 1000 Hz (Figure 2).
o s
si Although there are hearing data on fewer than 100
o
of the 25 000 species of bony fish, it is clear that there
Figure 1 Illustrations of the right inner ears from the perch is greater variation in the abilities of bony fish to
Stizostedion lucioperca (formerly Lucioperca sandra) (a) and
detect in sound (Figure 2). Some fishes detect sounds
goldfish Carassius auratus (b). Both from Retzius G. (1881).
l, lagena; m, utricular macula; o, otolith; s, saccule; si, sinus only up to 500–1000 Hz, whereas others can detect
impar (to connect left and right ears in goldfish). Anterior is sounds with better sensitivity and at frequencies up
to the left and dorsal to the top. to 3000 or 4000 Hz. A few species are able to detect

180
160
Threshold (dB re 1uPa)
140
120
100
80
60
40
100 1000 10000
Frequency (Hz)
Figure 2 Auditory thresholds for a variety of different fish
and shark species. Note that the audiograms were all
determined using different methods. Moreover, while
thresholds are most likely correctly represented using
pressure values for hearing specialists such as goldfish and
silver perch, it is not clear whether pressure or particle
motion (not shown here) would be more suitable for the
nonspecialists. All data from Fay, R. R. (1988) other than
silver perch (Ramcharitar, J. U. et al., 2004) and Atlantic
croaker (Ramcharitar, J. U. and Popper, A. N., 2004).
sounds well into the infrasonic and ultrasonic ranges
(reviewed in Popper, A. N. et al., 2003; Ladich, F. and
Popper, A. N., 2004).
Fishes that detect sounds above about 1500 Hz are
often referred to as hearing specialists, whereas those
that do not possess such capabilities are called non-
specialists (or generalists). It has been suggested that in
the hearing specialists, one or more of the otolith
organs may respond to sound pressure as well as to
acoustic particle motion (e.g., Popper, A. N. et al., 2003).
The response to sound pressure is thought to be
mediated by mechanical coupling between the swim
bladder (a gas-filled chamber in the abdominal cavity
that enables a fish to maintain neutral buoyancy) or
other gas bubbles and the inner ear. With this coupling,
the expansion and contraction of the gas-filled struc-
ture in a pressure field is translated to the ear. In
nonspecialists, however, the lack of a swim bladder
or its lack of coupling to the ear probably results in
any signal from the swim bladder attenuating before it
gets to the ear. As a consequence, these fishes detect
little or no pressure component of the sound (Popper,
A. N. et al., 2003). Hearing generalists are most sensi-
tive to sounds produced by relatively near sources.
While some hearing specialists, such as catfish, use
sound for communication (as do some hearing gen-
eralists), others do not. Then here has been some
question about why fishes that do not use sound for
Underwater Hearing 229
communication evolved the ability to detect higher
frequencies. The most likely reason, at least for fresh-
water species, is that the fish evolved in shallow water
where there is substantial and rapid attenuation of
low frequencies (Rogers, P. H. and Cox, M., 1988). In
Goldfish
order for these species to glean any information
Atlantic salmon about their environment using sound, they would
Tuna
Atlantic cod
Plaice
need adaptations to detect the higher frequencies
Bull shark that propagate over longer distances in such waters.
American shad
Silver perch Specializations for enhancement of hearing gen-
Atlantic croaker
erally involve mechanisms that acoustically couple
100000 an air bubble, such as the swim bladder, with the ear.
It is likely that the swim bladder evolved to enable
fishes to maintain neutral buoyancy, thus cutting
down on energy used to maintain a particular depth
in the water column. However, mechanisms have
evolved that enable many fish species to use this
organ for both sound production (Zelick, R. et al.,
1999) and hearing (Ladich, F. and Popper, A. N.,
2004).
The nature of the coupling between the swim
bladder and inner ear varies among hearing specia-
lists. The best-known coupling is found in the fishes
of the superorder Otophysi, a group of primarily
freshwater fishes that includes goldfish and catfish.
These species have a series of bones, the Weberian
ossicles, connecting the swim bladder directly to the
inner ear. It has been hypothesized that motion of the
walls of the swim bladder during sound stimulation
results in motion of the Weberian ossicles that, in
turn, moves the fluids of the inner ear (Alexander, R.
McN., 1962) in a manner analogous to the function of
the mammalian middle ear bones.
Beyond the Otophysi, there are diverse connec-
tions between the swim bladder or other air bubbles
and the inner ear among taxonomically distinct spe-
cies. These may include anterior projections of the
swim bladder that terminate in contact with the
ear and/or newly evolved air bubbles located near
the ear.
One significant point about all of these structures is
that multiple mechanisms evolved to enhance hearing
that are spread throughout the fish taxa. Indeed, there
are instances of closely related species with very dif-
ferent hearing capabilities and air bubble connections
to the ear. For example, one species of the squirrel fish
family (Holocentridae) only detects sounds to about
1000 Hz, whereas another species that lives in the
same caves detects sounds to over 3000 Hz (Coombs,
S. and Popper, A. N., 1979). The two species have
substantial differences in ear structure and in the
relationship between the swim bladder and ear.
230 Underwater Hearing
Fishes of the commercially important family
Sciaenidae (croakers and drums) also have great
diversity in ear structure, in the relationship between
the ear and swim bladder, and in hearing capabilities
(Ramcharitar, J. U. et al., 2001).
Although the saccule and lagena are most often
implicated in fish hearing, there are a number of
cases in which the utricle appears to have taken on a
special role to enhance detection of low- or high-
frequency sounds. There is evidence that some marine
catfish use low-frequency echolocation to glean infor-
mation about their environment (Tavolga, W. N.,
1976), much as dolphins use high-frequency sounds
for biosonar. Echolocating catfish have hypertrophied
utricles that are hypothesized to function like a low-
frequency accelerometer to detect echoes of their own
sounds in order to navigate through the environment
(Popper, A. N. and Tavolga, W. N., 1981).
At the other end of the frequency range, the
clupeiform fishes (e.g., herring, anchovies, and sar-
dines) have utricles unlike those found in any other
vertebrate. Recent evidence has implicated this spe-
cialization for the detection of sounds up to 180 kHz
in a number of clupeids including the American shad
(Mann, D. A. et al., 2001). The adaptive significance of
this capability appears to be for the detection of
sounds produced by the echolocating dolphins
(Plachta, D. T. T. and Popper, A. N., 2003) that
often prey upon schools of clupeids.
The bottom line is perhaps the exceptional diver-
sity of structures that fishes have evolved that enable
them to use sound to obtain environmental informa-
tion. Although we are at the earliest stages of
understanding this diversity, an example of the critical
use of sound includes evidence that deep-sea fishes
evolved specializations to enhance hearing at depths
where there is little or no light (e.g., Buran, B. N. et al.,
2005). More recently, it has become apparent that some
larval fishes use sounds produced by reefs to find places
to settle (Simpson, S. D. et al., 2005). Data is currently
available on only a few extant species. It is likely that
further study will continue to demonstrate that hearing
not only evolved underwater but also that the broadest
adaptations are in this environment as well.
3.14.5 Marine Mammals
Marine mammals, like fishes, encompass diverse
groups of species, although it is arguable that they
are less diverse than fishes. Marine mammals comprise
five vertebrate groups. The two best known are the
cetaceans (dolphins and whales) and the pinnipeds
(seals, sea lions, and walruses). These will form the
focus of this discussion because there are sufficient
data on hearing in some of their component species
to provide insights into how aquatic ears re-evolved
from air-adapted ancestors. They also include species
that range from totally aquatic to amphibious to pri-
marily land (or ice), air-adapted ears.
Cetaceans are divided into two distinct groups. The
Odontoceti (or toothed whales) are predatory high-
frequency echolocators typified by the well-studied
bottlenose dolphins. The Mysticeti (or baleen whales)
include the largest species ever recorded, the blue
whale, as well as some smaller rorqual whale species.
All cetaceans live entirely in water and may spend as
much as 80% of their time submerged. Pinnipeds, by
contrast, are truly amphibious and all species spend
some portion of their time and do key activities (e.g.,
breeding and rearing young) on land. The sirenians
(manatees and dugongs) are, like cetaceans, obligate
aquatics, but to date few manatees have been studied
and there are no hearing data on dugongs. There are no
hearing or ear data on any member of the two remain-
ing and most recently evolved marine mammal groups,
the sea otters and polar bears.
3.14.5.1 Marine Mammal Auditory Systems
Significant structural differences between marine and
land mammal ears are primarily found in the outer
and inner ears. All marine mammals have special
adaptations of the external ear (valvular canal closure
mechanisms, semioccluded canals, and wax plugs)
and middle ear (heavily vascularized and innervated
middle ear mucosa, diminished or absent mastoids,
and broad-bore Eustachian tubes) consistent with
deep, rapid diving and long-term submersion.
However, recent data suggest that marine mammals
retain air-filled middle ears and the same fundamen-
tal inner ear components and hearing mechanisms as
terrestrial species.
Cetaceans have the most derived ear of any mam-
mal, marine or otherwise. As cetaceans evolved into
obligate aquatic mammals, their head tissues were
pushed, inflated, and telescoped (Barnes, L. G. et al.,
1985) to form a novel cranium with elongated jaws
(rostrum), scooped frontal bones, and nares trans-
posed upward and rearward, dorsal to the eyes.
Telescoping may have been driven head reshaping
primarily to allow minimal head exposure at the
surface, but the ear was effectively dragged along
with other skull elements to new positions in the
 Underwater Hearing 231

head, and profound structural changes for sound
transduction took place in virtually all parts of the
peripheral auditory system.
In cetaceans, sound most likely arrives at the ear
via specialized fatty tissues that are coupled to the
middle ear and that act as both pinnae and external
canals (Figure 3). Norris K. S. (1969) speculated that
a fatty core in the posterior third of the mandible acts
as a preferential path for underwater sound. Recent
studies have determined that these perimandibular
fats have complex shapes that effectively form inter-
nal pinnae (Ketten, D. R. et al., 2004). They also are
composed of very unusual lipids that have physical
properties consistent with acting as a specialized
channel matched to the acoustic impedance of under-
water sound (Koopman, H. N. et al., 2006).
Cetacean middle and inner ears in general were
reshaped also to meet the demands of underwater
physics of sound. They became encased in distinc-
tive, shell-shaped bony capsules (tympanic and
periotic bullae) that moved outside the brain case
and, at least in most modern odontocetes, lost all
firm bony connections to the skull. Instead, the tym-
panoperiotic bullae, and thus the middle and inner
ears of dolphins, are suspended by ligaments or struts
in a spacious, soft tissue-filled extracranial sinus. This
accomplishes two critical things for underwater
hearing. First, the ears have a three- to fivefold
greater separation than if they retained the intracra-
nial position common in land mammals, which means
they are separated to match the increased speed of
sound in water. Second, both the middle and inner
ears are acoustically isolated from most head tissues
that could conduct sound to the ear which improves
sound localization which is critical for echolocation.
Odontocetes and mysticetes have middle ears
adapted for radically different frequencies. Odonto-
cetes follow the ultrasonic land mammal pattern but
carry it to extremes with multiple stiffening agents for
the middle ear ossicles that include both well-devel-
oped stapedial ligaments and incudal struts (Ketten,
D. R., 2000). Further, the tympanic membrane is sub-
stantially reduced and relatively rigid in all
odontocetes. Bottlenose dolphins (Tursiops truncatus)
have recently been shown to have middle ear stiff-
nesses that are sixfold greater than those of land
mammals (Miller, B. S. et al., 2006). All of this is
consistent with audiometric data for odontocetes (dis-
cussed below) that shows broad hearing ranges from
about 150 Hz to well over 100 kHz, with peak hearing
over 40 kHz for most dolphins species.
Mysticetes, by contrast, have low-frequency,
mass-dominated middle ears. Unlike the small, stiff
middle ear and eardrum of dolphins, the mysticetes

Inner ear

Inner mandibular fats

Posterior
fats

Outer mandibular
fats

Figure 3 A three-dimensional reconstruction based on computerized tomography data of a bottlenose dolphin. The skull,
including the upper and lower jaws or rostrum, are transparent to show the brain (pink) inside the skull and the ear bones (red).
The ear bones, housing middle and inner ear structures, are outside the skull but inside the lower jaw (mandible) and are
connected to the three fat bodies (orange) (Ketten, D. R. et al., 2004, reprinted with permission, ª Ketten, D. R., 2003). These
fats form rabbit ears that are oriented anteriorly and slightly ventral and provide a low-impedance path to the middle ear
compared to other head tissues. Reprinted by permission of Ketten, D. R.
232 Underwater Hearing
have a thick, multilayered eardrum that is a unique
elongated pouch called the glove finger (Reysenbach
de Haan, F. W., 1956). This unusual structure not
only reduces the probability of tympanic membrane
perforation in diving but also increases middle
ear volume and is coupled to a disproportionately
large middle ear cavity, all of which are consistent
with the expectation of good infrasonic to low-fre-
quency hearing in most mysticetes (see Watkins, W.
A. and Wartzok, D., 1985 for vocalizations and
Ketten, D. R., 2000 for anatomical correlates).
There is no evidence to date of echolocation by
mysticetes, and whether they preceded, succeeded,
or coevolved with odontocetes is not yet clear
(Thewissen, J. G. M., 1998).
Thus, as a group, mysticete and odontocete mid-
dle ears span infra- to ultrasonic hearing with
adaptations that clearly couple these ears so effec-
tively to underwater sound that they may no longer
be able to sense airborne sound at anything except
very high levels.
There is no clear consensus on how whale and
dolphin middle ears function underwater. Both con-
ventional ossicular motion and translational bone
conduction have been proposed for dolphins (see
review in Ketten, D. R., 2000), and the role of the
middle ear in cetaceans therefore remains an open
question.
Cetacean inner ears have a well-developed spiral
cochlea but substantially reduced vestibular systems.
In some ways the cetacean cochlea is in fact hyper-
trophied in having more cells and more complex
membrane structures than most land mammals. All
whales and dolphins typically have more than 2000
ganglion cells mm 1 of basilar membrane, which is
double to triple the ganglion cell densities of other
mammals (Ketten, D. R., 2000). By contrast, the ves-
tibular and optic nerves in cetaceans, in comparison to
those of most land mammals, are depauperate.
Cetacean vestibular systems have both far smaller
canal radii than other mammals (the blue whale semi-
circular canals are comparable to those of mice) and
very few nerve fibers. Vestibular fibers comprise less
than 5% of the acousticovestibular nerve cetaceans in
contrast to 40–50% in most terrestrial mammals.
In odontocetes, acute ultrasonic hearing is
achieved by multiple stiffening elements in the
inner ear, including doubled bony membrane suspen-
sions and exceptional thickness-to-width basilar
membrane ratios (1.0 : 0.01) that exceed even those
of bats (Ketten, D. R. and Wartzok, D., 1990).
Odontocete basilar membrane thicknesses typically
range from 25 mm at the base to 5 mm at the apex or
double those of most other species. Basilar membrane
widths vary in the opposite direction; basal widths
are 30–50 mm at the base and increase to 300–500 mm
apically. Thus the odontocete basilar membrane is
relatively thick and narrow. It therefore resembles a
stiff beam throughout its length.
Mysticete membranes are thin rectangles
throughout, with base-to-apex membrane ratios of
0.1 : 0.001 based on thicknesses from 7 mm at the
base to 2 mm at the apex and widths ranging from
100 mm at the base (similar to the base in humans) to
2200 mm at the apex or threefold that of humans and
1.2-fold that of elephants (Ketten, D. R., 2000). These
ratios are directly correlated with the resonant fre-
quencies along the membrane, whereas the gradients
reflect the octave range, which for all cetaceans
implies hearing covering 10–12 octaves.
Pinniped ears are more conventional than those of
cetaceans. External pinnae are reduced or absent in
some species, but conventional external ear canals
are present and functional at least for in-air hearing.
One critical amphibious adaptation in seals and sea
lions is a spiral cartilage–muscle sphincter that seals
the meatus (Møhl, B., 1968), implying that the canal
can be voluntarily closed. Whether the external canal
remains air-filled, collapses, or floods when under-
water remains unclear; neither is it known if the canal
is a functional sound path to the ear in water.
The tympanic and periotic bones of pinnipeds
resemble those of terrestrial mammals. The ear
bones are not acoustically isolated as with those of
cetaceans, and the middle ears only have a moderate
layer of cavernous tissue with a wide range of ossi-
cular chain configurations ranging from very massive
(elephant seal) to moderately stiff (harbor seal;
Møhl, B., 1968; Marsh, S. E. et al., 2001), implying a
wide variation in peak frequencies among species.
Most pinniped inner ears resemble those of terres-
trial high-frequency generalists with evidence for
some ultrasonic, but not well-developed, high ultra-
sonic hearing (Solntseva, G. N., 1990). At least one
species, the elephant seal, has a membrane structure
consistent with better low-frequency hearing than
most other pinnipeds (Wartzok, D. and Ketten, D. R.,
1999)
3.14.5.2 Marine Mammal Audiometrics
Audiograms are available for 11 of the nearly 80
cetacean species (Au, W. W. L., 2000), but the data
are only from smaller odontocetes. Consistent with

2D Graph 4
160
Amazon River dolphin
Beluga dolphin
140 Harbor porpoise
Threshold (dB re 1 uPa)
False killer whale
Bottlenose dolphin
120
100
80
60
40
20
1 10
Frequency (kHz)
Figure 4 Hearing thresholds for a variety of odontocete
cetaceans. Data for the Amazon River dolphin and the
beluga dolphin (Popov, V. and Supin, A., 1990) were
measured using auditory brainstem response methods.
Data from the harbor porpoise (Kastelein, R. et al., 2002),
false killer whale (Thomas, J. A. et al., 1988), and bottlenose
dolphin (Johnson, C. S., 1967) were all obtained with
behavioral measures.
the anatomically derived basilar membrane esti-
mates, electrophysiological and behavioral measures
show functional hearing ranges that span 10 octaves
or more and excellent ultrasonic capacities for the
species tested (Figure 4). Best thresholds measured to
date typically range from 40 dB re 1 mPa to 60 dB re
1 mPa, with peak sensitivities ranging from 12 kHz in
the killer whale (Orcinus orca) to well over 100 kHz in
several species including the freshwater Amazonian
boto (Inia geoffrensis) and the harbor porpoise
(Phocoena phocoena; Nachtigall, P. E. et al., 2000;
Kastelein, R. et al., 2002).
Ultrasonic echolocation signals produced by dol-
phins have been recorded from 21 species and are
highly species specific, although active echolocation
has been demonstrated unequivocally in only the 11
species tested to date (Nachtigall, P. E. et al., 2000).
Virtually all parameters echolocation signals can be
modified by the animal, including pulse repetition
rate, interval, intensity, and spectra, given sufficient
background interference (Au, W. W. L., 2000).
However, the dominant normal click spectra for
each species is relatively constant and ranges
between 12 and 120 kHz, with source levels typically
near 120–140 dB re 1 mPa but reportedly as high
as 230 dB re 1 mPa (summary table in Wartzok, D.
and Ketten, D. R., 1999). Species recorded to date
produce species-stereotypic broadband echolocation
clicks, with peak energy between 10 kHz and
Underwater Hearing 233
200 kHz, burst-pulse click trains, and constant-
frequency (CF) or frequency-modulated (FM) whis-
tles with peak spectra from 4 to 16 kHz (Tyack, P.,
1999) that appear to be used for intraspecific
communication.
Functional significance for species variations in
echolocation and communication signals has not
been fully investigated, but habitat and peak spectra
of echolocation signals are strongly correlated
(Ketten, D. R. and Wartzok, D., 1990). Odontocetes
that employ signals above 100 kHz tend to be inshore,
estuarine, and freshwater dolphins that hunt in rela-
100
tively shallow water environments such as harbors or
rivers. These species locate small fish amidst tangled
roots and stems in heavily silted waters. They have
auditory systems adapted primarily to receive and
analyze ultrahigh frequencies which have short
wavelengths consistent with echolocating small,
nearby objects.
Off-shore animals are generally larger, travel in
highly social pods, and forage in deeper, clearer
waters. These species have broader frequency-adapted
ears consistent with processing ultrasonic but lower-
frequency peak spectra and longer ranging echoloca-
tion signals as well as even lower mid-sonic frequency
whistles for communication with podmates.
Bottlenose dolphins, the most commonly studied
dolphin species, perform 6–8 dB better than an ideal
receiver. Most species are capable of 1–4 azimuthal
resolution, although as little as 0.5 has been
reported for harbor porpoises. Minimal intensity dis-
crimination in bottlenose dolphins (1 dB) equals
human values, and temporal discrimination (8%
of signal duration) is superior to that of humans.
Frequency discrimination in dolphins is significantly
better than in most mammals and is best, unsurpris-
ingly, between 5 kHz and 60 kHz in the most
common species which are mostly offshore (Popper,
A. N., 1980). Intensity discrimination thresholds
(ITD) for odontocetes equal those of any land mam-
mal and decline with increasing sound level.
Measured values range from 1–2 dB for bottlenose
dolphins up to 3–5 dB for harbor porpoises and the
Amazonian boto.
Detection of a source position, known as localiza-
tion, is a third feature at which odontocetes excel.
Two cues are critical for mammalian auditory system
localization: differences in arrival time (interaural
time) and sound level (interaural intensity). On
land, the normal sound path is around the head,
pinna to pinna, and thus the interaural time differ-
ences (ITDs) are calculated based on the distance
234 Underwater Hearing
between receiver points in the head. In most mam-
mals, this is the distance measured around the head
from the center of each pinna divided by the speed of
sound in air. In aquatic animals, however, sound
could travel through the head via tissues with den-
sities close to sea water.
As discussed above, anatomical evidence suggests
that specialized jaw fats act as preferential, low-impe-
dance channels that are able to carry sound to the
middle ear in odontocetes. Behavioral experiments
(Brill, R. L. et al., 1988) found that echolocation by
bottlenose dolphins is impaired if the jaws are blocked
from receiving sounds by neoprene shields. These
results suggest that interjaw distances are the appro-
priate measure for ITD values in odontocetes. The
interjaw or interear distances of dolphins seem large
but because of the speed of sound in water, they equate
to the ear separations of larger bats, which is consistent
with equally good angular resolution in both groups.
In addition to localization, detection of signals in
noise is also critical for echolocation in natural envi-
ronments. Critical bands and critical ratios are two
measures of the ability of an ear to overcome masking,
the phenomenon in which competing sounds elimi-
nate or degrade perception of another (Yost, W. A.,
1994). Odontocetes have more critical bands than most
mammals and smaller critical ratios than humans or
even many bats, making them better than most mam-
mals at detecting signals in noise. The best critical
ratios to date (8–40 dB) are for the false killer whale
(Pseudorca crassidens) which is also the species that has
performed best in echolocation discrimination tasks
(Nachtigall, P. E. et al., 2000; Supin, A. Y. et al., 2003).
Recent studies using auditory evoked potentials
(AEP) or auditory brainstem responses (ABR) employ-
ing amplitude-modulated stimuli (AMS) in bottlenose
dolphins and false killer whales have demonstrated that
odontocetes extract envelope features at higher mod-
ulation frequencies than other mammals, including
humans where they are important for speech percep-
tion, particularly at low frequencies (Dolphin, W. F.,
1995; Supin, A. Y. et al., 2003). These data suggest that
auditory central nervous system adaptations in toothed
whales may include regions specialized for both low
and high frequencies.
There are no direct behavioral or electrophysiolo-
gic hearing data for mysticetes, but deep ocean
stationary arrays and deployable recording tags have
substantially increased knowledge of mysticete
sounds. In general, mysticete vocalizations are signifi-
cantly lower in frequency than those of odontocetes, as
hypothesized from anatomical evidence (Wartzok, D.
and Ketten, D. R., 1999). Mysticete sounds are char-
acterized as low-frequency moans (fundamental
frequency below 200 Hz); simple calls (impulsive, nar-
rowband signals below 1 kHz); complex calls
(broadband pulsatile AM or FM signals); and complex,
seasonally varied songs (Watkins, W. A. and Wartzok,
D., 1985). Infrasonic signals, typically in the 10–16 Hz
range, are well documented in at least two mysticetes,
blue whales (Balaenoptera musculus) and fin whales
(Balaenoptera physalus ; Watkins, W. A., 1981). It has
been speculated that mysticetes use infrasonic signals
for long-distance communication or topographic scale
echolocation, but there is not as yet any clear evidence
or field tests that support the idea.
Pinnipeds are divided into three groups: Phocidae:
true or non-eared seals; Otariidae: eared seals; and
Odobenidae: walruses. Audiometric data show they
vary from partially to fully adapted for underwater
hearing (Figure 5). However, to date it is not certain
how most species accomplish hearing in both media.
One possibility is that pinnipeds have dual systems
operating independently for aquatic and airborne sti-
muli and in different frequency ranges related to
behaviors in each medium (e.g., feeding in water versus
pup location on land). A second possibility is that
pinnipeds are adapted primarily for one environment
or the other or have one system for hearing in both
media but not optimized for either. The current data
suggest that among tested species both of these possible
strategies have evolved.
The 11 pinniped species tested to date have peak
sensitivities between 10 and 30 kHz, with a functional
high-frequency limits up to 75 kHz (Richardson, W. J.
180
Northern elephant seal
California sea lion
160 Harbor seal
Threshold (dB re 1 uPa)
Harp seal
140
120
100
80
60
0.1 1 10 100
Frequency (kHz)
Figure 5 Underwater behavioral response auditory
thresholds for four species of pinniped. Northern elephant
seal and California sea lion from Kastak D. and
Schusterman R. (1998); Harbor seal from Møhl B. (1964);
Harp seal from Terhune J. M. and Ronald K. (1972).

et al., 1995, Kastelein, R. et al., 2002; Southall, B. L. et al.,
2004). Low-frequency functional limits are not yet
well established for most pinnipeds, but parallel stu-
dies of harbor seals (Phoca vitulina) versus elephant
seals (Mirounga angustirostris) suggest that elephant
seals have significantly better underwater low-fre-
quency hearing sensitivity than other pinnipeds
tested to date, with functional hearing down to 75 Hz
(Kastak, D. and Schusterman, R., 1998).
In air pinniped audiograms have peak sensitivities
at slightly lower frequencies than in water (3–10 kHz;
Kastak, D. and Schusterman, R., 1998). Thresholds for
airborne sounds are poorer, on average, in phocids, the
seals, which have no overt pinna, but there is little
difference in aerial versus underwater audiograms for
otariids, the eared seals and sea lions. This implies that
phocids may be better adapted for underwater hear-
ing, whereas otariids evolved a single system that
operates adequately but not optimally in air or water.
In frequency discrimination and localization tasks,
pinnipeds perform more poorly than odontocetes.
Angular resolution ranges from 1.5 to 9.0 , but
most have 4.0 to 6.0 of resolution (Richardson, W.
J. et al., 1995). Minimal intensity discrimination (3 dB)
in California sea lions is poorer than that of dolphins
or humans, but frequency discrimination in phocids
and sea lions is similar to that of bottlenose dolphins.
Critical ratios for pinnipeds are generally equal to
those of dolphins and humans. Like odontocetes,
pinnipeds in water could have small-to-large func-
tional inter-ear distances depending upon whether
they use the external canal, specialized tissues, or
the inner ear as the sound reception point under-
water. However, to date, there are no clear data on
the configuration of any pinniped underwater sound
reception path.
Most pinniped sounds recorded to date are in the
sonic range, and the repertoires are complex, varying
by context, sex, and season (Watkins, W. A. and
Wartzok, D., 1985; Richardson, W. J. et al., 1995).
Call descriptions run the gamut from grunts to
rasps, rattles, and warbles in addition to whistles,
clicks, and pulses ranging from 100 Hz to 15 kHz,
with peak spectra below 5 kHz. Like cetaceans,
source levels in water are commonly near 130 dB re
1 mPa although levels as high as 193 dB re 1 mPa have
been reported (Richardson, W. J. et al., 1995). Despite
producing click-like sounds, there is no evidence that
pinnipeds are able to echolocate. Infrasonic to seismic
sounds are produced by northern elephant seals in
air. Thus, both air and underwater vocalizations for
these amphibious species, like those of cetaceans and
Underwater Hearing 235
other mammals, are consistent with conclusions from
ear models and with the general characteristics of
audiograms in tested species.
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