4
DOUGLAS WARTZOK AND DARLENE R. KETTEN
Marine Mammal Sensory Systems
Sensory systems evolved to allow animals to receive and
process information from their surroundings. To understand how sensory systems operate in any given environment, we must understand how the physical characteristics
ofthat environment affect the available information and its
propagation and reception. In a very real sense we need to
look at both the medium and the message (McLuhan and
Fiore 1967). Signals in the marine environment can be substantially different from those in air, and the oceanic medium
itselfchanges the message in a number ofways.
When their evolutionary paths took them into the
oceans, marine mammals had to adapt sensory systems that
had evolved in air into ones that were able to detect and
process Signals in water. The sensory systems of marine
. mammals are functionally similar to those of terrestrial
mammals in that they act as highly selective filters. If every
environmental cue available received equal attention, the
brain would be barraged by sensory inputs. Instead, sensory
organs are filters, selecting and attending to signals that, evolutionarily, proved to be important. Consider how predator
and prey are driven to be both similar and different sensorially. Because their activities intersect in place and time, they
need to have similar visual sensitivities, but different fields
of view. The predator usually has binocular overlap that
provides a precise judgment of distance to the prey. The
prey may forego binocular vision and accurate visual depth
judgments in favor ofgreater lateral visual fields to detect a
predator. Thus, two species may have overlapping sensory
ranges, but no two have identical sensory capacities. Consequently, each animal's perceived world is only a subset ofthe
real phYSical world, that is, it is a species-specific model, constructed from the blocks ofdata its senses can capture.
In animal behavior, this concept is called the Umwelt (von
UexkU1l1934). As a technical term, Umwelt means an animal's perceptually limited construct of the world. In common usage, it simply means the environment. This dual
meaning reflects the complex interaction ofsensory adaptations and habitat. Senses are tuned to relevant stimuli by evolution but are limited by the physical parameters ofthe habitat. For example, human sensory systems are geared to
diurnal, airborne cues. Humans are highly developed visually, with 38 times more optic nerve fibers than auditory
nerve fibers, and a hearing range (20 to 20,000 Hz) that is narrower than that ofmany other animals. By observing species
adapted to different habitats and analyzing their sensory biology, we can learn how they detect and use phYSical cues
that are normally imperceptible to us. Ifwe develop technology that translates those cues into our sensory ranges, we
can glimpse at the world as other species perceive it. Marine
mammals offer us a very special glimpse. In aquatic environ117
In: Biology ofMarine Mammals. J. Reynolds and S. Rommel (eds.), Smithsonian Institution Press, 1999, pp. 117-175.
118
DOUGLAS WARTZOK AND
DARLENE R.
KETTEN
ments, our air-adapted senses are out of their element and
are effectively detuned. By studying marine mammal sensory systems and abilities, we can understand how land
mammal senses were evolutionarily retuned to operate in
water. From that knowledge, we gain a valuable window
into the oceans, the most extensive and unexplored environment on earth.
In this chapter, we discuss marine mammal audition, vision, chemoreception, tactile sensation, and magnetic detection. We begin with an overview of the basic aspects of
sensory receptor systems, and then, for specific sensory systems, examine how water versus air affects the parameters
and propagation ofrelated Signals and discuss how air-based
receptors were adapted to function effectively in an aquatic
environment. Different sensory systems and different marine mammal groups (sirenians, cetaceans, pinnipeds, fissipeds, ursids) are discussed in varying detail based on the
extent ofdata available for each.
Generally, the term sensory system refers to the peripheral, as opposed to the brain, or central, components an
animal uses to detect and analyze a signal. There are four essential functions for any sensory system: (1) capture an environmental signal, (2) filter it, (3) transduce it to a neural
impulse, and (4) send processed information to the central
nervous system. Each function may involve more than one
form ofreceptor or peripheral processor. The block diagram
in Figure 4-1 compares a generic sensory receptor system
with equivalent stages for mammalian eyes and ears. In vision, the first step, signal capture, is accomplished by the re-
fraction oflight at the cornea and the pupil's ability to control
the light intensity entering the eye. Second, the lens focuses
light on the retina while also acting as a first-stage filter, passing only some portions of the full spectrum of light. The
tapetum, a reflective layer behind the retina, reflects the photons not captured on the first passage through the retina back
through for a second chance at absorption. Third, pigments
within the rod and cone receptor cells absorb each wavelength with a different efficiency. Fourth, the rods or cones
pass a chemical signal to horizontal or bipolar cells that modify and transmit the Signal to amacrine or ganglion cells. Axons ofganglion cells make up the optic nerve, which passes
signals to midbrain structures and ultimately to the cortex.
In hearing, the first step is the capture ofsound by the external ear. The external ear and the ear canal act as first-stage
filters, attenuating some sounds based on their direction
(pinnal shadowing) and amplifying others according to the
resonance characteristics ofthe outer ear and canal. Second,
the middle ear components act as second stage filters. The
middle ear bones mechanically transmit vibrations of the
eardrum, or tympanic membrane, to the oval window,
which is the acoustic entrance to the fluid-filled inner ear.
This bony chain acts as a series oflevers that provides a nearly
4o-dB boost to the incoming signal, which compensates for
the loss ofacoustic power that would normally occur from a
simple transmission of sound in air into flUid. The mass,
stiffuess, and shape ofthe middle ear cavity and ofthe middle
ear ossicular chain also influence the efficiency with which
different frequencies are transmitted to the inner ear. Third,
Figure 4-1. A generic sensory system is shown with
parallel stages for mammalian
visual and auditory systems.
Conditoning
&
Transmission
Lens focusing
& Tapetal
Reflection
Middle ear
Ossicular
Impedance
Match
& Amp6fication
Optic nerve
Marine Mammal Sensory Systems
at the level of the inner ear, the basilar membrane acts as a
bank of filters that determine the range of frequencies the
brain will ultimately process. The detectable sound or "hearing" range is dictated by the stiffness and mass characteristics
of this membrane. Fourth, when sensory cells with flexible
cilia, the hair cells, are bent through the motion ofthe basilar
membrane, a chemical signal is transmitted via the auditory
afferent (inward) fibers to the brainstem. Thus, in both the
eye and ear, the'signal goes through a minimum ofthree and
as many as five layers of signal processing before it is transformed into a neural impulse.
For both sensory systems, there is extensive central processing as well as efferent (outward) feedback signals from
the central nervous system that affect the responses at the
receptor. Depending on the stimulus, the behavioral and
physiologic state of the animal, and the type of receptor, a
stimulus can be perceived but elicit no action, or it can
prompt a set of signals to be sent to an effector that modulates the stimulus intensity, as in withdrawal from pain,
pupillary contraction in bright light, or rotation ofthe head
or pinna to enhance detection ofa particular sound. Now we
turn to a more detailed look at individual sensory systems.
Audition
Hearing is simply the detection of sound. "Sound" is the
propagation ofa mechanical disturbance through a medium.
In elastic media, such as air and water, that disturbance takes
the form of acoustic waves. The adaptive significance of
sound cues is underscored by the ubiquity ofhearing. There
are lightless habitats on earth with naturally blind animals,
but no terrestrial habitat is without sound, and no known
vertebrate is naturally profoundly deaf.
Mechanistically, hearing is a relatively simple chain of
events: sound energy is converted by biomechanical transducers (middle and inner ear) into electrical signals (neural
impulses) that provide a central processor (brain) with
acoustic data. Mammalian ears are elegant structures, packing more than 75,000 mechanical and electrochemical components into an average volume of 1 cm'. Variations in the
structure and number ofthese components account for most
ofthe hearing capacity differences among mammals (for an
overview, see Webster et al. 1992).
Normal functional hearing ranges and the sensitivity at
each audible frequency (threshold, or minimum intensity
required to hear a given frequency) vary widely by species
(Fig. 4-2). "Functional" hearing refers to the range of frequencies a species hears without entraining nonacoustic
mechanisms. In land mammals, the functional range is generally considered to be those frequencies that can be heard at
thresholds below 60 dB SPL. (dB SPL refers to a decibel measure of sound pressure level. The basis for this measure and
how it differs in air and water are explained in detail in the
next section.) For example, a healthy human ear has a potential maximum frequency range of0.02 to 20 kHz, butthe normal functional hearing range in an adult is closer to 0.04 to 16
kHz. 1 In humans, best sensitivity (lowest thresholds) occurs
between 500 Hz and 4 kHz, which is also where most ofthe
acoustic energy in speech occurs (Fig. 4-2; Schuknecht 1993;
Yost 1994). To hear frequencies at the extreme ends of any
animal's total range generally requires intensities that are
uncomfortable, and some frequencies are simply unde-
100
.... human
...... owl monkey
-e-
80
C.
60
-
40
In
"0
' ''0
'0
.c:
UI
...
CI)
.c:
I-
rat
cow
.... elephant
-0- dog
...... opossum
.... bat
-0-
...J
CJ)
20
0
-20 +-~~~.,.--~~~.---~~~r--~~.........,..,r---~
10
100
.1
1
.01
Frequency (kHz)
119
Figure 4-2. Audiograms ofrepresentative
terrestrial mammals. Note that the ordinate
is labeled dB SPL and therefore, thresholds
are atornearO dB in the regions ofbest
sensitivity for most species (data compiled
from Fay 1988). The human curve ends
abruptly near 100 Hz at its low-frequency
end because most human hearing smdies
have focused on speech perception and
subjects are not tested over the full human
hearing range. Compare these audiograms
for land mammals in air with the underwater
audiograms for cetaceans and pinnipeds in
Figure 4-5, taking into consideration the
effect that differing reference pressures have
on reported threshold values.
120
DOUGLAS WAR TZOK AND
DARLENE R.
KETTEN
teetable because oflimitations in the resonance characteristics of the middle and inner ear. Exceptionally loud sounds
that are outside the functional range of normal hearing
can sometimes be perceived through bone conduction or direct motion ofthe inner ear, but this is not truly an auditory
sensation.
Analyzing how hearing abilities, habitat, and ear anatomy are linked in different species, particularly in animals
from diverse habitats, provides insights into how each component in the auditory periphery functions and how different hearing capacities evolved. "Sonic" is an arbitrary term
that refers to the maximal human hearing range. Frequencies outside this range are deemed infrasonic (below 20 Hz)
or ultrasonic (above 20 kHz). Ofcourse, many animals hear
sounds inaudible to humans. Most mammals have some ultrasonic hearing (Le., can hear well at ultrasonic frequencies)
and a few, like the Asian elephant (Elephas maximus) hear infrasonic signals (Fig. 4-2).
Hearing ranges are both size and niche related. In general, mammalian ears scale with body size (Manley 1972;
Ketten 1984, 1992; West 1985). Inland mammals, the highest
frequency an animal hears is generally inversely related to
body mass; smaller animals typically have good high frequency hearing, whereas larger animals tend to have lower
overall ranges (von Bekesy 1960, Greenwood 1962, Manley
1972, Ketten 1984). Yet, regardless of size, crepuscular and
nocturnal species typically have acute ultrasonic hearing,
whereas subterranean species usually have good infrasonic
hearing, and, in some cases, can detect seismic vibrations
(Sales and Pye 1974, Heffner and Heffner 1980, Payne et al.
1986, Fay 1988).
How well do marine mammals mesh with this general
land mammal hearing scheme? Marine mammals evolved
from land-dwelling ancestors during the explosive period of
mammalian radiation (see Barnes et al. 1985). Today, marine
mammals occupy Virtually every aquatiC niche (freshwater
to pelagic, surface to profundal) and have a size range ofseveral magnitudes (e.g., harbor porpoise [Phocoena phocoena],
1 m and 55 kgvs. the blue whale [Balaenoptera musculus], 40 m
and 94,000 kg; Nowak 1991). Water is a relatively dense
medium in which light attenuates much faster than sound,
therefore marine mammals are, in a sense, de facto crepuscular species, but we also expect to see a wide range ofhearing given their diversity of animal size and habitat. Because
marine mammals retained the essentials ofair-adapted ears,
that is, an air-filled middle ear and spiral cochlea, some similarities in hearing mechanism between land and aquatic
mammals would not be surprising. In fact, hearing in marine
mammals has the same basic size versus auditory structure
relationship as in land mammals, but marine mammals have
a significantly different auditory bauplan, or ear size versus
frequency relationship (Solntseva 1971, 1990; Ketten 1984,
1992). Consequently, although some marine mammals, consistent with their size, hear well at low frequencies, the
majority, despite their relatively large size, hear best at ultrasonic frequencies because of unique auditory mechanisms
that evolved in response to the marine environment.
Land and marine ears have significant structural differences. Because of some of these differences, a common
definition of the term ear is somewhat problematiC. In this
chapter, ear is used in the broadest sense to encompass all
structures that function primarily to collect and process
sound. As marine mammal ancestors became more aquatic,
air-adapted mammalian ears had to be coupled to waterborne sound for hearing to remain functional. Ear evolution took place in tandem with, and in part in response to,
body reconfigurations.Just as the physical demands ofoperating in water exacted a structural price in the locomotory
and thermoregulatory systems of marine mammals (see
Pabst, Rommel, and McLellan, Chapter 2, this volume),
physical differences in underwater sound required auditory
system remodeling. In modern marine mammals, the extent of ear modifications parallels the level ofaquatic adaptation in each group (Ketten 1984, 1992; Solntseva 1990).
The greatest differences from land mammals are found in
cetaceans and sirenians. As they evolved into obligate
aquatic mammals, unable to move, reproduce, or feed on
land, every portion of the head, including the auditory periphery, was modified. Modern cetaceans have the most derived cranial structure ofany mammal (Barnes and Mitchell
1978, Barnes et al. 1985). "Telescoping," a term coined by
Miller (1923), refers to the evolutionary revamping of the
cranial vault as the maxillary bones of the upper jaw were
transposed back to the vertex of the skull, overlapping the
compressed frontal bones. As the rostrum elongated, the
cranial vault foreshortened, and the nares and narial passages were pulled rearward to a dorsal position behind
the eyes. Telescoping may have been related primarily to
changes that allow respiration with only a small portion of
the head exposed, but it also produced a multilayer skull that
has a profound effect on how sound enters and leaves the
cetacean head. Many land mammal auditory components,
like external pinnae and air-filled external canals, were lost
or reduced and the middle and inner ears migrated outward. In most odontocetes, the ears have no substantial
bony association with the skull. Instead, they are suspended
by ligaments in a foam-filled cavity outside the skull. Consequently, they are effectively acoustically isolated from bone
conduction, which is important for echolocation. There are
also few bony, thin-walled air chambers, which is important
for avoiding pressure-related injuries. Specialized fatty tissues (low impedance channels for underwater sound recep-
Marine Mammal Sensory Systems
tion) evolved that appear to function in lieu of external airfilled canals.
Mysticete ears are also specialized but they appearto have
been shaped more by size adaptations than by special hearing functions. Sirenian ears are not as well understood, but
they too appear to have many highly derived adaptations for
underwater sound reception. Today, cetacean and sirenian
ears are so specialized for waterborne sound perception that
they may no longer be able to detect or interpret airborne
sound at normal ambient levels. On the other hand, ears of
sea otters (Enhyra lutris) and some otariids have very few
anatomical differences from those of terrestrial mammals,
and it is possible these ears represent a kind of amphibious
compromise or even that they continue to be primarily air
adapted.
That brings us to three major auditory questions: (1) How
do marine and terrestrial ears and hearing differ?; (2) How do
these differences relate to underwater sound perception?;
and (3) How do amphibious species manage hearing in both
domains? To address these questions requires collating a
wide variety of data. Behavioral and electrophysiological
measures are available for some odontocetes and pinnipeds,
but there are no published hearing curves for any mysticete,
sirenian, or marine fissiped. Anatomical correlates of hearing are fairly well established (Greenwood 1961,1962,1990;
Manley 1972; for reviews, see Fay 1988,1992; Echteler et al.
1994). Anatomical data are available on some aspects ofthe
auditory system for approximately one-third of all marine
mammal species, including nearly half of the larger, noncaptive species. Therefore, to give the broadest view of current marine mammal hearing data, both audiometric and
anatomical data are discussed. An outline of physical measures ofsound in air versus water and ofthe basic mechanisms
of mammalian hearing are given first as background for
these discussions.
Sound in Air Versus Water
In analyzingmarine mammal hearing, it is important to consider how the physical aspects of sound in air versus water
affect acoustic cues. Basic measures ofsound are frequency,
speed, wavelength, and intensity. Frequency if), measured
in cycles Isec or hertz (Hz), is defined as:
f=c/'A,
=
(equation 1)
=
where c the speed of sound (m/sec) and 'A the wavelength (mkycle). The speed of sound is directly related to
the density of the medium. Because water is denser than
air, sound in water travels faster and with less attenuation
than sound in air. Sound speed in moist ambient surface air
is approximately 340 m/sec. 2 Sound speed in seawater aver-
121
ages 1530 m/sec, but varies with any factor affecting density. The principal physical factors affecting density in seawater are salinity, temperature, and pressure. For each 1%
increase in salinity, speed increases 1.5 m/sec; for each 1°C
decrease in temperature, speed decreases 4 m/sec; and for
each 100 m depth, speed increases 1.8 m/sec (Ingmanson
and Wallace 1973). Because these factors act synergistically, the ocean has a highly variable sound profile that may
change both seasonally and regionally (Fig. 4-3). For practical purposes, in-water sound speed is 4.5 times faster than
in air and, at every frequency, the wavelength is 4.5 times
greater than in air.
How do these physical differences affect hearing? Mammalian ears are primarily sound-intensity detectors. Intensity, like frequency, depends on sound speed and, in turn, on
denSity. Sound intensity (1) is the acoustic power (P) impinging on surface area (a) perpendicular to the direction of
sound propagation, or power/ unit area (I Pia). In general
terms, power is force (F) times velocity (P Pv). Pressure is
force I unit area (p Pia). Therefore, intensity can be rewritten as the product of sound pressure (p) and vibration velocity (v):
=
=
=
(equation 2)
I= Pia =Pvla =pv
For a traveling spherical wave, the velocity component
becomes particle velocity (u), which in terms of effective
sound pressure can be defined as p I pc where p is the density
ofthe medium. The product pc is called the charateristic impedance ofthe medium.
We can then redefine intensity (equation 2) for an instantaneous sound pressure for an outward traveling plane wave
in terms ofpressure, sound speed, and denSity:
(equation 3)
I=pv= p(plpc) =p2/pc
=
=
=
=
Recall that for air c 340 m/sec and for seawater c 1530
m/sec; for air, p
0.0013 glcm3 ; for seawater, p
1.03
3
glcm • The follOwing calculations using the intensity-pressure-impedance relation expressed in equation 3 show how
the differences in the physical properties ofwater versus air
influence intensity and acoustic pressure values:
lair
=p2 1(0.0013 glcm3)(340 m/sec)
=p2 I (0.442 g-m/sec-cm
Iwater
3
)
=p2 1(1.03 glcm )(1530 m/sec)
=p2 1(1575 g-m/sec-cm3)
3
To examine the sensory implications ofthese differences,
we will construct a hypothetical mammal, the neffin ("never
found in nature"), that hears equally well in water as in air.
For this to be trUe, the neffin, with an intenSity-based ear,
would require the same acoustic power/ unit area in water as
in air to have an equal sound percept, or (Iair IwateJ
=
122
DOUGLAS
WARTZOK AND DARLENE R.
KETTEN
sound speed (mlsec)
1460
1470
1480
1490
1500
1510
1520
Mixed
500
Thermocline
1000
g
2000
Deep Isothermal
.c
is.
Ql
"tl
1530
2500
Figure 4-3. Sound speed profiles fortemperate, tropical, and polar conditions. In
polar waters, there is an inverse trend close ro
the surface where the water is near freezing;
density and therefore, velOCity decrease.
(Adapted from Ingmanson and Wallace 1973
andJensen et aI. 1994.)
4000
lair
= P;i) (0.442 g-m/sec-cm3 ) = Iwater
=P~,",e/ (1575 g-m/sec-cm3 )
p;iP565.4)
Pa;/59.7)
=
=P~ater
(equation 4)
Pwarer
This implies that the sound pressure in water must be approximately 60 times that required in air to produce the same
intensity and therefore, the same sensation in the neffin ear.
For technological reasons, received intensity, which is
measured in watts 1m2 , is difficult to determine. Consequently, to describe .hearing thresholds, we capitalize on the
fact that intensity is related to the mean square pressure of
the sound wave over time (equation 3) and use an indirect
measure, effective sound pressure level (SPL) (for discussion,
see Au 1993). Sound pressure levels are conventionally expressed in decibels (dB), defined as:
dBSPL= 10logcp~/p;)
=20 log CPm/Pr)'
(equation 5)
where Pm is the pressure measured and Pr is an arbitrary reference pressure. Currently, two standardized reference pressures are used. For airborne sound measures, the reference is
dB SPL or dB re 20 J..l.Pa rms, derived from human hearing. 3
For underwater sound measures, the reference pressure is
dB re 1 J..l.Pa. Notice that decibels are expressed on a logarithmic scale based on a ratio that depends on reference pressure.
In the earlier hypothetical example, with identical reference pressures, the neffin needed a sound level approximately 35.5 dB greater in water than in air (from equation 4,
10 log 3565.4) to hear equally well in both. However, if conventional references for measuring levels in air versus water
are used, the differences in reference pressure must be considered as well. This means that to produce an equivalent
sensation in a submerged neffin, the underwater sound pressure level in water would need to be 35.5 dB + 20 (log 20) dB
greater than the airborne value. That is, a sound level of61.5
dB re 1 J..l.Pa in water is equivalent to 0 dB re 20 J..l.Pa in air. To
the neffin, they should sound the same because the intensities are equivalent. Thus, underwater sound intensities with
conventional 1 J..l.Pa reference pressures must be reduced by
61.5 dB for gross comparisons with in-air sound measures using a 20 J..l.Pa reference pressure.
It is important to remember that these equations describe
idealized comparisons of air versus waterborne sound. In
comparing data from different species, bear in mind that experimental conditions can significantly impact hearing data.
Both subtle and gross environmental effects (salinity, temperature, depth, ambient noise, surface reflection, etc.) as well as
individual state (motivation, age, pathology) influence results.
Comparisons ofterrestrial and marine mammal hearing data
are particularly difficult because we have no underwater
equivalent of anechoic chambers; results are often obtained
from few individuals, and test conditions are highly variable.
Basic Hearing Mechanisms
Hearing capacities are the output of the integrated components ofthe whole ear. All mammalian ears, including those
Marine Mammal Sensory Systems
ofmarine mammals, have three basic divisions: (1) an outer
ear, (2) an air-filled middle ear with bony levers and membranes, and (3) a fluid-filled inner ear with mechanical resonators and sensory cells. The outer ear acts as a sound collector. The middle ear transforms acoustic components into
mechanical ones detectable by the inner ear. The inner ear
acts as a band-pass filter and mechanochemical transducer of
sound into neural impulses.
The outer ear is subdivided conventionally into a pinna or
ear flap that assists in localization and the ear canal. The size
and shape of each component in each species is extraordinarily diverse, which makes any generalized statement
about the function ofthe outer ear debatable. In most mammals, the pinnal flaps are distinct flanges that may be mobile.
These flanges act as sound diffractors that aid in localization,
primarily by acting as a funnel that selectively admits sounds
along the pinnal axis (Heffuer and Heffuer 1992).
The middle ear is commonly described as an impedancematching device or transformer that counteracts the approximately 36-dB loss from the impedance differences between air and the fluid-filled inner ear, an auditory remnant
of the original vertebrate move from water onto land. This
gain is achieved by the mechanical advantage provided by
differences in the middle ear membrane areas (large tympanic vs. small oval window) and by the lever effect ofthe ossicular chain that creates a pressure gain and a reduction in
particle velocity at the inner ear.
Improving the efficiency of power transfer to the inner
ear may not, however, be the only function for the middle
ear. Recent studies on land mammals have led to a competing (but not mutually exclusive) theory called the peripheral filter-isopower function, in which the middle ear has a
"tuning" role (for comprehensive discussions, see Zwislocki 1981, Rosowski 1994, Yost 1994). The middle ear varies
widely among species in volume, stiffuess (K), and mass (M).
Each species has a characteristic middle ear resonance based
on the combined chain of impedances, which, in turn, depends on the mechanical properties ofits middle ear components. For any animal, the sum ofimpedances is lowest (i.e.,
middle ear admittance is greatest and energy transmission
most efficient), atthe middle ear's resonant frequency (f). As
expected, this frequency also tends to be at or near the frequency with the lowest threshold (best sensitivity) for that
species (Fay 1992).
Stiffuess and mass have inverse effects on frequency in a
resonant system:
f=
Gn) )
K/ M.
(equation 6)
Put another way, mass-dominated systems have a lower resonant frequency than stiffuess-dominated systems. Increasing stiffuess in any ear component (membranes, ossicles,
123
cavity) improves the efficiency of transmission of high frequencies. Adding mass to the system (e.g., by increasing cavity volume or increasing ossicular chain mass) favors low
frequencies. Consequently, in addition to impedance matching, middle ears may be evolutionarily tuned by different
combinations ofmass or stiffening agents in each species. Ultrasonic species, like microchiropteran bats and dolphins,
have ossicular chains stiffened with bony struts and fused articulations (Reysenbach de Haan 1956, Pye 1972, Sales and
Pye 1974, Ketten and Wartzok 1990). Low frequency species,
like heteromyid desert rodents, mole rats, elephants, and
mysticetes, have large middle ears with flaccid tympanic
membranes (Webster 1962; Hinchcliffe and Pye 1969; Webster and Webster 1975; Fleischer 1978; Ketten 1992, 1994).
Inner ears are similarly tuned, in that inner ear stiffuess
and mass characteristics are major determinants of speciesspecific hearing ranges. The inner ear consists ofthe cochlea
(primary hearing receptor; Fig. 4-4) and the vestibular system (organs of orientation and balance). Mammalian inner
ears are precocial, that is, they are structurally mature and
functional at birth and may be active in utero. The cochlea is
a fluid-filled spiral containing a primary resonator, the basilar membrane, and an array ofneuroreceptors, the organ of
Corti (see Fig. 4-7). When the basilar membrane moves, cilia
on the hair cells of the organ of Corti are deflected eliciting
chemical changes that release neurotransmitters. Afferent
fibers ofthe auditory nerve (cranial nerve VIII) synapsing on
the hair cells carry acoustic details to the brain, including frequency, amplitude, and temporal patterning of incoming
sounds. Efferent fibers also synapse with the hair cells, but
their function is not yet fully understood.
A key component in this system is the basilar membrane.
Interspecific differences in hearing ranges are dictated
largely by differences in stiffuess and mass that are the result
of basilar membrane thickness and width variations along
the cochlear spiral. Because the cochlea is a spiral with a
decreasing radius, the spiral portion with the largest radius (closest to the oval and round windows) is referred to
as the base or basal turn; the section with the smallest radius
(farthest from the middle ear) is the apex or apical turn.
From base to apex, changes in the construction ofthe basilar
membrane in each mammal mechanically tune the ear to a
specific set offrequencies. Each membrane region has a particular resonance characteristic and consequently greater
deflection than other regions ofthe membrane for a particular input frequency. For an animal to be sensitive to a sound,
its basilar membrane must have resonance capabilities
matching that sound at some pOint along the cochlear spiral.
For any input signal within the hearing range of the animal, the entire basilar membrane responds to some degree.
At anyone moment, each region ofthe membrane has a dif-
124
DOUGLAS WAR TZOK AND
DARLENE R.
KETTEN
semi-circular ........-I
canals
auditory
nerve
:I
~:=;~"X'~'
ferent amount of deflection and a different phase related to
the input signal. Over time, changes in amplitude and phase
at each point give the impression of a traveling response
wave along the cochlea, but because the membrane segments that have resonance characteristics closest to frequencies in the signal have greater displacements than other segments ofthe membrane, a characteristic profile or envelope
develops for the signal.
Basilar membrane dimensions vary inversely, and generally regularly, with cochlear dimensions. The highest frequency each animal hears is encoded at the base of the
cochlear spiral (near the oval window), where the membrane is narrow, thick, and stiff. Moving toward the apex of
the spiral, as the membrane becomes broader and more
pliant, progressively lower frequencies are encoded. Therefore, mammalian basilar membranes are essentially tonotopically arranged resonator arrays, ranging high to low
from base to apex, rather like a guitar with densely packed
strings graded to cover multiple octaves. 4 The ear, however,
is a reverse instrument in that sound energy is the primary
input rather than a product, and it is the differential tuning
based on the construction of the inner ear membrane
"string" array that forms the basis of hearing range differences among species.
Recall from the earlier discussion of animal size in relation to hearing that, in general, small mammals have good
high frequency hearing characteristics and large mammals
have comparatively low hearing ranges. Early inner ear
models were based on the assumption that all mammalian
basilar membranes were constructed ofsimilar components
that had a constant gradient with length and that length
Figure 4-4. The drawing illustrates rhe
fundamental structure ofa mammalian inner
ear with a 2.5 turn cochlea and 3 semicircular
canals. A wedge has been removed from the
basal turn to show rhe rhree chambers or
scalae in rhe cochlea. (See Fig. 4-7 for additionalintracochlear detail.) ScM, scala media;
SeT, scala tympani; ScV; scala vestibuli.
(Figure was redrawn to scale based on illustrations ofhuman and guinea pig ears in
Lewis et al. 1985.)
scaled with animal size. On average, smaller animals were
assumed to have shorter, narrower, stiffer membranes,
whereas larger animals had longer, broader, less stiff membral1es (von Bekesy 1960; Greenwood 1961, 1990). Given
that assumption, frequency distributions in the inner ear of
any species could be derived by comparing one parameter,
basilar membrane length, with an arbitrary standard, the av·
erage human membrane length. For many land mammals,
this assumption is correct, but only because length is an indirect correlate ofother key features for basilar membrane resonance. For these ears, now termed generalists (Fay 1992,
Echteler et al. 1994), basilar membrane thickness and width
covary regularly with length; therefore, length can proportionately represent sti.ffuess.
Only recently has it become clear that some species,
termed specialists (Echteler et al. 1994), do not have the same
thickness-width-length relationship as do generalist land
mammals (Manley 1972; Ketten 1984,1997). Most specialist
animals have retuned their inner ears to fit an atypical tuning
for their body size by either increasing mass to improve low
frequency sensitivity in small ears (as in mole rats) or adding
stiffening components to increase resonant frequencies in
larger inner ears (as in dolphins) (Hinchcliffe and Pye 1969,
Sales and Pye 1974, Webster and Webster 1975, Ketten 1984).
The most extreme case of specialization is to be found in
some bats, which have relatively constant basilar membrane
dimensions for about 30% ofthe cochlea and thereby devote
a disproportionate amount of the membrane to encoding
very narrow bands offrequenCies related to a component of
their echolocation signal (Bruns and Schmieszek 1980, Vater
1988a, K6ssl and Vater 1995).
Marine Mammal Sensory Systems
Marine mammal ears fall into both categories and some
species have a mix ofgeneralist and specialist traits. Like land
mammals, pinnipeds and cetaceans have basilar membranes
that scale with animal size. Consequently, because marine
mammals are relatively large, most have basilar membranes
longer than the human average. Ifmarine mammal ears followed the generalist land mammal pattern, most would have
relatively poor ultrasonic hearing. For example, standard
land mammal length-derived hearing models (Greenwood
1961, 1990; Fay 1992) predict an upper limit ofhearing ofapproximately 16 kHz for bottlenose dolphins (Tursiops truncatus), which actually have a functional high frequency hearing
limit of 160 kHz (Au 1993). Before the discovery of dolphin
echolocation, it was assumed that these large animals had
predominately low functional hearing ranges similar to
cows. Hearing is not constrained to low frequencies in marine mammals, because they have radically different inner
ear thickness-width gradients than generalist land mammals. In odontocetes, very high ultrasonic hearing is related
also to the presence ofextensive stiffening additions to the inner ear. These features, discussed in detail later, demonstrate
the usefulness of comparative audiometric and anatomical
studies for teasing apart sensory mechanisms. In fact, one
important outgrowth of marine mammal hearing studies
has been the development of multifeature hearing models
that are better predictors of hearing characteristics for all
mammals than traditional, single-dimension models (Ketten 1994).
Marine Mammal Sound Production
Recordings of naturally produced sounds are available for
most marine mammal species (Watkins and Wartzok 1985),
and they proVide the broadest acoustic framework for hearing comparisons. Sound production data obtained in a wide
variety ofbackground noise conditions cannot be used to infer hearing thresholds because it is likely that produced
sound levels are elevated over minimum audible levels to
override background noise. For example, some recordings of
odontocete and mysticete sounds have source levels estimated to be as high as 180 to 230 dB re 11lPa (Richardson et
al. 1991, Au 1993, Wtirsig and Clark 1993). However, because
mammalian vocalizations typically have peak spectra at or
near the best frequency for that species, they are generally
good indirect indicators offrequencies the animal normally
hears well (Sales and Pye 1974, Popper 1980, Watkins and
Wartzok 1985, Henson et al. 1990, Ketten and Wartzok 1990,
Popov and Supin 1990a). A classic example is the discovery of
ultrasonic signal use by dolphins (Kellogg 1959, Norris et al.
1961), which prompted several decades ofinvestigations into
125
echolocation and ultrasonic hearing abilities in marine
mammals.
Cetaceans
Cetaceans can be divided into high and low frequency sound
producers, which are coincident with the two suborders
(Table 4-1). Sound production data for odontocetes are consistent with the audiometric data (Le., ultrasonic use is common and differences in peak spectra ofproduced sounds are
consistent with best frequency ofhearing in species that have
been tested) (compare Table 4-1 and Fig. 4-5A). Mysticete
sound production data imply they are primarily low frequency animals, and it is likely that many baleen species hear
well at infrasonic frequencies.
Odontocetes produce species-stereotypic broadband
clicks with peak energy between 10 and 200 kHz, individually variable burst pulse click trains, and constant frequency
(CF) or frequency modulated (FM) whistles ranging from 4
to 16 kHz (see Tyack, Chapter 7, this volume). Ultrasonic signals are highly species specific and have been recorded from
21 species, although echolocation (or 'biosonar") has been
demonstrated in only 11 species ofsmaller odontocetes (Au
1993). All modern odontocetes are assumed, like bats, to be
true echolocators, not simply ultrasonic receptors. That is,
they "image" their environment by analyzing echoes from a
self-generated ultrasonic signal (Kellogg 1959, Norris et al.
1961, Popper 1980, Wood and Evans 1980, Pilleri 1983,
Watkins and Wartzok 1985). Echolocation is a two-way
function; to be an effective echolocator, an animal must have
a coordinated means ofgenerating a highly directional signal
and receiving its echo. For this reason, evidence for high frequency ears alone is not sufficient to determine whether any
marine mammal (or fossil species) is an echolocator.
Captive odontocetes routinely vary pulse repetition rate,
interpulse interval, intensity, and click spectra, particularly
in response to high ambient noise (Schevill 1964, Norris
1969,Auetal.1974,Popper 1980, Thomas et al. 1988,Moore
1990, Popov and Supin 1990a). Normally, however, each
species has a characteristic echolocation frequency spectrum (Schevill1964, Norris 1969, Popper 1980). Well-documented peak spectra ofodontocete sonar signals range from
approximately 20 kHz up to 160 kHz with source levels as
high as 228 dB, but more commonly in range of120 to 180 dB
(Table 4-1).
There are strong correlations between habitat types, societal differences, and peak spectra (Gaskin 1976, Wood and
Evans 1980, Ketten 1984). Considering that frequency and
wavelength are inversely related, there is an inverse relationship between frequency and the size of the object or detail
that can be detected with echolocation. On the basis oftheir
Table 4-1.
Scientific Name
Marine Mammal Sound Production Characteristics
Common Name
Signal Type
Frequency
Range
(kHz)
Frequency Near
Source Level
Maximum
Energy (kHz)
(dBre 1 J.lPa)
References
(Partial references only for some species)
Cetacea
Odontoceti
Delphinidae
Cephalorhynchus
commersonii
Commerson's
Pulsed sounds
< 10
Clicks
Click
C. heavisidii
Heaviside's dolphin
C. heetori
Hector's dolphin
Delphinus delphis
Common dolphin
Feresa attenuata
Globicephala
macrorhynchus
Pygmy killer whale
Short-finned pilot
whale
G. melaena
Long-finned pilot
whale
Grampus griseus
Lagenodelphis
hosei
Lagenorhynchus
acutus
L. albirostris
L. australis
Risso's dolphin
Fraser's dolphin
Pulsed sounds
Click
Click
Pacific white-sided
dolphin
L. obscurus
Dusky dolphin
Northern right
whale dolphin
Killer whale
False killer whale
0.8-5'
0.8-4.5'
2-5
112-135
160
150-163
0.5-18
4-16
0.2-150
30-60
23-67
0.5-> 20
2-14
180
Click
Whistles
30-60
1.6-6.7b
180
1-8
Clicks
Click
Whistles
Rasp/pulse
burst
Click
Whistles
Clicks
Whistles
Click
Whistles
Whistles, tones
Whistles
Whistles
Click
6-11
3.5-4.5
2-5
Dziedzic 1978
Pryor et al. 1965
Caldwell and Caldwell 1969, Fish and Turl1976
Evans 1973
Busnel and Dziedzic 1966a
65
McLeod 1986
Caldwell et al. 1969
Watkins 1967
-120
7.6-13.4
Au 1993
Leatherwood et al. 1993
6-15 b
Steiner 1981
8-12
Watkins and Schevill1972
0.3-5
to 12
2-20
0.3
to 5
4-12
1.0-27.3
1-16
60-80
6.4-19.2b
1.8,3
1.5-18
6-12
Low
180
Schevill and Watkins 1971
Schevill and Watkins 1971
Caldwell and Caldwell 1971
Evans 1973
Wang Ding et al. 1995
Leatherwood and Walker 1979
Steiner et al. 1979, Ford and Fisher 1983, Morton et al. 1986
Schevill and Watkins 1966
0.25-0.5
2
0.1-35
0.5-25
Watkins et al. 1~77
Watkins et al. 1977
Dawson 1988, Dawson and Thorpe 1990, Au
1993
Caldwell and Caldwell 1968, Moore and Ridg-
Taruski 1979, Steiner 1981
1-18
0.1-> 8'
Watkins and Schevill1980, Dziedzic and de
Buffrenil1989
Dziedzic and de Buffrenil1989
Kamminga and Wiersma 1981, Shochi et al.
1982, Evans et al. 1988, Au 1993
way 1995
Busnel and Dziedzic 1966a
Busnel and Dziedzic 1966a
Whistles
Click
Scream
Click
Pulsed calls
Pseudorca
crassidens
6
116-134
Whistles, chirps,
Barks
Whistles
Click
Click
Growls, Blats
Atlantic white-sided Whistles
dolphin
White-beaked
Squeals
dolphin
Peale's dolphin
Pulses (buzz)
L. obliquidens
Lissodelphis
borealis
Orcinus orca
0.2-5
dolphin
12-25
1-6
180
160
4-9.5
25-30,95-130
220-228
Schevill and Watkins 1966
Diercks et al. 1971, Diercks 1972
Schevill and Watkins 1966, Awbrey et al. 1982,
Ford and Fisher 1983, Moore et al. 1988
Busnel and Dziedzic 1968, Kamminga and van
Velden 1987
Kamminga and van Velden 1987, Thomas and
Turl1990
Table 4-1
continued
Scientific Name
Sotalia flUviatilis
Common Name
Tucuxi
Sousa chinensis
Stenella attenuata
Humpback dolphin
Spotted dolphin
S. clymene
S. coernleoalba
Clymene dolphin
Spinner dolphin
S. longirostris
S. plagiodon
S. styx
Steno bredanensis
Long-snouted
spinner dolphin
Spotted dolphin
Gray's porpOise
Rough-toothed
dolphin
Tursiops trum:atus Bottlenosed
dolphin
Signal Type
Frequency
Range
(kHz)
3.6-23.9
Whistles
Whistles
Whistles
Pulse
Whistles
Whistles
1.2->16
3.1-21.4
6.7-17.8b
to 150
6.3-19.2
1-22.5
6.8-16.9 b
109-125
Wang Ding et al. 1995
Evans 1967
Diercks 1972
Mullin et al. 1994
Watkins and Schevill1974, Steiner 1981, Norris
Wide band
5-60
108-115
et al. 1994, Wang Ding et al. 1995
Watkins and Schevill1974, Norris et al. 1994
1-160
5-60
1-20
8-12
low-65
Brownlee 1983
Watkins and Schevilll974, Norris et al. 1994
1-160
5.0-19.8
1-8
0.1-8
60
6.7-17.9b
Ketten 1984
Caldwell et al. 1973, Steiner 1981
Caldwell and Caldwell 1971b
6->24
8-12.5
4-7
Pulse bursts
Screams
Pulse
Whistle
Click
Click
Whistles
Clicks
Squawks, barks,
growls, chirps
Whistles
Whistles
Click
Whistles
80-100
0.8-24
Monodon
monoceros
Phocoenidae
Neophocaena
phocaenoides
Narwhal
Finless porpOise
High
Wang Ding et al. 1995
Caldwell and Caldwell 1970, Norris et al. 1972,
Kamminga et al. 1993
Schultz and Corkeron 1994
Norris et al. 1994
Brownlee 1983
Caldwell et al. 1973
5-32
3.5-14.5b
Busnel et al. 1968
Busnel and Dziedzic 1966b
125-173
Norris and Evans 1967
Lilly and Miller 1961, Tyack 1985, Caldwell
et al. 1990, Schultz and Corkeron 1994,
Wang Ding et al. 1995
Wood 1953
0.2-150
0.2-16
4-20
Clickd
Beluga
7.1-18.5b
References
(Partial references only for some species)
Whistles
Click
Rasp, grate, mew,
bark, yelp
Click
Bark
Whistle
Monodontidae
Delphinapterns
leucas
Frequency Near
Maximum
Source Level
Energy (kHz)
(dB re 1 flPa)
Diercks et al. 1971, Evans 1973
Evans and Prescott 1962
Caldwell and Caldwell 1967, Evans and Prescott
30-60
110-130
218-228
1962
Au et al. 1974, Au 1993
Whistles
0.26-20
2-5.9
Schevill and Lawrence 1949, Sjare and Smith
Pulsed tones
0.4-12
1-8
1986a,b
Schevill and Lawrence 1949, Sjare and Smith
Noisy
vocalizations
Echolocation
click
Pulsed tones
0.5-16
4.2-8.3
1986a,b
Schevill and Lawrence 1949, Sjare and Smith
Whistles
Click
0.3-18
Clicks
1.6-2.2
Click
40-60, 100-120
206-225
1986a,b
Au et al. 1985, 1987, Au 1993
Ford and Fisher 1978
0.5-5
0.3-10
40
2
128
218
Ford and Fisher 1978
M0hl et al. 1990
Pilleri et al. 1980
Kamminga et al. 1986, Kamminga 1988
Continued on next page
Table 4-1
continued
Scientific Name
Phocoenoides dalli
Phocoena
phocoena
P. sinus
Physeteridae·
Kogia breviceps
Physeter catodon
Platanistoidea
lniidae
Inia geoffiensis
Common Name
Dall's porpoise
Harbor porpoise
Signal Type
Frequency
Range
(kHz)
Clicks
Click
0.04-12
Clicks
2
Pulse
Click
100-160
135-149
Pontoporiidae
Lipotes vexillifer
Pontoporia
blainvillei
Ziphiidae
Hyperoodon
'ampullatus
Hyperoodon spp.
Mesoplodon
carlhubbsi
M. densirostris
110-150
110-150
Pygmy sperm
whale
Sperm whale
Clicks
60-200
120
Clicks
0.1-30
2-4,10-16
Clicks in coda
16-30
Squeals
Whistle
Click
< 1-12
0.2-5.2
25-200
Click
20-120
Clicks
Click
0.8-16
Baiji
Franciscana
Whistles
Click
3-1804
Northern bottlenose whale
Whistles
3-16
Indus susu
Bottlenose whale
Hubb's beaked
whale
Blainville's beaked
whale
Clicks
Click
Pulses
Whistles, chirps
Whistles
135-177
160-180
M0hl and Anderson 1973
Busnel er al. 1965, M0hl and Anderson 1973,
Kamminga and Wiersma 1981, Akamatsu
Backus and Schevilll966, Levenson 1974,
Watkins 1980a,b
Watkins 1980a,b
Caldwell and Caldwell 1970
Wang Ding et al. 1995
Norris et al. 1972
Kamminga et al. 1989
Diercks et al. 1971, Evans 1973, Kamminga
100
95-105
85-105
156
et al. 1993
Xiao andJing 1989
Low
Andersen and Plieri 1970, Plieri et aI. 1971
Herald et al. 1969
156
Jing et al. 1981, Xiao andJing 1989
Busnel et al. 1974
15-100
0.3-24
Winn et al. 1970
Winn et al. 1970
Wmn et al. 1970
Buerki et al. 1989, Lynn and Reiss 1992
0.5-26
0.3-80
Evans 1973, Evans and Awbrey 1984
Evans and Awbrey 1984, Hatakeyama and
Soeda 1990, Hatakeyma et al. 1994
Busnel and Dziedzic 1966a, Schevill et al. 1969
Santoro et al. 1989, Caldwell and Caldwell 1987
1-2
l.8-3.8 b
6
References
(Partial references only for some species)
et al. 1994
Silber 1991
128-139
Click
Bourn
120-148
165-175
100
Vaquita
Click
Platanistidae
Platanista minor
Frequency Near
Maximum
Source Level
Energy (kHz)
(dBre 1 ~Pa)
8-12
0.3-2
Caldwell and Caldwell 1971a
<1-6
Buerki et al. 1989, Lynn and Reiss 1992
2.6-10.7
Mysticeti
Balaenidae
Balaena
mysticetus
Bowhead whale
Calls
0.100-0.580
0.14-0.16
128-190
Tonal moans
0.025-0.900
0.10-0040
128-178
Thompson et al. 1979, Ljungblad et al. 1980,
Norris and Leatherwood 1981, Wiirsigand
Clark 1993
Ljungblad et al. 1982, Cummings and Holliday
1987, Clark et al. 1986
Table 4-1
continued
Frequency
Scientific Name
Balaena
mysticetus
Common Name
Bowhead whale
Signal Type
Pulsive
Frequency Near
Range
Maximum
Source Level
References
(kHz)
Energy (kHz)
(dB re 11lPa)
(Partial references only for some species)
0.025-3.500
Song
0.02-0.50
<4
Tonal
0.03-1.25
0.16-0.50
Pulsive
0.03-2.20
0.05-0.50
152-185
Clark andJohnson 1984, Wiirsig et al. 1985,
158-189
Cummings and Holliday 1987
Ljungblad et al. 1982, Cummings and Holliday
1987, Wiirsig and Clark 1993
Eubalaena
australis
Southern right
whale
Cummings et al. 1972, Clark 1982, 1983
172-187
181-186
E. glacialis
Northern right
Call
< 00400
Moans
< 00400
Cummings et al. 1972, Clark 1982, 1983
Clark (in Wiirsig et al. 1982)
Watkins and Schevill1972, Clark 1990
< 0.200
whale
Watkins and Schevill1972, Thompson et al.
1979, Spero 1981
Neobalaenidae
Caperea
rnarginata
Pygmy right whale
Balaenopteridae
BaLaenoptera
Minke whale
acutorostrata
165-179
Dawbin and Cato 1992
0.06-0.14
151-175
Winn and Perkins 1976, Schevill and Watkins
Down sweeps
0.06-0.13
165
Moans, grunts
0.06-0.14
0.06-0.14
Schevill and Watkins 1972
Schevill and Watkins 1972, Winn and Perkins
Ratchet
. 0.85-6
0.85
0.10-0.20
Thumps in pairs
<0.300
Sweeps, moans
0.060-0.135
1972
151-175
1976
B. borealis
B. edeni
Sei whale
Bryde's whale
Thump trains
0.10-2
Fmsweeps
Moans
1.5-3.5
Pulsed moans
Discrete pulses
0.070-0.245
0.124-0.132
0.10-0.93
0.165-0.900
Winn and Perkins 1976
Winn and Perkins 1976
Thompson et al. 1979, Knowlton et al. 1991
152-174
0.70-0.95
0.700-0.900
B. musculus
Blue whale
Moans
0.012-00400
0.012-0.025
188
B. physalus
Fin whale
Moans
0.016-0.750
0.020
160-190
Pulse
0.040-0.075
Pulse
0.018-0.025
Cummings et al. 1986
Edds et al. 1993
Edds et al. 1993
Cummings and Thompson 1971, 1994, Edds
1982, Stafford et al. 1994
Ragged pulse
Megaptera
novaeangliae
Humpback whale
Clark 1990
Watkins 1981
0.020
Watkins 1981
< 0.030
Rumble
Moans, down-
0.014-0.118
sweeps
Constant call
0.02-0.04
Moans, tones,
0.03-0.75
upsweeps
Rumble
0.01-0.03
Thompson et al. 1979, Edds 1988
< 0.030
0.020
160-186
Watkins 1981
Watkins 1981, Watkins et al. 1987, Edds 1988,
155-165
Edds 1988
Watkins 1981, Cummings et al. 1986, Edds 1988
Cummings and Thompson 1994
Whistles', chirps'
1.5-5
Clicks'
16-28
Songs
0.03-8
Watkins 1981, Edds 1988
Thompson et al. 1979
1.5-2.5
0.1-4
144-186
Thompson et al. 1979
Thompson et al. 1979,Watkins 1981, Edds
1982,1988, Payne et al. 1983, Silber 1986,
Clark 1990
Social
0.05-10
Song
0.03-8
components
Shrieks
Horn blasts
Moans
0.02-1.8
Grunts
0.025-1.9
<3
0.120-4
144-174
Thompson et al. 1979
Thompson et al. 1979, Payne and Payne 1985
Thompson et al. 1986
0.750-1.8
179-181
00410-00420
181-185
Thompson et al. 1986
0.035-0.360
175
Thompson et al. 1986
190
Thompson et al. 1986
Continu.ed on next page
Table 4-1
Scientific Name
Megaptera
novaeangliae
Eschrichtiidae
Eschrictius
robustus
Fissipedia
Mustelidae
Enhydra lutris
continued
Common Name
Humpback whale
Signal Type
Pulse trains
Frequency
Range
(kHz)
0.025-1.25
Frequency Near
Source Level
Maximum
Energy (kHz)
(dB re 1 JlPa)
0.025-0.080
References
(Partial references only for some species)
179-181
Thompson et al. 1986
183-192
Thompson et al. 1986
Slap
0.03-1.2
Call
0.2-2.5
1-1.5
Moans
0.02-1.20
Modulated pulse
0.08-1.8
0.020-0.200,
0.700-1.2
0.225-0.600
FMsweep
0.10-0.35
0.300
1984
Dahlheim et al. 1984, Moore and Ljungblad
Pulses
0.10-2
0.300-0.825
1984
Dahlheim et al. 1984, Moore and Ljungblad
Clicks (calves)
0.10-20
3.4-4
Sea otter
Growls', whine
3-5
Walrus
Bell tone
Gray whale
Dahlheim and Ljungblad 1990
185
Cummings et al. 1968, Fish et al. 1974, Swartz
and Cummings 1978
Dahlheim et al. 1984, Moore and Ljungblad
1984
Fish et al. 19::'4, Norris et al. 1977
Kenyon 1981, Richardson et al. 1995
Pinnipedia
Odobenidae
Odobenus
rosmarus
Clicks, taps,
knocks
Rasps
Grunts
Otariidae
Arctocephalus
philippii
Callorhinus
Clicks
Schevill et al. 1966, Ray and Watkins 1975, Stir-
0.4-1.2
0.1-10
<2
0.2-0.6
0.4-0.6
~1
~L
0.1-0.2
0.1-0.2
ling et al. 1983
Schevill et al. 1966, Ray and Watkins 1975, Stirling et al. 1983
Schevill et al. 1966
Stirling et al. 1983
Norris and Watkins 1971
Juan Fernandez
fur seal
Northern fur seal
Clicks, bleats
Poulter 1968
Northern sea lion
Clicks, growls
Poulter 1968
California sea lion
Barks
ursinus
Eumetopias
jubatus
Zalophus
californianus
Phocidae
Cystophora
cristata
Hooded seal
Whinny
Clicks
<1-3
Buzzing
< 1-4
Bearded seal
Song
Gray seal
Clicks, hiss
6 Calls
Hydrurga
leptonyx
Leopard seal
Knocks
Pulses, trills
Thump, blast
Ultrasonic
<3.5
Schusterman et al. 1967
0.5-4
< 1
Schusterman et al. 1967
Schusterman et al. 1967
Schusterman et al. 1967
Terhune and Ronald 1973
0.2-0.4
Grunt
Snort
Buzz, click
Erignathus
barbatus
Halichoerus
grypus
<8
t06
0.02-6
0.1-1
1.2
1-2
178
0-30,0-40
0.1-5
to 16
0.1-5.9
Asselin et al. 1993
Asselin et al. 1993
Ray 1970, Stirling and Siniff1979, Rogers et al.
0.1-3
To 10
1995
Rogers et al. 1995
0.04-7
up to 164
Terhune and Ronald 1973
Terhune and Ronald 1973
Ray et al. 1969, Stirling et al. 1983, Cummings
et al. 1983
Schevill et al. 1963, Oliver 1978
50-60
Low
Thomas et al. 1983a
Marine Mamma! Sensory Systems
Table 4-1
Scientific Name
Leptonychotes
weddellii
Lobodon
carcinophagus
Ommatophoca
rossii
continued
Common Name
Signal Type
Frequency
Range
(kHz)
Frequency Near
Maximum
Source Level
Energy (kHz)
(dB re 1 llPa)
References
(Partial references only for some species)
Weddell seal
>34 Calls
0.1-12.8
Crabeater sea!
Groan
<0.1-8
Ross seal
Pulses
0.25-1
4-1-4
0.1-7.1
<0.1-16
0.1-3
130-140
Moh! et al. 1975, Watkins and Schevill1979,
Terhune and Ronald 1986, Terhune 1994
30
131-164
0.4-16
<5
95-130
Moh! et al. 1975
Stirling 1973, Cummings et al. 1984
0.5-3.5
8-150
12-40
Phoca fasciata
Ribbon seal
P. groenlandica
Harp sea!
Siren
Frequency
sweeps
15 sounds
P. hispida
Ringed seal
Clicks
Barks, clicks,
P.largha
P. vitulina
Spotted seal
Harbor seal
yelps
Social sounds
Clicks
Roar
Growl, grunt,
Sirenia
Dugongidae
Dugong dugon
131
Dugong
153-193
0.1-1.5
High
Thomas and Kuech!e 1982, Thomas et al.
1983b, Thomas and Stirling 1983
Stirling and Siniff 1979
Watkins and Ray 1985
160
0.4-4
0.4-0.8
< 0.1-0.4
< 0.1-0.25
groan
Creak
0.7-4
0.7-2
Chirp-squeak'
Sound l'
Chirp'
Al!sounds
3-8
1-2
2-4
0.5-18
Watkins and Ray 1985
Watkins and Ray 1977
Beier and Wartzok 1979
Schevill et al. 1963, Cummings and Fish 1971,
Renouf et al. 1980, Noseworthy et al. 1989
Hanggi and Schusterman 1992, 1994
Hanggi and Schusterman 1992, 1994
Hanggi and Schusterman 1992, 1994
Low
1-8
Nair and La! Mohan 1975
Marsh et al. 1978
Marsh et al. 1978
Nishiwaki and Marsh 1985, Anderson and Barclay 1995
Trichechidae
Trichechus
inunguis
T.manatus
Amazonian
manatee
West Indian
manatee
Squeaks, pulses
Squeaks
6-16
6-16
0.6-16
0.6-5
Evans and Herald 1970
Low
Schevill and Watkins 1965
Data compiled from Popper 1980, Watkins and Wartzok 1985, Ketten 1992, Au 1993, Richardson etal. 1995, Ketten 1997.
'Equipment capable of recording to 10 kHz only.
bFrequency determined as '"mean minimum frequency minus 1 sd ... to ... mean maximum frequency plus 1 sd:' (sensu Richatdson et aI. 1995).
cRecorded in air.
dperformance in high background noise (Au 1993)
epew recordings or uncertain verification of sound for species.
ultrasonic signals, odontocetes fall into two acoustic groups:
Type I, with peak spectra (frequencies at maximum energy)
above 100 kHz, and Type II, with peak spectra below 80 kHz
(Ketten 1984, Ketten and Wartzok 1990) (Table 4-1). Type I
echolocators are inshore and riverine dolphins that operate
in acoustically complex waters. Amazonian boutu (Inia
geoffrensis) routinely hunt small fish amid the roots and stems
choking silted "varzea" lakes created by seasonal flooding.
These animals produce Signals up to 200 kHz (Norris et aL
1972). Harbor porpoises typically use 110 to 140 kHz signals
(Kamminga 1988). Communication signals are rare (or are
rarely observed) in most type I species (Watkins and Wartzok 1985); their auditory systems are characterized primarily
by ultra-high frequency adaptations consistent with short
wavelength Signals. Type II species are nearshore and
offshore animals that inhabit low object density environments, travel in large pods, and, acoustically, are concerned
with both communication with conspecifics and detection
of relatively large, distant objects. They may use ultra high
frequency Signals in high background noise, but typically
132
DOUGLAS WARTZOK AND
DARLENE R.
KETTEN
140
-0--
Beluga
..... Klllerwhale
....- Harbor porpoise
___ Balji
_
+
y
Bottlenose dolphin
Bottlenose dolphin
False killer whale
-0- Risso's dolphin
'N""/"
Boutu
20'-\--'--"""""'nTT-.,......,....,...,..n,TTr-.,-,...,-nT1T,---r--r-TTrrrn--.,....,-,
10
100
1,000
10,000
100,000
A
Frequency (Hz)
16
o
Sea lion
o
Sea lion
+
Fur seal
• ..s::r
Cil
0.
::J
... 120
Fur seal
___ Harbor seal
~
III
~
-0- Harbor seal
-
Ringed seal
't:l
- . - Harp seal
J:
III 80
- . - Monk seal
(5
~
J:
I-
40-r---r--r-n,.,..,-.,.,.--r-r-r-TnTTT"-.,.-r-r..,...,-rrrr-"'-"T--r'TTTTTT-""--r-1
1.000
10,000
10
100
100,000
B
Frequency (Hz)
they use lower ultrasonic frequencies with longer wavelengths that are consistent with detecting larger objects over
greater distances and devote more acoustic effort to communication signals than Type I species.
Use of deep ocean stationary arrays has substantially increased our database of mysticete sounds. Recent analyses
suggest that mysticetes have multiple, distinct sound production groups, but habitat and functional relationships for
the potential groupings are not yet clear (Wiirsig and Clark
1993; for review, see Edds-Walton 1997). In general, mysticete vocalizations are Significantly lower in frequency than
those of odontocetes (Table 4-1). Most mysticete signals are
characterized as low frequency moans (0.4-40 sec; funda-
Figure 4-5. Underwater audiograms for
(A) odontocetes and (B) pinnipeds. For some
species, more than one curve is shown because data reported in different studies were
not consistent. Note that for both the bottlenose dolphin and the sea lion, thresholds
are distinctly higher for one ofthe two animals tested. These differences may reflect
different test conditions or a hearing deficit in
one ofthe animals. (Data compiled from
Popper 1980, Fay 1988, Au 1993, Richardson
eta!. 1995.)
mental frequency well below 200 Hz); Simple calls (impulsive, narrow band, peak frequency < 1 kHz); complex calls
(broadband pulsatile AM or FM signals); and complex
"songs" with seasonal variations in phrasing and spectra
(Thompson et al. 1979; Watkins 1981; Edds 1982, 1988;
Payne et al. 1983; Watkins and Wartzok 1985; Silber 1986;
Clark 1990; Dahlheim and Ljungblad 1990). Infrasonic
Signals, typically in the 10- to 16-Hz range, are welldocumented in at least two species, the blue whale (Balaenoptera musculus) (Cummings and Thompson 1971, Edds
1982), and the fin whale (Balaenoptera physalus) (Watkins
1981; Edds 1982, 1988; Watkins et al. 1987). Suggestions that
these low frequency signals are used for long-distance
Marine Mammal Sensory Systems
communication and for topological imaging are intriguing
but have not been definitively demonstrated.
Pinnipeds
The majority of pinniped sounds are in the sonic range (20
Hz - 20 kHz), but their signal characteristics are extremely
diverse (compare Table 4-1 with Fig. 4-5B). Some species are
nearly silent, others have broad ranges and repertoires, and
the form and rate ofproduction vary seasonally, by sex, and
whether the animal is in water or air (Watkins and Wartzok
1985, Richardson et al. 1995). Calls have been described as
grunts, barks, rasps, rattles, growls, creaky doors, and warbles in addition to the more conventional whistles, clicks,
and pulses (Beier and Wartzok 1979, Ralls et al. 1985,
Watkins and Wartzok 1985, Miller and Job 1992). Although
clicks are produced, there is no clear evidence for echolocation in pinnipeds (Renouf et al. 1980, Schusterman 1981,
Wartzok et al. 1984).
Phocid calls are commonly between 100 Hz and 15 kHz,
with peak spectra less than 5 kHz, but can range as high as
40 kHz. Typical source levels in water are estimated to be
near 130dBre IIlPa, butlevels as high as 193 dBre IIlPahave
been reported (Richardson et al. 1995). Infrasonic to seismic
level vibrations are produced by northern elephant seals
(Mirounga angustirostris) while vocalizing in air (Shipley et
al. 1992).
Otariid calls are similarly variable in type, but most are in
the 1 to 4 kHz range. The majority ofsounds that have been
analyzed are associated with social behaviors. Barks in water
have slightly higher peak spectra than in air, although both
center near 1.5 kHz. In-air harmonics that may be important
in communication range up to 6 kHz. Schusterman et al.
(1972), in their investigation of female California sea lion
(Zalophus californianus) signature calls, found important interindividual variations in call structure and showed that the
calls have fundamental range characteristics consistent with
peak in-air hearing sensitivities.
Odobenid sounds are generally in the low sonic range
(fundamentals near 500 Hz; peak < 2 kHz), and are commonly described as bell-like although whistles are also reported (Schevill et al. 1966, Ray and Watkins 1975, Verboom
and Kastelein 1995).
Sirenians
Manatee (Trichechus manatus and T. inunguis) and dugong
(Dugong dugonj underwater sounds have been described as
squeals, whistles, chirps, barks, trills, squeaks, and froglike
calls (Sonoda and Takemura 1973, Anderson and Barclay
1995, Richardson et al. 1995) (Table 4-1). West Indian manatee (Trichechus manatus) calls typically range from 0.6 to 5
133
kHz (Schevill and Watkins 1965). Calls ofAmazonian manatees (Trichechus inunguis), a smaller species than the Florida
manatee (a subspecies ofT. manatus), are slightly higher with
peak spectra near 10 kHz, although distress calls have been
reported to have harmonics up to 35 kHz (Bullock et al.
1980). Dugong calls range from 0.5 to 18 kHz with peak spectra between 1 and 8 kHz (Nishiwaki and Marsh 1985, Anderson and Barclay 1995).
Fissipeds
Descriptions of otter sounds are similar to those for pinnipeds and forterrestrial carnivores (Table 4-1) (Le., growls,
whines, snarls, and chuckles) (Kenyon 1981). Richardson et
al. (1995) state that underwater sound production analyses
are not available but that in-air calls are in the 3- to 5-kHz
range and are relatively intense.
In Vivo Marine Mammal Hearing Data
As indicated in the introductory sections, hearing capacity is
usually expressed as an audiogram, a plot of sensitivity
(threshold level in dB SPL in air and dB re 11lPa in water) versus frequency (Figs. 4-2 and 4-5), which is obtained by behavioral or electrophysiological measures ofhearing.
Mammals typically have a U-shaped hearing curve. Sensitivity decreases on either side of a relatively narrow band of
frequencies at which hearing is significantly more acute. The
rate of decrease in sensitivity is generally steeper above this
best frequency or peak senSitivity region than below. Behavioral and neurophysiological hearing curves are generally
similar, although behavioral audiograms typically have
lower thresholds for peak sensitivities (Dallos et al. 1978). Interindividual and intertrial differences in audiograms may be
related to variety ofsources, including ear health, anesthesia,
masking by other sounds, timing, and anticipation by the
subject.
Hearing curves are available for approximately 12 species
of marine mammals. All have the same basic V-shaped pattern as· land mammal curves (compare Fig. 4-5A,B with Fig.
4-2). As noted earlier, peak sensitivities are generally consistent with the vocalization data in those species for which
both data sets are available (compare Table 4-1 with Fig.
4-5A,B). Detailed reviews of data for specific marine mammal groups are available in Bullock and Gurevich (1979), McCormick et al. (1980), Popper (1980), Schusterrnan (1981),
Watkins and Wartzok (1985), Fay (1988), Awbrey (1990), Au
(1993), and Richardson et al. (1995). Data discussed here for
cetaceans and sirenians are limited to underwater measures.
Most pinnipeds are in effect "amphibious" hearers in that
they operate and presumably use sound in both air and
134
DOUGLAS WARTZOK AND
DARLENE R.
KETTEN
water; therefore, data are included from both media where
available. No published audiometric data are available for
mysticetes, marine otters (Lutra ftlina and Enhydra lutris), or
polar bears (Ursus maritimus).
Cetaceans
Electrophysiological and behavioral audiograms are available for seven odontocete species (Au 1993), most of which
are Type II delphinids with peak sensitivity in the 40- to 80kHz range. Data, generally from one individual, are available
also for beluga whales (Delphinapterus leucas), boutu, and
harbor porpoise. There are no published audiograms for
adult physeterids or ziphiids, or any mysticete. The available
data indicate that odontocetes tend to have at least a 10octave functional hearing range, compared with 8 to 9 octaves in the majority of mammals. Best sensitivities range
from 12 kHz in killer whales (Schevill and Watkins 1966, Hall
andJohnson 1971) to more than 100 kHz in boutu and harbor
porpoise (M0hl and Andersen 1973, Voronov and Stosman
1977, Supin and Popov 1990).
Until recently, most odontocete audiometric work was
directed at understanding echolocation abilities rather than
underwater hearing per se. Therefore, much of what is
known about odontocete hearing is related to ultrasonic
abilities. Acuity measures commonly used in these studies
include operational Signal strength, angular resolution, and
difference limens. The first two are self explanatory. Difference limens (DL) are a measure offrequency discrimination
based on the ability to differentiate between two frequencies or whether a single frequency is modulated. Difference
limens are usually reported simply in terms ofHz or as relative difference limens (rdl) , which are calculated as a percent
equal to 100 times the DL in Hz / frequency. Au (1990) found
that echolocation performance in bottlenose dolphins was 6
to 8 dB poorer than that expected from an optimal receiver.
Target detection thresholds as small as 5 cm at 5 m have
been reported, implying an auditory angular resolution
ability of 0.5°, although most data suggest 1° to 4° for horizontal and vertical resolutions are more common (Bullock
and Gurevich 1979, Popper 1980, Au 1990). Minimal intensity discrimination in bottlenose dolphins (1 dB) is equal to
human values; temporal discrimination("-"8% ofsignal duration) is superior to human abilities. Frequency discrimination in bottlenose dolphins varies from 0.28% to 1.4% rdl for
frequencies between 1 and 140 kHz; best values are found
between 5 and 60 kHz (Popper 1980). These values are similar to those of microchiropteran bats and superior to the
human average (Grinnell 1963, Simmons 1973, Sales and
Pye 1974, Long 1980, Pollack 1980, Popper 1980, Watkins
and Wartzok 1985). Frequency discrimination and angular
resolutions in harbor porpoises (0.1 % to 0.2% rdl; 0.5° to 1°)
are on average better than those for bottlenose dolphins
(Popper 1980).
An important aspect ofany sensory system for survival is
the ability to detect relevant signals amidst background
noise. Critical bands and critical ratios are two measures of
the ability to detect signals embedded in noise. In hearing
studies, the term masking refers to the phenomenon in
which one sound eliminates or degrades the perception of
another (for a detailed discussion, see Yost 1994). To measure
a critical band, a test signal, the target (usually a pure tone),
and a competing Signal, the masker, are presented simultaneously. Fletcher (1940) showed that as the bandwidth ofthe
masker narrows, the target suddenly becomes easier to detect. The critical band (CB) is the bandwidth at that point
expressed as a percent ofthe center frequency. Ifthe ear's frequency resolution is relatively poor, there is a broad skirt of
frequencies around the target tone that can mask it, and the
CB is large. If the ear has relatively good frequency resolution, the CB is relatively narrow. Critical ratios (CR) are a
comparison ofthe signal power required for target detection
versus noise power, and are simply calculated as the threshold level ofthe target in noise (in dB) minus the masker level
(dB). Critical bands tend to be a constant function ofthe CRs
throughout an animal's functional hearing range. Consequently, CR measures with white noise, which are easier to
obtain than CBs, have been used to calculate masking bandwidths based on the assumption that the noise power integrated over the critical band equals the power ofthe target at
its detection threshold, or,
CB (in Hz)
=
lO(CR/lO)
(equation 7)
(Fletcher 1940, Fay 1992). This implies that the target
strength is at least equal to that ofthe noise; however, there
are exceptions. Although uncommon, negative CRs, meaning the Signal is detected at levels below the noise, have been
reported for human detection of speech signals' and for
some bats near their echolocation frequencies (Schuknecht
1993, Kossl and Vater 1995). Critical bands are thought to depend on stiffuess variations in the inner ear. In generalist
ears, the critical bandwidths are relatively constant at about
0.25 to 0.35 octaves/mm ofbasilar membrane (Ketten 1984,
1992; West 1985; Allen and Neeley 1992). Although hearing
ranges vary widely in terms of frequency, most mammals
have a hearing range of 8 to 9 octaves, which- is consistent
with earlier findings that the number of CBs was approximately equal to basilar membrane length in millimeters
(Pickles 1982, Greenwood 1990).
Based on CR and CB data, odontocetes are better than
most mammals at detecting signals in noise. Odontocetes
have more CBs and the CRs are generally smaller than in
humans. Furthermore, odontocete critical bandwidths ap-
Marine Mammal Sensory Systems
proach zero and are not a constant factor ofthe critical ratio
at different frequencies. The bottlenose dolphin has 40 CBs,
which vary from 10 times the CR at 30 kHz to 8 times the CR
at 120 kHz Uohnson 1968, 1971; Moore and Au 1983;
Watkins and Wartzok 1985; Thomasetal. 1988, 1990b). Critical ratios for bottlenose dolphins (20 to 40 dB) are, however,
generally higher than in other odontocetes measured. The
best CRs to date (8 to 40 dB) are for the false killer whale
(Pseudo rca crassidens) (Thomas et al. 1990b), which is also the
species that has performed best in echolocation discrimination tasks (Nachtigall et al. 1996).
Sound localization is an important aspect of hearing in
which the medium has a profound effect. In land mammals,
two cues are important for localizing sound: differences in
arrival time (interaural time) and in sound level (interaural
intensity). Binaural hearing studies are relatively rare for marine mammals, butthe consensus from research on both pinnipeds and odontocetes is that binaural cues are important
for underwater localization (Dudok van Heel 1962, Gentry
1967, Renaud and Popper 1975, Moore et al. 1995); however,
because of sound speed differences, small or absent pinna,
and ear canal adaptations in marine mammals, localization
mechanisms may be somewhat different from those ofland
mammals.
In mammals, the high frequency limit offunctional hearing in each species is correlated with its interaural time distance (IATD the distance sound travels from one ear to the
other divided by the speed ofsound; Heffner and Masterton
1990). The narrower the head, the smaller the IATD, the
higher the frequency an animal must perceive with good sensitivity to detect arrival time through phase differences. For
example, consider a pure tone, which has the form of a sine
wave, arriving at the head. Ifthe sound is directly in front of
the head, the sound will arrive at the same time and with the
same phase at each ear. As the animal's head turns awayftom
the s~)Urce, each ear receives a different phase, given that the
inter-ear distance is different from an even multiple of the
wavelength of the sound. Therefore, IATD cues involve
comparing time of arrival versus phase differences at different frequencies in each ear. Phase cues are useful primarily at
frequencies below the functional limit; however, the higher
the frequency an animal can hear, the more likely it is to have
good sensitivity at the upper end of frequency range for
phase cues.
Clearly, IATDs depend on the sound conduction path in
the animal and the media through which sound travels. For
terrestrial species, the normal sound path is through air,
around the head, pinna to pinna. The key entry point for localization cues is the external auditory meatus, and therefore
the IATD is the intermeatal (1M) distance measured around
the head divided by the speed ofsound in air. In aquatic ani-
=
135
mals, sound can travel in a straight line, by tissue conduction,
through the head given that tissue impedances are similar to
the impedance of seawater. Experiments with delphinids
suggest that intercochlear (IC) or interjaw distances are the
most appropriate measure for calculating IATD values in
odontocetes (Dudok van Heel 1962, Renaud and Popper
1975, Moore et al. 1995). The Ie distances of dolphins are
acoustically equivalent to a rat or bat 1M distance in air because of the increased speed of sound in water. Supin and
Popov (1993) proposed that marine mammals without pinnae were incapable of using IATD cues, given the small interreceptor distances implied by the inner ear as the alternative underwater receptor site. Recently, however, Moore et
al. (1995) demonstrated that the bottlenose dolphin has an
IATD on the order of7llsec, which is better than the average
human value (10 Ilsec) and well below that of most land
mammals tested. IfIM distances are used for land mammals
and otariids in air and IC distances are used for cetaceans and
underwaterphocid data, marine mammal and land mammal
data for IATD versus high frequency limits follow similar
trends.
Intensity differences can be detected monaurally or binaurally, but binaural cues are most important for localizing
high frequencies. In land mammals, intensity discrimination
thresholds (IDT) tend to decrease with increasing sound levels and are generally better in larger animals (Fay 1992,
Heffner and Heffner 1992). Humans and macaques commonly detect intensity differences of0.5 to 2 dB throughout
their functional hearing range; gerbils and chinchillas, 2.5 to
8 dB. Behavioral and evoked potential data show intensity
differences are detectable by odontocetes at levels equal to
those of land mammals and that the detection thresholds,
like those ofland mammals, decline with increasing sound
level. Binaural behavioral studies ,and evoked potential
recordings for bottlenose dolphin indicate an approximate
IDT limit ofl to 2 dB (Bullocket al. 1968, Moore et al. 1995).
In harbor porpoise, IDTs range 0.5 to 3 dB (Popov et al. 1986).
Thresholds in boutu range from 3 to 5 dB (Supin and Popov
1993), but again, because of small sample size and methodological differences, it is unclear whether these numbers represent true species differences. Fay (1992) points out that the
IDT data for land mammals do not fit Weber's Law, which
would predict a flat curve for IDT (Le., intensity discrimination in dB should be nearly constant). Rather, the IDTs
decrease with increasing level and increase slightly with
frequency.
In the past decade, auditory evoked potential (AEP) or
auditory brainstem response (ABR) procedures have been
established for odontocetes (Popov and Supin 1990a, Dolphin 1995). These techniques are highly suitable for studies
with marine mammals for the same reasons they are Widely
136
DOUGLAS WARTZOK AND DARLENE R. KETTEN
used for measuring hearing in infants or debilitated humans-namely, they are rapid, minimally invasive, and require no training or active response by the subject. An
acoustic stimulus is presented by ear or jaw phones and the
evoked neural responses are recorded from surface electrodes' or mini-electrodes inserted under the skin. The signals recorded reflect synchronous discharges oflarge populations ofauditory neurons. The ABRs consist ofa series of5
to 7 peaks or waves that occur within the first 10 msec after
presentation of click or brief tone burst stimuli. Most mammals have similar ABR patterns, bur there are clear speciesspecific differences in both latencies and amplitudes of each
wave Uewett 1970, Dallos et al. 1978, Achor and Starr 1980,
Dolan et al. 1985, Shaw 1990). The delay and pattern ofthe
waves are related to the source ofthe response. For example,
wave I in most mammals is thought to derive from synchronous discharges ofthe auditory nerve; wave II from the auditory nerve or cochlear nucleus. The ABRs from dolphins
show clear species dependence. Typical ABRs from harbor
porpoise and bottlenose dolphin have three positive peaks
with increasing amplitudes, but those in harbor porpoise
have longer latencies (Bullock et al. 1968, Ridgway et al.
r981, Bibikov 1992).
Recent work using continuous amplitude modulated
stimuli (AMS) at low frequencies in bottlenose dolphins and
false killer whales suggest odontocetes can extract envelope
features at higher modulation frequencies than other mammals (Kuwada et al. 1986, Dolphin and Mountain 1992, Dolphin 1995). Supin and Popov (1993) also showed that envelope following responses (EFR) are better measures of low
frequency auditory activity than ABR. The anatomical correlates ofEFRs have not been identified, but the data suggest
auditory central nervous system adaptations in dolphins
may include regions specialized for low as well as high
frequencies.
Pinnipeds
Pinnipeds are particularly interesting because they are faced
with two acoustic environments. Different ways for sensory
information to be received and processed are required for
equivalent air and water hearing in their amphibious lifestyle. One pOSSibility is that pinnipeds have dual systems, operating independently for aquatic and airborne stimuli. If
this is the case, hearing might be expected to be equally acute
but possibly have different frequency ranges related to behaviors in each medium (e.g., feeding in water vs. the location of a pup on land). An alternative to the neffinlike dual
but equal hearing is that pinnipeds are adapted primarily for
one environment and have a "compromised" facility in the
other. Renouf (1992) argued that there is an "a priorijustifi-
cation for expecting otariids and phocids" to operate with
different sensory emphases, given that phocids are more
wholly aquatic. This question cannot be definitively resolved
until more pinniped species have been tested. As with
cetaceans, present data are limited to a few individuals from
mostly smaller species. However, the most recent data suggest there are significant differences among pinnipeds in
both their primary frequency adaptations and in their adaptations to air versus water to warrant more Widespread
species research.
Underwater behavioral audiograms for phocids are
somewhat atypical in that the low frequency tail is relatively
flat compared to other mammalian hearing curves (compare
Figs. 4-2 and 4-5A with Fig. 4-5B; see also Fay 1988 or Yost
1994 for additional comparisons). In the phocids tested (harbor seal [Phoca vitulina], harp seal [Phoca groenlandica], ringed
seal [Phoca hispida], and Hawaiian monk seal [Monachus
schauinslandi]), peak sensitivities ranged between 10 and 30
kHz, with a functional high frequency limit ofabout 60 kHz,
except for the monk seal which had a high frequency limit of
30 kHz (Schusterman 1981, Fay 1988, Thomas et al. 1990a).
Low frequency functional limits are not yet well established
for phocids, and it is likely that some ofthe apparent flatness
will disappear as more animals are tested below 1kHz. However, the fact that all phocid plots have remarkably little decrease in overall sensitivity below peak frequency is notable.
Currently available data from an on-going study comparing
harbor seal and northern elephant seal hearing suggest that
the elephant seal has Significantly better underwater low frequency hearing thresholds than other pinnipeds tested to
date (KastakandSchusterman 1995, 1996).
In-air audiograms for phocids have more conventional
shapes with peak sensitivities at slightly lower frequencies (3
to 10 kHz) (Fay 1988; Kastak and Schusterman 1995, 1996).
In-air evoked potential data on these species are consistent
with behavioral results (Bullock et al. 1971, Dallos et al.
1978). In-air and underwater audiograms cannot be compared directly; however, when the data are converted to intensity measures, the thresholds for airborne sounds are
poorer, on average (Richardson et al. 1995), implying that
phocids are primarily adapted for underwater hearing.
Underwater audiograms and aerial audiograms are available for two species of otariids. Underwater hearing curves
for California sea lions and northern fur seals (Callorhinus
ursinus) have standard mammalian shapes. Functional underwater high frequency hearing limits for both species are
between 35 and 40 kHz with peak sensitivities from 15 to 30
kHz (Fay 1988, Richardson et al. 1995). As with phocids,
otariid peak sensitivities in air are shifted to lower frequencies « 10 kHz; functional limit near 25 kHz), but there is rel-
Marine Mammal Sensory Systems
atively little difference in the overall in-air versus underwater
audiogram shape compared with phocids. The fact that the
otariid aerial and underwater audiograms are relatively similar suggests that otariids may have developed parallel,
equipotent hearing strategies for air and water or even, in the
case of the California sea lion, have"opted" evolutionarily
for a slight edge in air.
In frequency discrimination and localization tasks, pinnipeds perform less well than odontocetes. Angular resolution ranges from 1.5° to 9°, with most animals performing in
the 4° to 6° range (M0hI1964, Bullocketal. 1971, Moore and
Au 1975). There is wide individual variability and no consistent trend for aerial versus aquatic stimuli. Minimal intensity
discrimination (3 dB) by California sea lions is poorer than
that ofdolphins or humans (Moore and Schusterman 1976);
typical frequency discrimination limens for several phocids
and the sea lion (1 % to 2% rdl) (M0hI1967; Schusterman and
Moore 1978a,b; Schusterman 1981) are similar to some of
the bottlenose dolphin data but are on average Significantly
larger (less sensitive) than those for harbor porpOise.
Critical ratio data are available for only three pinnipeds
(Richardson et al. 1995). In the northern fur seal, underwater
critical ratios measured over a fairly narrow range (2 to 30
kHz) were on a par with those ofmost odontocetes at those
frequencies (18 to 35 dB). Critical ratios for one harbor seal in
air and in water were generally similar but also had anomalously higher values for some data pOints. Data reported for
the ringed seal were conSistently 10 dB or more greater than
those of the other two species, that is, significantly poorer
than those of fur seals, harbor seals, or most odontocetes.
Turnbull and Terhune (1993) concluded that eqUivalent performances in air and water can be explained by having an external reception system (ear canal and middle ear) in which
both Signal and noise levels produce parallel impedance
shifts. However, this implies an identical filter response in air
and water, which means either identical processing or parallel but equally efficient paths in the two domains. That is, the
ear canal and middle ear transfer functions remain constant
regardless of the medium. Given the usual assumptions
about the mechanisms underlying CRs, however, the results
could also be attributed to a common inner ear response in
both media.
Like odontocetes, pinnipeds in water have small acoustic
inter-ear distances. It is not known whether they have specialized mechanisms for maintaining the external canal as
the sound reception point underwater or iftissue conduction
is used. M0hl and Ronald (1975), using cochlear microphonics, determined that in-air reception in the harp seal is
through the external canal, but they also found that underwater, the most sensitive region was located below the mea-
137
tus in a region paralleling the canal. Pinnae allow monaural
cues to be used; therefore, eared species may use two different strategies for localizing in air and in water.
Sirenians
Very few audiometric data are available for sirenians, the
other obligate aquatic group. Published data for the West Indian manatee consist of one evoked potential study and preliminary reports from on-goingwork on manatee behavioral
audiogram (Patton and Gerstein 1992, Gerstein et al. 1993,
Gerstein 1994). Several evoked potential studies ofAmazon
manatee have been published (Bullock et al. 1980, Klishin
et al. 1990, Popov and Supin 1990a), but no behavioral data.
No audiometric data are available for dugongs.
Current behavioral data for the West Indian manatee indicate a hearing range ofapproximately 0.1 to 40 kHz, with
best sensitivities near 16 kHz. Functional hearing limits
within this range are not yet established. This octave distribiltion (7 to 8 octaves) is narrower than that of bottlenose
dolphins (10.5 octaves: 0.15 to 160 kHz; Au 1993) and phocid
seals (8 to 9 octaves: 0.08 to 40 kHz; Kastak and Schusterman
1995, 1996) that have been tested over a wide range offrequencies. Bestthresholds for manatees (50 to 55 dB re 11lPa)
are similar to in-water thresholds for several pinnipeds (45 to
55 dB re 1 IlPa), but are significantly higher than those for
odontocetes tested in similar conditions (30 to 40 dB re 1
IlPa). An interesting feature of the manatee audiogram is
that it is remarkably flat (Le., there is less than a 15-dB overall
difference in thresholds between 5 and 20 kHz). In terms of
level and shape, therefore the West Indian manatee audiogram more closely resembles the "essentially flat" audiograms ofphocids noted by Richardson et al. (1995) than it
does the sharply tuned curve typical ofodontocetes. Bullock
et al. (1982), using evoked potential techniques to measure
West Indian manatee hearing, found a maximal upper frequency limit (35 kHz), which is similar to the behavioral results but a markedly different peak sensitivity (1.5 kHz).
They also reported a sharp decline in response levels above
8kHz.
Popov and Supin (1990a) found peak responses in evoked
potential studies ofthe Amazon manatee between 5 and 10
kHz with thresholds of 60 to 90 dB re 1 IlPa. Klishin et al.
(1990) reported best sensitivities to underwater stimuli in the
West Indian manatee to be between 7 and 12 kHz, based on
auditory brainstem responses from awake animals.
Fissipeds
No conventional audiometric data are available for sea otters. Behavioral measures of hearing in air for two North
American river otters (Lutracanadensis) (Gunn 1988) indicate
138
DOUGLAS WARTZOK AND DARLENE R. KETTEN
a functional hearing range in air ofapproximately 0.45 to 35
kHz with peak sensitivity at 16 kHz, which is consistent with
Spector's (1956) more general description of their hearing.
Noise Trauma
One area that is relatively unexplored audiometrically is marine mammal susceptibility to hearing loss. Particularly
when data are obtained from one animal, it is important to
consider whether that hearing curve is representative of the
normal ear for that species. Age and/or exposure to noise
can Significantly alter hearing in mammals. Hearing losses
are recoverable (TTS, temporary threshold shift) or permanent (PTS) according to the extent ofinner ear damage (for
reviews, see Lipscomb 1978, Lehnhardt 1986, Richardson et
al. 1991). Damage location and severity are correlated with
the power spectrum ofthe Signal in relation to the sensitivity
of the animal. For narrow-band, high frequency Signals,
losses typically occur in or near the Signal band, but intensity
and duration can act synergistically to broaden the loss.
Long or repeated exposures to TTS level stimuli without adequate recovery periods can induce permanent threshold
shifts. In general, ifthe duration ofintense noise is short and
the noise is narrow and not impulsive, hearing is recoverable
and the loss is near the signal's peak frequency. Ifexposure is
long, or ifthe signal is broadband with a sudden onset, some
hearing, particularly in the higher frequencies, can be permanently lost.
In humans, PTS results most often from protracted, repeat intense exposures (e.g., occupational auditory hazards
from background noise) or sudden onset of intense sounds
(e.g., rapid, repeated gun fire). Acoustic trauma induced by
sudden onset, loud noise (a 'blast" of sound) is not synonymous with blast trauma, nor are noise and blast effects ofthe
same magnitude. Blast injuries generally result from a Single
exposure to an explosive shock wave that has a compressive
phase with a few microseconds initial rise time to a massive
pressure increase over ambient followed by a rarefactive wave
in which pressure drops well below ambient. Blast damage
may be reparable or permanent according to the severity of
the single blast exposure. Hearing loss with aging (presbycusis), in contrast, is the accumulation ofPTS and TTS insults
to the ear. Typically, high frequencies are lost first with the
loss gradually spreading to lower frequencies over time.
In experiments, multihour exposures to narrow band
noise are used to induce PTS. Most mammals incur losses
when the signal is 80 dB over the animal's threshold. Temporary threshold shift has been produced in humans for frequencies between 0.7 and 5.6 kHz (our most sensitive range)
from underwater sound sources when received levels were
150 to 180 dB re 1 IlPa (Smith and Wojtowicz 1985, Smith et
al. 1988). Taking into account differences in measurements
of sound pressure in air versus water (equations 4 and 5),
these underwater levels are consistent with the 80- to 90-dB
exposure levels that induce TTS in humans at similar frequencies in air. Sharp rise-time Signals produce broad spectrum PTS at lower intensities than slow onset Signals both in
air and in water (Lipscomb 1978, Lehnhardt 1986).
Currently, there are insufficient data to determine accurately TTS and PTS exposure guidelines for any marine
mammal. Although there is the pOSSibility that dive-related
adaptations ameliorate acoustic trauma, recent studies show
losses in marine mammals consistent with age-related hearing changes (Ketten et al. 1992, 1995). Significant differences
in the hearing thresholds oftwo California sea lions reported
by Kastak and Schusterman (1995) are consistent with agerelated hearing differences between the animals. In odontocetes, postmortem examinations of ears from older bottlenose dolphins with known hearing losses found neural
degeneration patterns similar to those of older humans,
which are consistent with a progressive, profound high frequency loss (Ketten et al. 1995).
It is likely that all marine mammals can be impacted by
sound at some combination of frequency and intensity, but
those parameters will vary considerably by species. In terms
ofresearch, the pOSSibility of a hearing loss from both natural and anthropogenic acoustic impacts should be considered in the interpretation ofthe data for any animal for which
there is little orno history. The possibility ofhearingloss over
time needs to be tested with long-term studies and should be
considered in interpreting data from older animals. Finally,
as we expand our use ofocean technolOgies that have direct
and indirect sonic effects, we must be aware oftheir potential
to produce acoustic impacts in ranges important for aquatic
species.
Ears
All marine mammals have special adaptations ofthe external
(Closure, wall thickening, wax plugs) and middle ear (thickened middle ear mucosa, broad eustachian tubes) consistent
with deep, rapid diving and long-term submersion, but they
retain an air-filled middle ear and have the same basic inner
ear configuration as terrestrial species. Each group has distinct adaptations that correlate with both their hearing capacities and with their relative level of adaptation to water.
Cetaceans
EXT ERN ALE AR. Pinnae are absent, although vestigial
pinnal rings occur in some individuals. External auditory
canals are present in cetaceans, but it is debatable whether
they are functional. In odontocetes, the external canal is ex-
Marine Mammal Sensory Systems
ceptionally narrow and plugged with cellular debris and
dense, waxy cerumen. The canal has no observable attachment to the tympanic membrane or the middle ear. In mysticetes, the canal is narrow along most of its length, but the
proximal end flares, cloaking the "glove finger," a complex,
thickened membrane capped by a waxy mound in adults
(Reysenbach de Haan 1956). Reysenbach de Haan (1956) and
Dudok van Heel (1962) were among the first researchers to
suggest soft tissue paths as an alternative to conventional external canal sound conduction in odontocetes. Reysenbach
de Haan (1956) reasoned that because the transmission characteristics ofblubber and seawater are similar, using a canal
occluded with multiple substances would be less efficient
than conduction through body fat, fluid, or bone. Dudokvan
Heel (1962) found the minimum audible angle in bottlenose
dolphin was more consistent with an interbullar critical interaural distance than with intermeatal distances, and concluded the canal was irrelevant. A passive resonator system
involving the teeth of the lower jaw has been suggested for
delphinids (Goodson and Klinowska 1990), but this cannot
be considered a general explanation because it cannot account for echolocation by relatively toothless species (e.g.,
the Monodontidae [narwhals and belugas] and Ziphiidae
[beaked whales]). Currently, the lower j aw is considered the
primary reception path for ultrasonic Signals in odontocetes.
Norris (1968, 1980) observed that the odontocete lower jaw
has two exceptional properties: a fatty core and a thin, ovoid
"pan bone" area in the posterior third of the mandible. Norris (1969) speculated this mandibular fat channel acts as a
preferential low impedance path to the middle ear and the
pan bone as an acoustic window to the middle ear region
(Fig. 4-6).
Several forms ofdata support this hypothesis. The fats in
the mandible are wax esters with acoustic impedances close
to seawater (Varanasi and Malins 1971). Evoked responses
139
and cochlear potentials in spotted and bottlenose dolphins
were significantly greater for sound stimuli above 20 kHz
from transducers placed on or near the mandible (Bullock
et al. 1968, McCormick et al. 1970). Measurements with implanted hydrophones in severed bottlenose dolphin heads
found best transmission characteristics for sources directed
into the pan bone (Norris and Harvey 1974). Brill et al. (1988)
found that encasing the lower jaw in neoprene significantly
impaired performance in echolocation tasks. Some results
disagreed, notably those by Popov and Supin (1990b) and
Bullock et al. (1968), who found best thresholds for low to
sonic frequencies near the external meatus. However, recent
computerized tomographic and magnetic resonance imaging of dolphins revealed a second channel of similar fats lateral to the pan bone (Ketten 1994), which may explain the
discrepancy in the data as the lateral fatty lobes are near
the meatus in delphinids. No discrete soft tissue channels to
the ear have as yet been identified in mysticetes.
TYMPAN 0 PERr oTr ceo MP L EX. The temporal bones
of cetaceans are distinctive in both form and construction.
The inner ear is housed in the periotic, which is fused at one
or more points to the tympanic, or middle ear bone. This
"tympanoperiotic" bullar complex is located outside the
skull in a peribullar cavity formed evolutionarily by eliminating the small, pneumatized, mastoid spaces common in
terrestrial animals. The periotic and tympanic are bordered
laterally and ventrally by the mandible and hyoids. The extracranial position ofthe tympanic and periotic is important
because it increases the acoustic separation ofthe middle and
inner ears, as discussed earlier in the section on localization
and interaural distances.
Tympanic and periotic volumes are highly correlated
with animal size (Ketten and Wartzok 1990). Mysticete bullae are two to three times larger than those of most odontoFigure 4-6.
Sound paths in the dolphin head.
(See also Pabst, Rommel, and McLellan, Chapter 2, this volume.) Outgoing ultrasonic signals
(E) are generated in the vestibular (vs) and
tubular (ts) nasal sac diverticulae and reflected
offthe cranium and prema.xillary sac (ps)
's E s
(Norris 1980, Au 1993). Incident sounds (I)
from anterior targets enter the lowerjaw where
lipids act as preferential low-impedance
acoustic conduits to the ear (Varanasi and
Malins 1971, Norris 1980). Lateral, trumpeciike
fatty lobes (lateral channel) with densities equal
to those in the jaw overlie the pan bone and may
act as additional input channels for signals from
the rear or side ofcile animal. (Ketten 1994;
figure ©Ketten 1992, revised 1997.)
140
DOUGLAS WARTZOK AND DARLENE
R.
KETTEN
cetes. Mysticete tympanics are nearly twice the volume of
the periotics. In odontocetes, periotic and tympanic volumes
are nearly equal. The periotic is ovoid, massive, and thickwalled in all cetaceans. The odontocete tympanic is thinwalled and conical, tapering anteriorly. Mysticete tympanics
are thick-walled and spherical. This means mysticetes have
larger middle ear cavities with relatively low frequency resonance characteristics compared to smaller, higher resonance
odontocete middle ear cavities. The fine strucmre of the
tympanoperiotic and the solidity ofthe tympanoperiotic suture differ among species, but no specific auditory effect has
been determined for these differences (Kasuya 1973, Ketten
1984, Ketten and Wartzok 1990).
Odontocete tympanoperiotics are suspended in a spongy
mucosa, the peribullar plexus, by five or more sets of ligaments. This mucosal cushion and the lack of bony connections to the skull isolate the ear from bony sound conduction
and hold the tympanic loosely in line with the mandibular
fatty channels and pan bone. Because peribullar sinuses are
most extensive in riverine, ultra-high frequency species; like
the boutu, and are poorly developed in pelagic mysticetes,
Oelschlager (1986) suggested that the peribullar plexus and
expanded sinuses are primarily echolocation-related adaptations, functioning as acoustical isolators for the ear, and were
not driven evolutionarily by diVing.
In mysticetes, extensive bony flanges wedge the periotic
against the skull. The tight coupling of these flanges to the
skull suggests both bony and soft tissue sound conduction to
the ear occur in baleen whales.
MID D LEE A R.
Ossicles of odontocetes and mysticetes
are large and dense, and vary widely in size, stiffuess, and
shape (Reysenbach de Haan 1956, Belkovich and Solntseva
1970, Solntseva 1971, Fleischer 1978). In odontocetes, a bony
ridge, the processus gracilis, fuses the malleus to the wall of
the tympanic and the interossicular joints are stiffened with
ligaments and a membranous sheath. Mysticete ossicles are
equally massive but have none ofthe high frequency-related
specializations ofodontocetes. The ossicles are not fused to
the bulla and the stapes is fully mobile with a conventional
fibrous annular ligament. Furthermore, as noted earlier,
the tympanic bone scales with animal size and is on average
double the volume of the periotic. Therefore, the mysticete
middle ear cavity is substantially larger than that of any
odontocete and, in combination with their massive ossicles
that are loosely joined, forms a characteristically low frequencyear.
The middle ear cavity in both odontocetes and mysticetes
is lined with a thick, vascularized fibrous sheet, the corpus
cavernosum. Computerized tomography (CT) and magnetic resonance imaging (MRI) data suggest the intratym-
panic space is air-filled in vivo (Ketten 1994). Ifso, a potential
acoustic difficulty for a diving mammal is that changing middle ear volumes may alter the resonance characteristics of
the middle ear, and, in mrn alter hearing sensitivity. Studies
are underway with free-swimming beluga whales (S. Ridgway, pers. comm.) to test whether hearing thresholds change
with depth. In light of the extensive innervation of the
middle ear corpus cavernosum by the trigeminal nerve, one
novel task proposed for the trigeminal in cetaceans has been
to regulate middle ear volume (Ketten 1992), which could
also explain exceptionally large trigeminal fiber numbers in
both odontocetes and mysticetes (Jansen and Jansen 1969,
Morgane andJacobs 1972).
There is no clear consensus on how cetacean middle ears
function. Both conventional ossicular motion and translational bone conduction have been proposed for cetaceans
(McCormick et al. 1970, 1980; Lipatov and Solntseva 1972;
Fleischer 1978). On the basis of experiments with anesthetized bottlenose dolphin and a Pacific white-sided dolphin (Lagenorhynchus obliquidens) McCormick et al. (1970,
1980) concluded that sound entering from the mandible by
bone conduction produces a "relative motion" between the
stapes and the cochlear capsule. In their procedure, immobilizing the ossicular chain decreased cochlear potentials, but
disrupting the external canal and tympanum had no effect.
Fleischer (1978) suggested the procedure introduced an artificial conduction pathway. From anatomical studies, he concluded sound from any path is traI1slated through tympanic
vibration to the ossicles, which conventionally pulse the oval
window. McCormick's theory assumes fixed or fused tympanoperiotic joints; Fleischer's requires a mobile stapes,
distensible round window, and flexible tympanoperiotic
symphyses. Both conclusions may have been confounded by
experimental constraints: McCormick'et al. (1970) had to
disrupt the middle ear cavity to expose the ossicles, and Fleischer's data were subject to postmortem and preservation artifacts. In addition, neither theory is completely compatible
with the wide structural variability of cetacean middle ears.
The question of middle ear mechanisms in cetaceans therefore remains open.
INN ERE A R.
The cetacean periotic houses the membranous labyrinth of the inner ear, which is further subdivided
into auditory and vestibular components.
In all cetaceans, the vestibular system is substantially
smaller in volume than the cochlea and may be vestigial
(Boenninghaus 1903, Gray 1951, Ketten 1992, Gao andZhou
1995). Although size is not a criterion for vestibular function,
cetaceans are unique in having semicircular canals that are
significantly smaller than the cochlear canal (Gray 1951,
Jansen and Jansen 1969). Innervation is proportionately re-
141
Manne Mammal Sensory Systems
Table 4-2.
Auditory, Vestibular, and Optic Nerve Distributions
Species
Inia geoffrensis
Lipotes vexillifer
Neophocaena
phocaenoides
Sousa chinensis
Phocoena
phocoena
Delphinapterus
leucas
Delphinus delphis
Lagenorhynchus
obliquidens
Stenella attenuata
Tursiops trulUatus
Physeter catodon
Balaenoptera
physalus
Megaptera
novaeangliae
Rhinolophus
ferrumequinum
Pteronotu5 pamellii
Cavia porcellus
Felis domesticus
Homo sapiens
Common
Name
Cochlear
Type
Bourn
Baiji
Finless porpoise
Membrane
Length
(mm)
Auditory
Ganglion
Cells
Density
(cells/mm
cochlea)
38.2
104,832
2744
Humpbacked
dolphin
Harbor porpoise
22.5
Beluga
42
Common dolphin
White-sided
dolphin
Spotted dolphin
Bottlenosed
dolphin
Sperm whale
Fin whale
Vestibular
Ganglion
Cells
Vestibular
Auditory
Ratio
Optic
Nerve
Fibers
Optic
Auditory
Ratio
Optic
Vestibular
Ratio
15,500
0.15
82,512
3,605
0.04
23,800
0.29
6.60
68,198
3,455
0.05
88,900
1.30
25.73
70,226
3,213
0.05
149,800
2.13
46.62
81,700
1.16
25.53
110,500
0.74
165,600
1.97
77,500
1.11
162,700
1.68
70,137
3117
149,386
3557
II
34.9
84,175
2412
II
34.9
70,000
2006
II
36.9
82,506
2236
II
38.9
96,716
2486
3,200
4,091
3,489
0.05
0.04
40.48
46.63
54.3
161,878
2981
172,000
1.06
M
64.7
134,098
2073
252,000
1.88
Humpback whale
M
58
156,374
2696
347,000
2.22
Horseshoe bat
T
16.1
15,953
991/1750'
Mustached bat
T
T
T
T
14.0
12,800
900/1900'
19.0
24,011
1264
8,231
0.34
28.0
51,755
1848
12,376
0.24
193,000
3.73
15.59
32.1
30,500
950
15,590
0.51
1,159,000
38.00
74.34
Guinea pig
Cat
Human
Data compiled from Yamada 1953; Gacek and Rasmussen 1961;Jansen and Jansen 1969; Firbas 1972; Morgane and Jacobs 1972; Bruns and Schmieszek 1980; Dawson 1980;
Kenen 1984, 1992; Vater 1988a,b; Nadoll988; Gao and Zhou 1991, 1992, 1995; Kessl and Vater 1995.
'Densities at auditory fovea as described by Bruns and Schmiezek (1980).
duced as well (Table 4-2); on average less than 5% of the
cetacean VllIth nerve is devoted to vestibular fibers (Fig.
4-4), as compared to approximately 40% in other mammals
(Ketten 1997). No equivalent reduction ofthe vestibular system is known in any land mammal. A pOSSible explanation is
that fusion ofthe cervical vertebrae in cetaceans resulted in
limited head movements, which resulted in fewer inputs to
the vestibular system that led to a reduction of related
vestibular receptors. This does not mean that cetaceans do
not receive acceleration and gravity cues but rather that the
neural 'budget" for these cues is less. In land mammals, similar vestibular reductions have been approximated only by
experimentation, disease, congenital absence ofcanals, or, in
some extreme cases, through surgery as a cure for vertigo
(GraybieI1964).
All cetacean cochleae have three scalae or chambers like
other mammals (Figs. 4-4 and 4-7): scala media (also called
the cochlear duct), scala tympani, and scala vestibuli. The
scalae are parallel flUid-filled tubes. Scala vestibuli ends at the
oval window; scala tympani, at the round window; and scala
media, which contains the organ ofCorti, is a blind pouch between them. Detailed descriptions of odontocete cochlear
ducts are available in Wever et al. (1971a,b,c, 1972), Ketten
(1984,1992,1997), Kettenand Wartzok(1990), andSolntseva
(1971, 1990). We briefly summarize histological observations and discuss in detail only the cochlear features thatinfluence hearing ranges and senSitivity.
Odontocete cochleae differ significantly from other
mammalian cochleae by having hypertrophied cochlear
duct structures, extremely dense ganglion cell distributions,
and unique basilar membrane dimensions. Wever et al.
(1971a,b,c, 1972) found all cellular elements ofthe organ of
Corti in Tursiops and Lagenorhynchus were larger and denser
than in other mammals. More recent studies reported hypertrophy of the inner ear in phocoenids and monodontids as
well (Ketten 1984, Ketten and Wartzok 1990, Solntseva
1990). Most ofthe hypercellularityis associated with the support cells of the basilar membrane and with the stria vascu-
142
DOUGLAS
WARTZOK
AND
DARLENE R.
KETTEN
periotic
bone
apical turn
B
A
spiral
ligament
" inner
bony lamina basilar
aUditory
membrane
fibers
spiral
ganglion cells
outer
bony lamina
c
o
Figure 4·7. (A) A schematic ofa typical dolphin cochlea is shown in cross-section with a corresponding photomicrograph (B) from a
25-!.Lm histologic section ofa Phocoena ear. (C) A schematic ofthe major features ofthe cochlear duct in the high-frequency basal region that
are equivalent to the magnified view (D) ofa 25-!.Lm section ofa Atlantic white-sided dolphin inner ear.
laris, which plays a major role in cochlear metabolism. Mysticete ears are less well-endowed cellularly, but this may be a
reflection ofpreservation artifacts that are more common in
baleen specimens because ofgreater difficulties in their collection and generally longer postmortem times before they
are preserved.
The fiber and ganglion cell counts for the auditory nerve
are exceptional in all cetaceans (Table 4-2). Auditory ganglion cell totals are more than double those ofhumans in all
species, but, more important, the innervation densities (neurons/mm basilar membrane) are two- to threefold greater
than in other mammals. Comparisons of the ratios of auditory, vestibular, and optic nerve fibers in cetaceans versus
representative land mammals (Table 4-2) underscore the hypertrophy of the cetacean auditory nerve. The vestibular to
auditory ratios are approximately 1/10 those ofland mammals. Optic to auditory ratios in Type II odontocetes and
mysticetes are apprOximately half those ofmost land mam-
mals (noting an exception for the exceptionally high human
optic value), whereas those of Type I riverine odontocetes
are an order ofmagnitude less.
Auditory ganglion cell densities in Type I odontocetes are
particularly notable, averaging more than 3000 cells/mm.
Using a mammalian average of 100 inner hair cells/mm
(Kiang, pers. comm.) and four rows ofouter hair cells / inner
hair cell, these data imply a ganglion to hair cell ratio of
nearly 6: 1 for Type I species. In humans, the ratio is 2.4: 1; in
cats (Felis domesticus), 3:1; and in bats, the average is 4:1 (Firbas 1972, Bruns and Schrnieszek 1980, Vater 1988b). Because
90% to 95% of all afferent spiral ganglion cells innervate inner hair cells, the average ganglion cell to inner hair cell ratio
is 24: 1 for cetaceans, or more than twice the average ratio in
bats and three times that of humans. Wever et a1. (1971c)
speculated that additional innervation is required primarily
in the basal region to relay greater detail about ultrasonic signals to the central nervous system in echolocation analyses.
Marine Mammal Sensory Systems
Electrophysiological results are consistent with this speculation. The central nervous system recordings in both porpoises and bats imply increased ganglion cells correspond to
multiple response sets that are parallel processed at the centrallevel. Bullocket al. (1968) found three distinct categories
ofresponse units in the inferior colliculus of dolphin brains,
that is, those that were signal duration specific, those that responded to changes in signal rise time, and those that were
specialized to short latencies with no frequency specificity.
This division ofsignal properties among populations ofneurons is consistent with, although not identical to, observations in bats ofmultiple categories offacilitation and analysis
neurons (Schnitzler 1983, Suga 1983). The odontocete inner
ear neural distribution data imply that equally extensive
analyses of signal characteristics are performed by odontocete auditory systems as well. However, although high afferent ratios in odontocetes could be related to the complexity
ofinformation extracted from echolocation Signals, this theory does not explain similar densities in mysticetes. The sim-
Table 4-3.
143
ilarity of odontocete and mysticete innervations suggests
that mysticetes may have equally complex processing but
possibly for infra- rather than ultrasonic tasks.
CETACEAN
INNER
EAR
STRUCTURE-HEARING
COR RE L ATE S. The cetacean basilar membrane is a
highly differentiated strucrure with substantial variations in
length, thickness (T), and width (W) (Table 4-3, Fig. 4-8).
Basilar membrane lengths in Cetacea, like those ofterrestrial
mammals, scale isomorphically with body size. In Cetacea,
cochlear length is correlated strongly with animal size (0.8 <
r < 0.95), but there is no Significant correlation for length and
frequency (Ketten 1992). Thickness and width, however, are
strongly correlated with hearing capacity (Ketten 1984, Ketten and Wartzok 1990). In most odontocetes, basilar membrane width is 30 !lm at the base and increases to 300 to
500 !lm apically. Basal widths of odontocetes are similar to
those of bats and one third that of humans (Firbas 1972,
Schuknecht and Gulya 1986). In odontocetes thicknesses
Cochlear Morphometry in Whales versus Land Mammals
Species
Inia geoffrensis
Phocoena phocoena
Grampus griseus
LagenorhJlUhus
albirostris
Stenella attenuata
Tursiops truncatus
Physeter catodon
Balaenoptera
acutorostrata
Balaena mysticetus
Balaenoptera physalus
Euba1aena glacialis
Rhinolophus
ferrumequinum
Pteronotus pamellii
Spalax ehrenbergi
Cavia porcellus
Felis domesticus
Homo sapiens
Common
Name
Boum
Harbor
porpOise
Risso's dolphin
White-beaked
dolphin
Spotted
dolphin
Bottlenosed
dclphin
Sperm whale
Minke
Bowhead
Fin whale
Right whale
Horseshoe bat
Mustached bat
Mole rat
Guinea pig
Cat
Human
Cochlear
Type
Turns
Membrane
Length (mm)
1.5
38.2
1.5
22.5
Outer
Lamina
(mm)
17.6
Base
Thickness
(!lm)
Base
Width
(!lm)
Apex
Thickness
(!lm)
Apex
Width
(!lm)
Basal Apical
T:W T:W
Ratio Ratio
25
30
5
290
0.83
0.017
II
2.5
41.0
20
40
5
420
0.50
0.012
II
2.5
34.8
8.5
20
40
5
360
0.50
0.014
II
2.5
36.9
8.4
20
40
5
400
0.50
0.013
II
2.25
38.9
10.3
25
35
380
0.71
0.013
1.75
54.3
M
2.25
50.6
100
1500
M
M
M
2.25
56.5
0.06
0.001
2.5
64.7
2.5
54.1
7
125
1400
0.06
0.002
.IE
2.25
16.1
35
80
2
150
0.44
0.013
.IE
2.75
14.0
22
50
2
110
0.44
0.018
Sb
T
T
T
3.5
13.7
4.25
18.5
3
28.0
2.5
33.0
< lOb
7.5
120
2.5
<8b
2.5
120
7.4
12
1670
2200
100
200
70
2
250
0.11
0.008
80
5
370
0.15
0.014
120
550
Data compiled from Wever et aI. 1971a, b: Firbas 1972: Bruns and Schmieszek 1980: Norris and Leatherwood 1981: Ketten 1984. 1992, 1994: West 1985: Vater 1988a,b: Nadol
1988: Echteler et al. 1994: Kossl and Vater 1995.
aOuter osseous lamina length unknown.
bLaminar remnant present but not in contact with basilar membrane.
Width (W) = pars arcuara and pectinata: Thickness (T) = pars pecrinata maximum.
J
=aquatic> 100 kHz: II =aquatic < 90 kHz: M =aquatic < 2 kHz: 1£ =:eolian> 20 kHz: Sb =subterranean; T =terrestrial.
144
DOUGLAS
WARTZOK AND
DARLENE
R.
KETTEN
ODONTOCETE
MYSTICETE
1 mm
osl
P. phocoena . Type I
m
m
T. truncatus . Type II
E. glacialis . Type M
Figure 4-8. Three-dimensional schematics summarize basilar membrane dimensions and support element differences among Type 1,
Type II odomocete, and Type M mysticete inner ears in cetaceans. The cochlea are inverted from in vivo orientations. The schematics are
drawn to the same scale for the three species illustrated (see Table 4-3). (g) spiral ganglion; (isl) inner bony spiral lamina; (m) basilarmembrane; (osl) outer bony spiral lamina; (P) posterior; M (medial); (V) ventral.
typically range from 25 11m at the base to 5 11m at the apex
(Table 4-3). Therefore, a typical cross-section of an odomocete basilar membrane is square at the base becoming rectangular apically. Mysticete membranes are thin rectangles
throughout, varying in thickness between 7 11m at the base
to 2 11m at the apex. Width gradients in mysticetes can be as
great as in odontocetes with membranes in some species
ranging from 100 11m at the base (similar to the base in humans) to 1600 11m at the apex. The apical widths in mysticetes are three times that of human, three to five times
those of most odontocetes, and 1.2 times that of elephams,
which are known to perceive infrasonics (Payne et al. 1986).
Comparing bat, odontocete, and mysticete basilar membrane thickness to width (T:W) ratios is a good exercise in
structure-function relationships. T:W ratios are consistent
with the maximal high and low frequencies each species
hears and with differences in their peak spectra (Ketten and
Wartzok 1990; Ketten 1992, 1997). Echolocators have significantly higher basal ratios than mysticetes, and odontocete ratios are higher than for bats in the basal regions where their ultrasonic echolocation Signals are encoded. For example,
Phocoena, a Type I odontocete, has a basal T:W ratio of 0.9 and
a peak frequency of 130 kHz. Tursiops, a Type II odontocete,
has a T:W ratio of 0.7 and a peak signal of 70 kHz, and Rhinolophus, a bat, a 0.3 T:W ratio and a 40 kHz echolocation signal. All three have terminal apical ratios near 0.01. Mysticete
T:W ratios range from 0.1 at the base to approximately 0.001
at the apex, that is, the mysticete basal ratios are equivalent to
rnidapical ratios in the three echolocators and decrease
steadily to a value one-tenth that ofodomocetes at the apex.
The exceptionally low apical ratio in mysticeti is consistent
with a broad, flaccid membrane that can encode infrasonics.
Marine Mammal Sensory Systems
A striking feature of odontocete basilar membranes is
their association with extensive outer bony laminae. In
mammals, ossified outer spiral laminae are hallmarks of ultrasonic ears (Yamada 1953, Reysenbach de Haan 1956, Sales
and Pye 1974, Ketten 1984). Thick outer bony laminae (Fig.
4-7C) are present throughout the basal turn in all odontocetes, and the proportional extent of outer laminae is functionally correlated with odontocete ultrasonic frequency
ranges (Ketten and Wartzok 1990). In the basal, high frequency region of the cochlea, odontocete basilar membranes resemble thick girders, stiffened by attachments at
both margins to a rigid bony shelf. In Type I echolocators
with peak frequencies above 100 kHz an outer lamina is present for 60% ofthe cochlear duct (Fig. 4-8). Type II echolocators with lower peak frequencies have a bony anchor for
about 30% of the duct. Therefore, the Type I basilar membrane is coupled tightly to a stiffledge for twice as much ofits
length as a Type II membrane. If Type I and II membranes
have similar thickness:width ratios, a Type I cochlea with
longer outer laminae would have greater membrane stiffness andhigher resonant frequencies than an equivalent position in a Type II membrane without bony support. Both
membrane ratios and the extent or proportion of auxiliary
bony membrane supp'ort are important mechanistic keys to
how odontocetes achieve ultrasonic hearing despite ear size.
Both inner and outer laminae are present in mysticete
cochleae but they are morphologically and functionally very
different from those of odontocetes. Mysticete outer laminae are narrow spicules located on !=he outer edge ofthe spiralligament. They do not attach to the basilar membrane.
The broad, thin mysticete basilar membrane attaches only to
a flexible spiral ligament. It is likely that the spikelike outer
lamina in mysticetes is a remnant of an ancestral condition
rather than a functional acoustic structUre and that low basilar membrane ratios and large organ of Corti mass are the
principal structural determinants of mysticete hearing
ranges. To date, few mysticete species have been analyzed
for very low frequency sensitivity, but the inner and middle
ear anatomy argues strongly that they are low to infrasonic
specialists.
Pinnipeds
Pinniped ears are less derived than
cetacean ears. The external pinnae are reduced or absent.
Ear canal diameter and closure mechanisms vary widely in
pinnipeds, and the exact role ofthe canal in submerged hearing has not clearly been determined. Otariids have essentially terrestrial, broad-bore external canals with moderate
to distinctive pinnae. Phocids, particularly northern elephant seals, spend more time in water than otariids and have
only a vestigial cartilaginous meatal ring, no pinnae, andnarEXT ERN ALE A R .
145
row ear canals (D. R. Ketten and R. J. Schusterman, unpub!.).
Although the phocids have no external pinnae, it is not yet
known which species normally have air-filled versus partially
to fully blocked external canals. No specialized soft tissue
sound paths for underwater hearing have been clearly
demonstrated in seals.
An obvious amphibious adaptation in phocid ears is that
the external canal is well-developed and has a ring ofvoluntary muscle that can close the meatus (M0hl1967, Repenning 1972). It has been suggested that seal middle ears are capable ofoperating entirely liquid filled (Repenning 1972) and
that various soft tissue attachments to the ossicles are related
to the operation ofa liquid-filled middle ear or for enhancing
high frequency sensitivity in water (Ramprashad et a!. 1972,
Renouf 1992), but neither of these suggestions is consistent
with the level ofdevelopment ofthe external canal or the size
and development ofthe eustachian rube. Whether the external canal remains patent and air filled, collapses, or becomes
flooded during dives remains a heavily debated subject. The
ear canal contains a corpus cavernosum (cavernous epithelium) analogous to that in the middle ear, which may close
the canal and regulate air pressure~ dUring dives (M0hl1968,
Repenning 1972). There are strong theoretical arguments for
each .position. Flooding the canal would provide a low impedance channel to the tympanic membrane, but then
directing sound input to only one window ofthe cochlea becomes a problem. Ifthe middle ear is fluid filled, the oval and
round windows can receive simultaneous stimulation that
would interfere with normal basilar membrane response.
However, ifthe canal remains air filled, it poses the problem
of an impedance mismatch that could make the canal less
efficient for sound conduction to the middle and inner ear
than surrounding soft tissues when the animal is submerged.
To date, there is no clear evidence for speCialized soft tissues,
like those found in odontocetes, and no direct measures of
the shape ofthe ear canal when submerged.
The position and attachment to the skull ofthe tympanic
and periotic bones in pinnipeds is not significantly different
from that ofland mammals. The middle ear space is encased
in a tympanic bulla, a bulbous bony chamber with one softwalled opening, the tympanic membrane. The tympanicbulla
is fused to the periotic. Both have partially or fully ossified articulations with the skull. These connections are less rigid than
those in some land mammals, but the ears are not as clearly detached (and acoustically isolated) as those ofcetaceans.
MID D LEE A R.
Pinniped middle ears have a moderate
layer ofcavernous tissue, but it is less developed than that of
cetaceans (M0hl1968, Ramprashad et al. 1972, Repenning
1972, Fleischer 1978). Pinniped ossicular chains are diverse.
Those in otariids resemble terrestrial carnivores; ossides of
146
DOUGLAS WAR TZOK AND DARLENE R. KETTEN
phocids are more massive but with wide species variation in
shape (Doran 1879, Fleischer 1978), which suggests a wider
range of peak frequencies and more emphasis on lower
frequency reception than in otariids. Although some researchers indicate phocids have small eardrums (Repenning
1972), the size is not Significantly different from that ofequivalent mass land mammals. The oval and round window areas
in terrestrial mammals are ofapproximately the same size. In
pinnipeds, the oval window can be one-halfto one-third the
size of the round window. Eardrum to oval window ratios
have been cited frequently as a factor in middle ear gain, but
this association is still being debated (Rosowski 1994), and
depending on the exact size distributions among these three
membranes in each pinniped species, there could be wide
differences in middle ear amplification among pinnipeds.
INNER EAR. Relatively few pinniped inner ears have
been investigated and published data that are available are
largely descriptive (Ramprashad et al. 1972, Solntseva 1990).
Most pinnipeds have inner ears that resemble terrestrial
high frequency generalists (i.e., multiple turn spirals with
partial laminar support). Preliminary data on larger species
suggest they may have some low frequency adaptations consistent with their size. There is no indication of extensive
adaptation for either high ultrasonic or infrasonic hearing.
Pinnipeds have one feature in common with cetaceans-a
large cochlear aqueduct. M0hl (1968) suggested that this
would facilitate bone conduction, but the mechanism is not
clear, nor is it consistent with equally large aqueducts in
odontocetes.
Sirenians
Anatomical studies of sirenian ears are largely descriptive
and most work has been done only on manatees (Robineau
1969, Fleischer 1978, Ketten et al. 1992). Like Cetacea, they
have no pinnae. Also, the tympanoperiotics are constructed
of exceptionally dense bone, but like pinnipeds (and unlike
odontocetes), sirenian ear complexes are partly fused to the
inner wall ofthe cranium. Neonate ears vary less than 20% in
shape and size from adult specimens; consequently, the ear
complex is disproportionately large. In young manatees it
can constitute 14% ofskeletal weight (Domning and de BuffrenilI991).
EXT ERN ALE AR. Exact sound reception paths are not
known in sirenians. The unusual anatomy ofthe zygomatic
arch in manatees, combined with its relation to the squamosal and periotic have made the zygomatic a frequent candidate for a sirenian analogue to the odontocete fat channels.
The periotic is tied by a syndesmotic (mixed fibrous tissue
and bone) joint to the squamosal, which is fused, in turn,
to the zygomatic process, a highly convoluted cartilaginous
labyrinth filled with lipids. The zygomatic is, in effect, an inflated, oil-filled, bony sponge that has substantial mass but
less stiffuess than an equivalent process of compact bone
(Domning and Hayek 1986, Ketten et al. 1992). In the Amazonian manatee, the best thresholds in evoked potential
recordings were obtained from probes overlying this region
(Bullock et al. 1980, Klishin et al. 1990), but no clear acoustic
function has been demonstrated.
MID DLE EA R. The middle ear system ofsirenians is large
and mass dominated but the extreme denSity of the ossicles
adds stiffuess (Fleischer 1978, Ketten et al. 1992). The middle
ear cavity ofmanatees, as in other marine mammals, is lined
with a thick., vascularized fibrous sheet. The ossicles are
looselyjoined and the stapes is columnar, a shape that is common in reptiles but rare in mammals and pOSSibly unique
to manatees. The manatee tympanic membrane is everted
and supported by a distinctive keel on the malleus. Deeply
bowed, everted tympanic membranes, epitomized by the
fibrous "glove finger" in mysticetes, are common in marine
mammals but are relatively rare in nonaquatic species. Like
the eardrum of cats, the manatee tympanic membrane has
two distinct regions, implying that membrane response patterns are frequency dependent (Pickles 1982). The tympanic-to-oval window ratio is approximately 15:1in the West
Indian manatee, which places it midway between that ofhumans and elephants (Ketten et al. 1992, Rosowski 1994).
Chorda tympani, a branch of the facial nerve (cranial nerve
VII) that traverses the middle ear cavity, is relatively large in
manatees. It is crosses the middle ear but has no known auditory function. In humans, chorda tympani constitutes approximately 10% ofthe facial nerve. It conveys taste from the
anterior two-thirds of the tongue and carries parasympathetic pregangliOniC fibers to the salivary glands. In the West
Indian manatee, chorda tympani forms 30% of the facial
nerve bundle.
INN ERE AR. The sirenian inner ear is a mixture of
aquatic and land mammal features. Anatomically, T. manatus
inner ears are relatively unspecialized. The cochlea has none
ofthe obvious features related to ultra- or infrasonic hearing
found in cetacean ears. Basilar membrane structure and neural distributions are closer to those ofpinnipeds or some land
mammals than to those ofcetaceans (Ketten et al. 1992). The
outer osseous spiral lamina is small or absent, and the basilar
membrane has a small base-to-apex gradient. At the thickest
basal point, the membrane is approximately 150 llm wide
and 7 llm thick; apically it is 600 llm by 5 llm. Therefore, the
manatee has a relatively small basilar membrane gradient
compared to cetaceans, which is consistent with the audio-
Marine Mammal Sensory Systems
metric profile and 7-octave hearing range recently reported
for the West Indian manatee (Gerstein et al. 1993). Spiral
ganglion cell densities (500 /mm) are low compared to those
ofodontocetes, but auditory ganglion cell sizes (20!J.m x 10
!J.m) are larger than those ofmany land mammals.
The intracranial position of the periotic has important
implications for sound localization abilities in manatees. Depending on the sound channels used, the manatee IATD
could range from a minimum of 58 !J.sec (intercochlear distances) to a maximum of 258 !J.sec (external intermeatal
path). If manatees fit the conventional mammalian IATD
frequency regression, the potential IATDs imply that the
West Indian manatee should have an upper frequency limit
ofat least 50 kHz, similar to that ofa smaller odontocete. To
date, there is no indication that any species of manatee has
acute ultrasonic hearing (Schevill and Watkins 1965; Bullock
et al. 1980, 1982; Klishin et al. 1990; Popov and Supin 1990a).
Intensity differences from head shadow could provide some
directional cues, but the available anatomical data (Ketten et
al. 1992) suggest that manatees may have difficulty using
phase cues for sound localization and have poorer localization ability than other marine mammals.
Localization ability is of particular interest in Florida
manatees because ofthe number injured annually from collisions with boats in shallow coastal waters and canals. Since
manatee salvage programs began throughout Florida in
1971, more than 2400 dead manatees have been recovered
(D. Odell, pers. comm.). Human activities may account, directly or indirectly, for one-third to one-half of all deaths
during the past 15 years. Even more important, deaths from
collisions doubled in the past decade. In 1991, more than 30%
of all deaths were associated with boats (Ketten et al. 1992).
Although the sound spectra for most outboard motors are
well within what we believe to be the hearing range of
Florida manatees, the ability to determine a boat's direction
depends on the ability to localize engine noise. Therefore,
the collision hazard could be related more to localization
abilities than to hearing range or sensitivity per se.
Is the conclusion that sirenians have less localization ability than cetaceans tenable? Did environmental pressures that
.influenced the evolution of sirenia differ in some important
way from those of their terrestrial counterparts and from
other marine mammals that are consistent with proposed
differences in hearing? The tympanoperiotic complexes
of extinct Sirenia are remarkably similar to those of modern West Indian manatee. The structural commonalities
between fossil and modern manatee ears imply that few
functional changes have occurred in the sirenian auditory
periphery since the Eocene. Sirenians first appear in the fossil record in the early Eocene and were already adapted to at
least a partially aquatic lifestyle by the early to middle
147
Eocene (Barnes et al. 1985). Their closest affinities are with
proboscideans and tethytheres, and, like cetaceans, they
arose from unknown ungulate stock. A radiation in the late
Eocene led to modern dugongids and trichechids. The West
Indian manatee is a docile, slow grazer that lives in fresh or
estuarine environments. The Florida manatee averages 400
kg and 3 m, but can exceed 4 m in length (Ridgway 1972,
Odell et al. 1981). They cruise at an average speed of3 km/hr
and seldom attain speeds more than 20 km/hr even when
alarmed (Reynolds 1981). For most mammals, sounds related to predators, mates, and food sources are important
selection pressures. With the exception of Steller's sea cow
(Hydrodamalis gigas), sirenians have been tropical animals,
feeding on marine angiosperms or ~ea grasses, since the
Eocene (Domning 1977, 1981; Eva 1980; Domning et al.
1982). Trichechids therefore developed in a relatively stable
environment with few predators, and it is unlikely they use
sound to detect food. If acoustic cues carried little or no survival advantage, acoustic developments in ancestral species
may have been lost. The limited data on manatees are intriguing because ofthe diverSity ofthe results. Relatively little is known about masking or localization in any sirenian,
and we have no direct data for the dugong. Given their size
and salt water habitat, it is likely that dugongs evolved somewhat different sensory abilities from trichechids.
If hearing is not highly evolved in manatees, are there
other candidates for a premier sensory system? A highly developed chemosensory apparatus would be useful for a shallow water herbivore, and the dimensions ofchorda tympani
hint that gustation could be an important sense in sirenians.
On the other hand, peripheral targets for chorda tympani
in manatees have not been determined, and innervation
patterns in marine mammals do not always match those of
terrestrial species. Exceptional vibrissal discrimination has
been demonstrated for pinnipeds (Dehnhardt 1990, 1994;
Kastelein 1991) and suggests similar investigations with sirenians would be worthwhile.
Fissipeds and Ursids
These groups are linked by a lack ofdata. Remarkably little is
known about sea otter hearing even in comparison to the
sirenians, and data on polar bear hearing or ear adaptations
appear to be nonexistent.
The sea otter has a well-defined external ear flap and a
canal that is open atthe surface. Kenyon (1981) indicated that
the pinnal flange folds downward on dives, which suggests
that the canal is at least passively closed during dives, but
there are no data on whether speCialized valves are associated with the ear canal like those found in pinnipeds. Otter
auditory bullae are attached to the skull and resemble those
of pinnipeds. CT scans of sea otters (D. R. Ketten, unpub!.)
148
DOUGLAS WAR TZOK AND DARLENE R.
KETTEN
show that their middle and inner ears are grossly configured
like ears of similarly sized terrestrial carnivores, with the
same orientation and 2.5 turn distribution. Spector (1956)
and Gunn (1988) both indicated an upper frequency limit of
35 kHz for common river otters, which have similar ear
anatomy.
It is reasonable to assume that in-air hearing is welldeveloped in polar bears but there are no published audiograms for air or underwater hearing. Considering their size,
polar bears should have moderately good low frequency
hearing, but because they are also aquatic, they may have
evolved high frequency ear adaptations in parallel with other
marine mammals. Anatomically, polar bear ears are interesting because even casual observations show that polar bears
have a well-developed, moderately stiffpinnal flange resembling those of other ursids; however, because they dive in
cold waters, it is likely polar bears have special mechanisms
for preserving the integrity of the ear canal and middle ear.
Hearing in this group clearly warrants further research, particularly because they represent an unknown level of auditory adaptation for underwater hearing.
or prey in an environment that filters and attenuates light
very differently than does air. After detection ofan object, an
animal needs to form a sufficiently clear image ofthe object
to determine what action to take: ignore, flee, capture, etc.
Because there are fewer studies ofvision than of audition in
marine mammals, and because many of the known adaptations are similar, cetaceans and pinnipeds will be considered
together in the following discussion. We begin with a consideration oflight in water.
Light in the Ocean
As light passes through the water column, it is absorbed, refracted, and scattered. These effects are different depending
on the wavelength of the light, the concentration of chlorophyll in the water, and the concentration and type of dissolved organic matter. Based on the differences in transmission of light in different waters, Jerlov (1976) proposed a
classification scheme (Fig. 4~9) that shows the wavelength
dependence for the transmission oflight in different types of
oceanic waters. In more coastal waters, light oflonger wavelength is transmitted better, whereas in the open ocean,
shorter wavelength blue light is transmitted best.
In general, the photon flux density, or downward irradiance, of the light falls off as an exponential function of the
depth,
Vision
The characteristics ofmarine mammalvision can be divided
into two major functional categories: visual detection and visual acuity. The first relates to adaptations that maximize the
opportunity for marine mammals to detect either predators
(equation 8)
100
••...•..
80
·····\\.... 4
ctl
E
.•.
ctl
::l
~
60
o
~
CD
.0
E
:::J
Z
40
~
~
Ci5
a::
20
o
400
500
Wavelength in nm
Figure 4-9. Relative spectral distribution of
sunlight remaining in different marine waters, after the number ofquanta at the respective maxima is reduced to 20% to 25% ofthe
maximum number incident at the surface
(wavelength = 600 nm). Curves rescaled to
100 for comparison. Curve 1 represents the
spectral distribution ofquanta in the clearest
oceanic water at 70 m depth; curve 2, average
oceanic water at 22 m; curve 3, clearest
coastal water at 12 m; curve 4, average
coastal water at 5 m; and curve 5, average
inshore water at 3 m. (Reprinted from Munz
1965 ©Little Brown and Company.)
Marine Mammal Sensory Systems
where Id is the downward irradiance at depth d, Is is the irradiance at the surface, and k is the attenuation coefficient.
Light of a wavelength around 475 nm penetrates the best
through clear oceanic waters (Fig. 4-9, curve 1). For light of
this wavelength in typical oceanic waters Uerlov type IB,
]erlov 1976), kis approximately 0.033 and the irradiance falls
by 90% for approximately every 70 m ofdepth. In bright daylight, the surface irradiance for photons of 475 nm wavelength is about 1.6 x 10'4/cm2 1sec or 0.67 W 1m2 (McFarland
andMunz 1975).
Visual Detection
With the rapid attenuation oflight with depth, how deep can
marine mammals·use vision to detect predators or prey? Lavigne and Ronald (1972) found that the minimum light level
needed for a dark-adapted harp seal to distinguish between
light and dark was 1.35 X 10-9 W 1m2 at light of a wavelength
of 475 nm. The bright day surface irradiance decreases to 10-9
W 1m2 at approximately 615 m. Hence, this is the likely depth
limit for visual detection in this species. Wartzok (1979) reported a somewhat greater depth value for spotted seals
(Phoca largha) (670 m). The irradiance ofthe night sky with a
full moon is about six orders of magnitude less than that of
bright sunlight. Hence, on a bright moonlight night, irradiance decreases to 10-9 W 1m2 at about zoo m. Thus, the seal
that could detect light at 615 m during the day would have to
move about 415 m closer to the surface to do equally well on
a moonlit night. We do not know the minimum light level actually required to detect prey because the experiments only
measured the limits oflight detectability. Light levels for prey
detection are likely somewhat greater than these minimum
levels. Assuming they are 100 times greater, or 10-7 W 1m2 ,
B
A~
."... :',..: ........
0
'.
.
. .
-1
'-
..........
,,
"
(.)
c::
III
'6
'.
............
~
....
........
Cl
..Q
'"
-2
. ."
...::';. .
.
=
.j"
.:s..
........ '.-......:
...... :. D'
:.
.
o
(A) Diagram ofdistribution of
radiance found in the sea. For a given point,
0, the distribution in three dimensions is
given by the surface formed by revolving the
dotted line S around the axis uo. The relative
radiance in a given direction is the length of
the line in that direction joining the pOint 0
to a point on the surface S. (B) The log radiance oflight is plotted against <p, the angle
between a given direction and the downward
vertical axis. The log radiance for <p 0 has
been made equal to zero. (Solid line) Lake
Pend Oreilie (after Tyler 1960); (dashed line)
ftom an equation given by Tyler (see Denton
et al. 1985); (dotted line) for oceanic Mediterranean waters (after Lundgren 1976, cited by
Jerlov 1976). (Reprinted from Denton 1990
©Cambridge University Press.)
Figure 4-10.
........
(I)
the comparative depths for prey detection under sunlight
and moonlight become 476 and 61 m, respectively. The difference in depths remains 415 m because the ratio of intensities in equation 6 at functional depth in sunlight and
functional depth in moonlight remains constant.
So far we have been considering only the downwelling
light, that is, light that would be sensed by a detector looking
straight up. For predator or prey detection, the light coming
at other angles is equally important. Figure 4-10 shows the
relative intensity oflight at other angles. Regardless ofwater
type, the light scattered backtoward the surface is only about
1/100 that ofthe light downwelling. This gives an indication
of the Significant advantage a predator has when approaching another animal from below. A predator looking up sees
the prey as a shadow blocking light that is about two orders
of magnitude more intense than the light against which the
prey can detect a predator below. Typical countershading of
animals minimizes this difference in light intenSity. A dark
dorsal surface helps the animal reflect no more light toward
the surface than upwells naturally from the open ocean at
that depth. A pale ventral surface helps camouflage an animal against the brighter light downwelling from above, although the difference in downwelling and upwelling light is
so great that an animal which is not bioluminescent cannot
match the intensity ofthe downwelling light and will always
appear as a darker object against a lighter background. Many
marine predators, such as seals and sea lions (Hobson 1966),
typically attack prey from below for this reason.
To maximize the detection ofprey at depth, a predator attacking from below should adopt several sensory strategies,
including matching receptor pigment sensitivity to downwelling light, increasing denSity of photoreceptors, and enhancing photon capture by an elaborated tapetum. All of
,.,
'. '-
4> (degrees)
90
149
180
150
DOUGLAS WARTZOK AND DARLENE R. KETTEN
these strategies will be discussed. The photoreceptors
should have their greatest visual sensitivity at the same wavelength as the light that is best transmitted through the type of
ocean waters in which they typically feed (Munz 1965). For
both pinnipeds (Lavigne and Ronald 1975b) and cetaceans
(McFarland 1971), pigments in the rod receptors (the retinal
receptors specializing in low lightlevel sensitivity) ofspecies
that feed in the open ocean have a maximum sensitivity at
the blue end of the spectrum, matching the wavelengths of
light that best penetrate in the open ocean.
Detection of a visual signal depends on the number of
photons captured. Marine mammals maximize their visual
sensitivity by having a high density ofphotoreceptors and a
well-developed tapetum. The California sea lion has receptor densities of 200,000 to 260,000 per mm 2 (Landau and
Dawson 1970) and the bottlenose dolphin has 400,000 per
mm 2 (DralI977), compared to 120,000 to 160,000 in humans
(0sterberg 1935) and 800,000 in a nocturnal fish, the Iota
(Walls 1942).
The tapetum, a reflective layer behind the retina, reflects
the photons that were not absorbed by the visual pigment as
the light initially passed through the visual receptor layer.
.This reflection gives the visual pigment a second chance to
capture a photon and thus increases the probability ofdetection. Marine mammals have the most developed tapeta of
any mammal (Walls 1942, Dawson 1980). The tapeta are
thicker, up to 35 layers in the gray seal (Halichoerus grypus)
(Braekevelt 1986), and back the entire fundus (Nagy and
Ronald 1970, Dawson et al. 1972, Braekevelt 1986). Even at
the periphery ofthe tapetum, the average number ofcell layers, 15 to 20, is as many as at the center ofthe tapetum in terrestrial nocturnal predators such as the cat (Pedler 1963).
Dawson et al. (1987a) noted that the tapetum ofa Risso's dolphin (Grampus griseus) (a pelagic species) reflected more blue
light than that of a bottlenose dolphin (a coastal species).
This difference is consistent with the sensitivity hypotheSiS
for detection, but Dawson et a1. (1987a) cautioned against
building too much of a case on the basis of one Risso's dolphin specimen. All 11 bottlenose dolphins observed were
very similar to each other in spectral light reflected by the
tapetum.
In shallower depths, down to approximately 100 m in the
open ocean, the downwelling light still has a relatively broad
range ofwavelengths. In this depth range, a predator can use
a second method to detect prey, the contrast method (Lythgoe 1968). For contrast detection, the pigment in the eye
needs to have its best sensitivity offset somewhat from the
wavelength that best penetrates the ocean. To understand
why we need to remember that the wavelength-dependent
absorption as light passes through oceanic water will be the
same for all light paths. This means that in the first 100 m of
the ocean, downwelling light has a range of wavelengths
consistent with a 1OO-m path but an animal looking horizontally would see light that had passed through thousands of
meters of ocean, and thus would see light restricted to the
narrow band ofwavelengths that are best transmitted. A silvery-sided fish that reflected the horizontal light perfectly
would be invisible to a predator looking horizontally. However, ifthe fish also reflected some ofthe downwelling light,
it would be reflectinglight ofa different spectrum containing
longer wavelengths than the horizontal light a predator
would see on all sides ofthe fish. Ifthe predator had a visual
pigment with greater sensitivity to longer wavelengths of
light, then the difference in the light spectrum reflected from
the fish and the general horizontal background light would
be detected easily. There are several lines of evidence (discussed below) that show some marine mammals have more
than one type of photopigment, and thus can make use of
both sensitivity (when attacking prey from below) and contrast (when attacking prey from the side).
The vertebrate photoreceptors that function best at low
light levels are the rod photoreceptors. Rod pigments are
most accurately measured when they are extracted from a
dark-adapted eye preserved immediately after the death of
the animal. Such ideal conditions cannot be met for most
marine mammals, so the values for extracted pigments are
less accurate than for most terrestrial mammals. In addition,
many ofthe measurements are based on only a single specimen. Given these caveats, the current data show a basic correlation between what we know about the diving habits of
some cetacean species and the peak sensitivity of the photopigment in their rods. The deep-diving Baird's beaked
whale (Berardius bairdii) has a pigment maximum at 481 nm,
whereas the gray whale (Eschrichtius robustus) (a coastal
species) has a pigment maximum at 497 nm (McFarland
1971). Recall that shorter wavelengths are transmitted best
and reach greater depths. The humpback whale (Megaptera
novaeangliae), with a typical diving depth intermediate betWeen the beaked whale and the gray whale, has a pigment
maximum at 492 nm (DarmellI962). The Weddell seal (Leptonychotes weddelli) has a pigment maximum at 495 to 496
nm, similar to coastal fishes and terrestrial mammals, but the
deep diving southern elephant seal (Mirounga leonina) (Slip et
a1. 1994) has a pigment maximum at 485 to 486 nm (Lythgoe
and Dartnall 1970). The elephant seal pigment maximum
could be the result of a shift either to the wavelengths best
penetrating the depths, or to wavelengths emitted by bioluminescent prey (Young and Mencher 1980). Absorption
curves from these whales and seals suggest that there is only
one pigment. However, most ofthese studies are old and did
not use sensitive tests presently available. The nocturnal
New World owl monkey (Aotus trivirgatus) and nocturnal
Marine Mammal Sensory Systems
prosimian bush-baby (Galaga garnetti) used to be considered
species with all rod retinas (Walls 1942), but modern monoclonal antibody techniques have identifieq cones in the retinas ofboth species (Wilder and Rakic 1990).
A variety ofanatomical and behavioral evidence suggests
that odontocetes, phocids, otariids, and sirenians have more
than one photopigment. Anatomically, both rods and cones
have been described in the retinas of bottlenose dolphins
(Perez et al. 1972, Dawson and Perez 1973), Dall's porpoise
(Phacaenaides dalli) (Murayama et al. 1992), harbor porpoise
(Kastelein et al. 1990), sperm whales (Physetermacracephalus)
(Mann 1946), fin whales (Mann 1946), minke whales (Balaenoptera acutarostrata) (Murayama et al. 1992), harbor seals
Uamieson and Fisher 1971), harp seals (Nagy and Ronald
1975), and West Indian manatees (Cohen et al. 1982). Behavioral studies of critical flicker fusion frequency (the fastest
flicker rates that can be detected as a flicker rather than as
continuous light), indicate that the faster responding cone
systems exist in harp seals (Bernholtz and Mathews 1975)
and bottlenose dolphins (van Esch and de Wolf 1979). Lavigne and Ronald's (1975a) reanalysis ofvisual acuity studies in
California sea lions conducted by Schusterman and Balliet
(1971) and Schusterman (1972) indicate the presence ofboth
rod and cone visual systems. Finally, the demonstration of
color discrimination in spotted seals (Wartzok and McCormick 1978) also indicates the presence ofmore than one
visual pigment. The difficulty with which color discrimination was demonstrated in spotted seals (Wartzok and McCormick 1978) and the inability to demonstrate it in bottlenose dolphins (Simons and Huigen 1977, Madsen and
Herman 1980) suggest that these marine mammals are using
their dual pigment systems primarily for brightness detection and discrimination and did not evolve them mainly for
color vision.
Multiple pigment visual systems in marine mammals
probably serve three functions: (1) to maximize sensitivity
when at depth and approaching prey from below; (2) to maximize contrast when at shallower depths and approaching
prey from the side; and (3) to allow vision in up to nine orders
ofmagnitude ofchanges in light intensity. A rod system sensitive to the lowest levels oflight at depth would be bleached
out by the much higher intensities at or near the surface. The
combination of a rod system for vision at depth and a cone
system for vision near the surface, and on land in the case of
pinnipeds, allows marine mammals to function visually at almost all light levels and depths. One open question is what
adaptations have been made in the rod pigment to allow it to
regenerate quickly enough to reach maximum sensitivity as
the marine mammal dives to depth. Diving marine mammals often descend at rates of greater than 1 m/sec (Kooyman and Gentry 1986, Martin etal.1993, Watkinsetal. 1993,
151
Asaga et al. 1994), which translates into decreases in light intensity ofabout one order ofmagnitude, or one log unit, per
min. Initial dark adaptation has only been measured in humans (Hecht and Hsia 1945) where it occurs at a rate ofabout
0.5 log/min. Clearly the biochemical processes of rod pigment regeneration need to be modified in marine mammals
if they are to use the full potential sensitivity of their visual
system. Levenson and Schusterman (1998) presented preliminary evidence that northern elephant seals dark adapt
completely in 10 minutes. Given their sensitivity range, this
suggests that they are adapting at a rate approaching 1
log/min, and thus operating with near maximum sensitivity
at most depths.
There is good evidence that freely diving Weddell seals
detect novel holes in the ice at ranges where the light from
the hole just exceeds their visual sensitivity threshold. A prediction of maximum sensitivity was made from laboratory
results with harbor and spotted seals (Wartzok 1979). In spite
ofthe extrapolations from laboratory data to the field situation and from harbor and spotted seals to Weddell seals, the
detection distances correspond to those predicted based on
the maximum sensitivity at typical states of adaptation, and
on the extinction coefficients in the water column (Wartzok
et al. 1992).
The fact that the pupils of marine mammals are usually
constricted when they are in bright light at the surface is one
factor that helps prevent a total bleaching ofthe rod pigment.
The constricted pupil not only helps preserve a partial state
of dark adaptation, it is also essential for visual acuity in air.
Visual Acuity
Visual acuity is a measure ofhow well an animal can resolve
features in its visual environment. For example, it can be
measured by determining how far apart two points oflight
must be for the subject to detect that there really are two
lights, rather than one; or how broad alternating stripes of
black and white must be for the subject to recognize them as
stripes, rather than a uniform gray. Because these separations of lights or widths of stripes varies with distance from
the subject, visual acuity is usually measured in terms ofdegrees or minutes ofarc. As a point ofreference, the diameter
ofthe full moon is about one-halfdegree, or 30 min ofarc. Visual acuity is dependent on the focusing ability ofthe optics
ofthe eye, the denSity ofreceptors in the retina, the connections between the receptors, and the subsequent processing
ofthe signal in the central nervous system.
The extent to which light rays are refracted when they
pass through the interface between different media is dependent on the difference in refractive indices of the media
and the angle of the light with respect to the interface be-
152
DOUGLAS WARTZOK AND
DARLENE R.
KETTEN
tween the media. Ifthe light ray is perpendicular to the interface, the ray is not refracted. The strength ofa homogeneous
lens in air, therefore, is dependent on its refractive index and
its radius of curvature. A light ray entering a terrestrial eye
experiences its greatest difference in refractive index at the
air-cornea interface (Fig. 4-11). Depending on the radius of
curvature, this can produce a lens with a strength of25 to 40
diopters. Diopters are a measure ofthe refractive power ofa
lens given as the reciprocal of the focal length in meters. In
humans, focusing at the air-cornea interface accounts for
about two-thirds ofthe total focusing power ofthe visual system. The actual lens within the eye provides only about onethird of the focusing power. When terrestrial mammals returned to the sea, they had to compensate for the loss of a
major focusing element in their visual systems. The reason
they lost the cornea interface lens power is that the refractive
index of water is similar to that of the interior of the eye,
therefore there is little change in refractive index as light
passes from the water into the eye througl,J. the thin cornea.
To see well underwater, marine mammals have developed
much stronger lenses. Refractive measurements of the eyes
of several species have shown that they are approximately
emmetropic, neither near- nor far-Sighted, for underwater
vision (bottlenose dolphin: Dawson et al. 1972, Dral 1972;
harbor seal:]ohnson 1893; harp seal: Piggins 1970; Weddell
seal: Wilson 1970).
The lenses in marine mammal eyes are more similar to
those in fish eyes than they are to the lenses in terrestrial
mammalian eyes. In cetaceans, the lenses are spherical in
shape and the ciliary muscles that change the shape of the
lens for accommodation, or focusing, appear to be nonexistent (Dral1972). In pinnipeds, the lenses have a shape intermediate between those of cetaceans and terrestrial
mammals, and ciliary muscles are attached to the s,clera, an
arrangement that has been postulated to allow for a strong
pull on the thick lens Uamieson and Fisher 1974).
The strong lens that compensates for the loss of the
air-cornea interface when the animal is underwater leads to
severe myopia when the animal is out of the water and regains the air-cornea lens. Exactly how marine mammals
overcome myopia in air is not well understood. One way is
through extensive pupillary contraction to a slit that can
close further to form a pin hole. The slit is oriented vertically
in the majority of pinnipeds, and horizontally in cetaceans,
and in bottlenose dolphins it takes the shape of a horizontal
crescent that closes to two slits at the ends ofthe crescent (a
double slit pupil) (Herman et al. 1975, Dawson et al. 1979). A
pin hole camera approaches an infinite depth of field so an
eye with a pin hole pupil will be emmetropic and an eye with
a slit pupil could provide focused images over a range of
distances.
The constricted pupil works well for animals in bright
light, but as the light intensity decreases and the pupil opens,
visual acUity declines. Schusterman and Balliet (1971) compared visual acuity in California sea lions above and below
water as the illumination decreased (Fig. 4-12), and demonstrated that performance degraded much more rapidly in air
than underwater. The initial good visual acuity in air is also
attributable to an apparently unique feature ofthe cornea of
California sea lions (although no other otariids have been
carefully studied). In the center of the cornea there is a 6.6mm diameter circular flattened area (Dawson et al. 1987b).
Because this portion of the cornea has no curvature, it does
not act as an additional lens in the air, and the sea lion has
equivalent aerial and underwater vision as long as the pupil
does not dilate beyond this diameter.
Although the above considerations certainly contribute
to functional vision in air, a few problems are not fully ex-
optic nerve
vitreous chamber
......
......
.......
cornea - - - H
.........
iris
ciliary body
conjunctiva
retina
sclera
choroid
Figure 4-11. Ray drawings ofthe focusing
ofa seal's eye in air and underwater. Underwater (solid line rays) there is no refraction at
the cornea. The only refraction occurs at the
lens. When in air, there is bending ofthe light
at both the cornea and at the lens leading
to focusing well in front ofthe retina (i.e.,
myopia). The bending at the lens is exaggerated to clearly show the effect.
Marine Mammal Sensory Systems
153
90
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CALIFORNIA SEA LION
(SPIKE)
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UNDERWATER ...... ~......
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BACKGROUND LUMINANCE -
plained. First, Dawson et al. (1979) showed that the time
course of pupillary constriction is too slow to allow a bottlenose dolphin to constrict its pupil between the time its
head leaves the water on a leap and the time at which it has to
make the final trajectory correction before its flukes leave
the water. Nevertheless, dolphins can leap accurately to
targets placed at variable locations above the surface. Rivamonte (1976) argued that the double slit pupil becomes diffraction limited before the pupil has constricted sufficiently
to achieve the acuities reported in air (Herman et al. 1975),
and he proposed that the dolphin has a lens that overcorrects
for spherical aberration by having the central core ofthe lens
surrounded by a region oflower refractive index. Light passing through the periphery of the lens (i.e., coming from the
peripheral field ofview), would need the additional strength
ofthe air-cornea interface to focus, and thus would be out of
focus underwater, whereas light passing through the lens on
axis would be in focus underwater but out of focus in air.
There is behavioral evidence that dolphins preferentially use
peripheral areas ofthe retina for forming images in air (Dawson et al. 1972, Pepper and Simmons 1973, DraI1975).
Two areas of high ganglion cell density are found in the
retinas of the follOWing species: bottlenose dolphin (Dral
1975, Mass and Supin 1995); the common dolphin (Delphinus
delphis) (Dral 1983); the finless porpoise (Neophocaena phocaenoides), and the Chinese river dolphin (Lipotes vexillifer)
(Gao and Zhou 1987); harbor porpoise and gray whale (Mass
and Supin 1990, 1997); and Dall's porpoise and minke whales
(Murayama et al. 1992). A rostral high-density area could improve vision to the side, whereas a dorsotemporal highdensity area could improve frontal vision. However, the
peak densities of ganglion cells (500 to 670/mm 2 in bottlenose dolphins, DraI1977, Mass and Supin 1995) are well
0
LOG mL
Figure 4-12. Aerial and underwater visual
acuity thresholds as a function ofluminance.
(Reprinted from Schusterman and Balliet
1971, ©New York Academy ofSciences.)
below the peak densities in rabbits (1O,000/mm 2 , Rodieck
1973) and cats (4,000/mm 2 , Stone 1965). Mass and Supin
(1995) calculate that the cell densities in bottlenose dolphins
would limit the retinal resolution to about 9 min of arc underwater and 12 min ofarc in air.
Kroger and Kirschfeld (1994) showed that the cornea,
rather than being a thin membrane that does not add an optical element to the visual pathway, can be a negative lens for
images formed in the periphery of the visual field. Kroger
and Kirschfeld (1992, 1994) measured the variable thickness
and refractive index of the cornea in harbor porpoises, and
argued that the negative corneal lens was required to compensate for a too powerful positive lens in the eye ofthe porpoise to produce emmetropia for underwater viewing. The
same arrangement could help alleviate myopia in air.
Visual acuities ofcetaceans and pinnipeds fall in the range
of 5 to 9 min ofarc both for underwater vision and for in-air
vision at high light intensities (Schusterman and Balliet
1970a,b, 1971; White et al. 1971; Herman et al. 1975). These
values are similar to those reported for terrestrial hunters
such as the cat (Muir and Mitchell 1973).
Sirenians
Sirenians have been reported to have poor vision (Walls
1942), based on early studies of manatees (e.g., Chapman
1875) and dugongs (e.g., Petit and Rochon-Duvigneaud
1929). These studies suggested poor visual acuity both in air
and underwater with probably an exclusively rod retina, but
no tapetum. On the basis of observations of manatee visual
behavior, Hartman (1979) suggested they were not as visually deficient as the older literature indicated. More recent
studies (Cohen et al. 1982) indicated that the manatee has
both rods and cones in its retina with a central visual area
154
DOUGLAS WARTZOK AND
DARLENE
R.
KETTEN
where visual acuity may be enhanced. Although there is little
refractive error in the optics of the eye underwater (Piggins
et al. 1983), acuity is still considered to be only moderate.
The rod-dominated retina, with extensive summing of receptors to ganglion cells, indicates that acuity has been sacrificed for vision at low light levels in murky water, bur the lack
ofa tapetum indicates a less than full adaptation to functioning at these light levels.
Ursids
Polar bears show little adaptation for underwater vision.
With the loss ofthe air-eornea interface, the polar bear loses
more than 20 diopters oflens strength underwater (Sivak and
Piggins 1975). The peak sensitivity ofthe dark-adapted eye is
at 525 nm, even a bit longer wavelength than typical of terrestrial predators such as the cat. The polar bear has both
rods and cones in its retina as indicated by separate scotopic
(i.e., dark adapted) and photopic (i.e., light adapted) functions (Ronald and Lee 1981).
Fissipeds
The sea otter has the most spectacular accommodative
range ofany vertebrate. It is able to see well in air and in water by a unique method ofchanging the radius ofcurvature,
and hence the strength, ofits lens (Murphy et al. 1990). As
shown in Figure 4-13, when the sea otter is underwater, the
loss of the approximately 60 diopter corneal-air interface
lens is compensated for by the action of the ciliary and iris
muscles. The ciliary muscle opens a path for fluid to flow
from the anterior chamber into the corneoscleral venous
plexus. This reduces the pressure in the anterior chamber
and causes the lens to be pushed forward by the pressure differential between the posterior and anterior chambers. As
Relaxed
Accommodated
the lens is pushed forward, the iris sphincter forces it to assume a new shape with a much smaller radius of curvature,
increasing the strength of the lens by 60 diopters. Although
the iris does not close to a slit or pin hole, as in dolphins and
seals, because the accommodative mechanism is dependent
on the iris muscle, there is the same trade offbetween sensitivity in low light and visual acuity. Although no behavioral
studies have been done on sea otter acuity and light levels,
Schusterman and Barrett (1973) showed that an Asian"clawless" otter (Amblonyx cineria cineria) lost acuity underwater
more rapidly than in air when light levels decreased.
Chemoreception
Both air and water are fluids; therefore, the underlying principles of the spread of chemicals through diffusion and
convection in laminar and turbulent flow are the same. However, diffusion is approximately 10,000 times slower in water
than in air and average water currents are approximately 15
times slower than average air currents (Vogel 1981). Thus,
some aspects of chemical communication in water are farless efficient than chemical communication in air.
Smell and taste are closely aligned senses for detection of
substances in air and in liquids, respectively. Neither sensory
modality has been investigated with much rigor in marine
mammals. Olfactory sensation appears to decline in parallel
with adaptation to the marine environment. Gustatory sensation is present in dolphins, and presumably in other marine
mammals, but there is a paucity of experimental evidence.
The difficulty of controlling, measuring, and presenting
chemical stimuli, as well as the limited availability ofmarine
mammals for experiments, results in very slow progress in
this area. Lowell and Flanigan (1980), Watkins and Wartzok
Figure 4-13. Proposed mechanism of
visual accommodation for underwater vision
in the sea otter. In this model, the ciliary and
iridal muscles act to decrease markedly the
radius ofcurvature ofthe anterior lens surface, thus making a stronger lens to compensate for the loss ofthe air-corneal interface
lens. Contraction ofthe ciliary muscle will
bring about a di1<ition ofthe corneoscleral
venous plexus, lowering its hydrostatic
pressure and causing redistribution ofaqueous humor from the anterior chamber into
the plexus (arrow). This pressure will bring
about an anteriorward movement ofthe lens
which is then deformed by action ofthe iris
sphincter muscle. (Reprinted from Murphy
et al. 1990, ©Elsevier Science Inc.)
Marine Mammal Sensory Systems
(1985), and Nachtigall (1986) have reviewed basically the
same small set ofexperimental results.
Olfaction
Anatomically, the olfactory system of mysticetes, odontocetes, and sirenians is less developed than those ofterrestrial
mammals. Odontocetes lack olfactory bulbs and attendant
ganglia or fiber tracts (Breathnach 1960, Pilleri and Gihr
1970, Morgane andJacobs 1972). Manatees have a very rudimentary olfactory system, and, like cetaceans, lack an important component of the olfactory system, a vomeronasal
organ (Mackay-Sim et al. 1985). Pinnipeds have both peripheral (Kuzin and Sobolevsky 1976) and central (Harrison and
Kooyman 1968) olfactory structures, although in phocids
and walrus they are somewhat reduced compared to those of
otariids (Harrison and Kooyman 1968). Both otariids and
phocids show behavioral evidence of olfactory sensation.
Among many examples that could be cited, males sniff the
hindquarters offemales to assess the state ofestrus in northern fur seals (Callorhinus ursinus) (Bartholomew 1953) and
South African fur seals (Arctocephalus pusillus) (Rand 1955).
In southern elephant seals, experienced females begin
smelling a newborn pup sooner after birth than do primiparous females (McCann 1982), and learn the identity of
their pups sooner.
Gustation
Neuroanatomy (Jacobs et al. 1971) and tongue morphology
(Sukhovskaya 1972, Donaldson 1977, Yamasaki et al. 1978)
indicate that odontocetes have the ability to taste. Jacobs et
al. (1971) suggested that the well-developed olfactory lobes
in the rhinencephalon of bottlenose dolphins might be innervated by the trigeminal nerve, in place of the missing
olfactory nerve, and thus might be sensitive to substances
Stimulating receptors on the tongue. Taste buds located
in grooves or pits at the root of the tongue have been described in bottlenose dolphins (Sukhovskaya 1972, Donaldson 1977), common dolphins (Sukhovskaya 1972), and the
Striped dolphin (Stenella coeruleoalba) (Yamasaki et al. 1978,
Komatsu and Yamasaki 1980). In manatees, taste buds are located in dorsal and posterior lateral swellings on the tongue
(Yamasaki et al. 1980). In dugongs, the taste buds are located
in pits rather than swellings in the same general dorsal and
posterior lateral areas of the tongue (Yamasaki et al. 1980).
Although the number of gustatory receptors is greater in
sirenians than in cetaceans, they are still poorly endowed
compared to herbivorous land mammals.
Kuznetsov and colleagues, using a number of different
155
behavioral and phYSiological indicators, have reported
chemoreception for a number of substances (for review,
see Kuznetsov 1990). These studies showed that harbor
porpoise, common dolphin, and the Black Sea bottlenose
dolphin could detect a variety of chemicals with a welldeveloped ability to detect bitter chemicals, a less welldeveloped ability to detect salinity, and an apparent inability
to detect sugar. None ofthe experiments determined detection thresholds by comparing differing response levels with
different stimulus concentrations.
Nachtigall and Hall (1984) used a go I no-go operant conditioning technique with a bottlenose dolphin to establish
detection thresholds for sour (citric acid), bitter (quinine sulfate), salt, and sweet (sucrose). They showed thatthe dolphin
could detect tastes humans classify as sour and bitter at levels
only slightly above the range ofhuman detection thresholds.
In contrast to the results of Kuznetsov (1979), the dolphin
used by Nachtigall and Hall was able to detect sucrose, although at much higher thresholds than those of humans.
Nachtigall and Hall (1984) also showed a sensitivity to salt,
but these results were confounded by the animal being held
in salt water. In summary, the results show that dolphins
with taste receptors located only atthe root ofthe tongue can
detect chemicals assigned by humans to all four ofthe taste
groups.
Little work has been done on taste sensation in pinnipeds.
Kuznetsov (1982, cited in Friedl et al. 1990) reported that
Steller sea lions (Eumetopiasjubatus) detected sour, bitter, and
salty stimuli, but were insensitive to sweet. Friedl et al. (1990)
reported on experiments done with a California sea lion using the same techniques used by Nachtigall and Hall (1984).
The sea lion was good at detecting citric acid, and discriminated between freshwater and seawater, but had a high
threshold for bitter, and appeared not to detect sweet. As
Friedl et al. (1990) noted, "much work remains for patient researchers in the area of marine mammal chemoreception."
Tactile Sensation
Cetaceans
Most ofthe studies oftactile sensation in cetaceans have been
done in bottlenose dolphins with the objective to understand
how these animals maintain laminar flow over major portions of the body at fast swimming speeds. Gray's paradox
(Gray 1936) suggested that dolphin muscles would need to
be seven times more powerful than they are ifthe dolphin experienced the turbulent flow predicted by their body shape
and speed of movement through the water. Lang and coworkers (Lang 1966, Lang and Norris 1966, Lang and Pryor
156
DOUGLAS
WARTZOK AND
DARLENE
R.
KETTEN
1966) demonstrated that for several odontocetes drag coefficients measured during glides were indicative of turbulent
flow over the entire surface of the animal. They suggested
that energetically problematic high-speed swimming was
limited to short bouts so that reasonable estimates of propulsive power capabilities were not violated. However, drag
measured during a glide is not necessarily representative of
drag during active swimming (Alexander and Goldspink
1977). If the animals are capable of actively damping turbulence, they could likewise be capable ofnot damping it or enhancing it based on their intention to move forward or glide
to a stop. Support for some form of active damping comes
from observations showing that little turbulence is generated over most of the body of a swimming Pacific whitesided dolphin. A number of investigators have speculated,
based on the anatomy ofthe skin and the innervation of the
skin, that active damping ofincipient turbulence is occurring
(Kramer 1965, Surkina 1971, Kayan 1974, Khomenko and
Khadzhinskiy 1974, Babenko and Nikishova 1976, Ridgway
and Carder 1990).
The first step in determining whether dolphins are capable of active damping is to assess their tactile sensitivity.
Kolchin and Bel'kovich (1973) used galvanic skin responses
to map areas ofgreatest sensitivity on the body of common
dolphins. They found the area of highest sensitivity within
2.5 cm from the blowhole and in separate 5 -cm diameter circles around the eyes. The next most sensitive area was the
snout, lower jaw, and melon. The area of the back, both anterior and posterior to the dorsal fin, had a lower sensitivity.
Bryden and Molyneux (1986) found large numbers ofencapsulated nerve endings in the region of the blowhole in both
bottlenose dolphins and false killer whales. They suggested
that these mechanoreceptors were involved in detection of
the pressure changes associated with the blowhole breaking
the water surface. They found more receptors on the anterior lip of the blowhole, the first part of the blowhole that
would become exposed when the animal surfaced. These
most sensitive areas are not the most critical areas for dampening turbulence.
Using electroencephalograms to map areas of tactile
sensitivity on the body ofbottlenose dolphins, Ridgway and
Carder (1990) expanded on early studies by Lende and Welker (1972). They found highest sensitivity at the angle ofthe
gape, followed by the area around the eyes and melon, followed by the area around the tip of the snout and the blowhole. The least sensitive areas were on the remainder ofthe
dolphin's trunk. Although there are some differences in most
sensitive areas, the results ofRidgway and Carder (1990) and
Kolchin and Bel'kovich (1973) agree that the head region is
the most sensitive. The minimum detectable pressure values
of 10 mg/mm2 , obtained by Kolchin and Bel'kovich (1973)
using a static, weighted O.3-mm wire, are similar to those obtained for humans in their most sensitive areas such as the
fingertips and lips. Even the 40 mg/mm2 found on the common dolphin trunk shows a high level of tactile sensitivity
over the majority ofthe body.
Knowing a dolphin is capable of detecting pressure associated with turbulence as it swims is only part ofthe issue
of whether a dolphin can actively damp turbulence. To determine whether there is muscle control sufficient to effect
the damping, Haider and Lindsley (1964) and Ridgway and
Carder (1990) studied microvibrations in bottlenose dolphins. Haider and Lindsley (1964) showed that these vibrations were at least three times greater in amplitude in
Figure 4-14. A photograph of a ringed seal
surfacing through a manmade hole in the ice.
The extensively developed vibrissae are
obvious.
Marine Mammal Sensory Systems
dolphins than in humans (15 !lm, cf 5 !l maximum) and
somewhat faster in frequency (13 Hz, cf 11 Hz). Ridgway
and Carder (1990) showed that the dolphins responded to a
vibratory stimulus by entraining their spontaneous microvibrations to the frequency of the stimulus and by increasing
the normal amplitude of the microvibrations. This level of
control of spontaneous microvibrations suggests a possible
mechanism for damping turbulence by flexing the body surface away from regions of higher pressure and toward
regions oflower pressure in the water flowing over the dolphin. Currently there is no evidence showing that dolphins
actually use this mechanism.
Pinnipeds
The most obvious marine mammal tactile sensory structures are the vibrissae of pinnipeds. Not only are they obvious when viewing the animal (Fig. 4-14), they are also highly
innervated peripherally and well-represented cortically with
large areas devoted to input from the vibrissae. Anatomical
and phYSiological studies have been more successful in
demonstrating their importance than have behavioral studies. Dykes (1975) showed that the vibrissae ofharp seals and
harbor seals were heavily innervated with slowly and rapidly
adapting nerve fibers. Both fiber types had a range ofthresholds resulting in a sensory system that could provide detailed
information about static displacement and vibratory stimuli.
The sensitivity ofthe vibrissae is enhanced by the rich supply
of blood vessels in the dermal sheath (Ling 1966), which
could provide adaptive changes in the compliance, or flexibility, and by the histologically prominent circular sinuses
around the vibrissae (Stephens et al. 1973, Hyvarinen 1989).
In ringed seals, Hyvarinen (1989) found that each vibriss<ll
follicle is innervated by 1000 to 1600 fibers.
Ladygina et al. (1992) mapped the body surface ofnorthern fur seals onto,the somatosensory cortex. The fur seal has
a duplicate somatosensory projection in the cortex. Although a duplicate projection ofthe entire body has been observed in some monkeys (Merzenich et al. 1978, Nelson et al.
1980, Sur et al. 1982), it usually only occurs for those parts of
the body involved in particularly fine tactile discriminations
such as the forepaw ofthe gray squirrel (Sciurus carolinensis)
(Sur et al. 1978, Nelson et al. 1979, Krubutzeret al. 1986), the
hand ofprosimian primates (Carlson and Welt 1980, Sur et
al. 1980, Carlson and FitzPatrick 1982, FitzPatrick et al. 1982,
Carlson et al. 1986), and the vibrissae ofthe opossum (Didelphisvirginiana) (Pubols et al. 1976). Ladygina et al. (1992) calculated magnification factors (the relative distance between
two cortical recording places to the distance between the
two locations on the body that provided maximum stimulation of the cortical sites) and found that the factor varied
157
from 0.01 to 0.5. On the trunk, the value was 0.01, meaning
that a 1-mm shift in recording location in the cortex resulted
in a 1OO-mm shift in the most sensitive body area. For the vibrissae, the factor was as large as 0.5, meaning that a 1-mm
shift in recording location in some areas ofthe cortex corresponded to only a 2-mm shift on the maxillar vibrissal pad.
This indicates the extensive cortical space allocated to tactile
input from the vibrissae.
Dykes (1975) determined, using electrophysiological recordings from nerves innervating the vibrissae of harbor
seals, that the threshold for responses to vibratory stimuli
were less than 7 sec ofare. All ofthe rapidly adapting fibers responded to vibratory stimuli of256 Hz, but at 1024 Hz only
15% ofthe fibers followed the vibratory stimulus, and at 1500
Hz, fewer than 1% ofthe fibers followed the stimulus. In contrast, psychophysical studies by Renouf(1979) and Mills and
Renouf (1986) indicated a marked increase in sensitivity to
vibratory stimuli as frequencies increased to a peak sensitivity at 1000 Hz, with little decline in sensitivity out to 2500 Hz,
the highest frequency tested.
Dykes (1975) postulated that the sensitivity ofthe slowly
adapting nerve fibers to small, but not large, displacements,
and the ability of the rapidly adapting nerve fibers to detect
very small vibratory stimuli meant that the vibrissae were innervated to prOVide information about contour and texture.
Behavioral results are in line with this prediction.
Kastelein and van Gaalen (1988) showed that a walrus
(Odobenus rosmarus), fitted with eye cups blocking vision,
could use its vibrissae to distinguish between a square and a
triangle even when the surface areas of the stimuli were
gradually decreased to 0.4 cm'. Dehnhardt (1990) demonstrated that a California sea lion, deprived of vision by eye
cups, could distinguish among five different three-dimensional objects when allowed to touch them with its vibrissae.
In a subsequent experiment (Dehnhardt 1994), this same sea
lion detected diameter differences as small as 0.33 cm for
discs with a mean diameter of 1.12 cm. This threshold led to
a Weber's fraction (miniumum detectable diameter difference/mean diameter) of0.29. The sea lion tactile thresholds
followed Weber's law, which states that Weber's fraction
should be constant (Le., L\D will increase as D increases). Weber's fraction was also 0.29 for discs with a mean size of8.74
cm. Studies on two harbor seals showed similar values for
Weber's fraction at disc sizes of 1.12 cm, but values as low of
0.13 (male) and 0.08 (female) for discs of 5.04 and 8.74 cm
(Dehnhardt and Kaminski 1995). Thus, the best tactile size
discrimination threshold for the California sea lion was
about twice as great as it was for harbor seals. The small
number of individuals tested and the individual variability
observed preclude definitive species rankings on tactile ability. However, it is interesting to note that the Weber's frac-
158
DOUGLAS
WARTZOK
AND
DARLENE
R.
KETTEN
tions attained by the harbor seals are similar to those reported for the hands of lower primates such as macaque
monkeys (Semmes and Porter 1972, Carlson et al. 1989).
Also the Weber fractions for tactile size discrimination by sea
lions and harbor seals are similar to those obtained for visual
size discriminations by these and other marine mammal
species (California sea lion, Schusterman et al. 1965; harbor
seal, Feinsein and Rice 1966; spotted seal, Wartzok and Ray
1976; South African fur seal, Busch and Ducker 1987). This
similarity between tactile and visual discrimination Weber
fractions is an indication ofthe importance oftactile discrimination for pinnipeds.
All-or-none behavioral experiments, which investigated
the transmission of phasic (i.e., not static) information
through the vibrissae, showed little difference in the animal's
ability to complete the task whether vibrissae were present
or not. Renouf (1980) recorded the length of time harbor
seals required to capture live fish. Animals with vibrissae
clipped off showed no increase in time required in either
clear or murky water. Although the vibrissae might not serve
a role in fish capture, they could well be important for benthic feeding, particularly at depths where light levels have
fallen below threshold. Benthic prey have been observed in
fecal samples of harbor seals (Hark6nen 1987) and ringed
seals (Kelly and Wartzok 1996). Lindt (1956) described
Southern sea lions (Otaria byronia) swimming near the benthos with their vibrissae erect and touching the sea bottom.
Kelly and Wartzok (1996) reported that ringed seals repeatedly dove to the bottom on apparent feeding dives.
As a test of Montagna's (1967) suggestion that one function of the vibrissae might be speed sensing, Renouf and
Gaborko (1982) trained a seal to swim through hoops maintaining a constant speed of 6 km/hr. When the animal was
able to do this, its vibrissae were cut off. After the removal of
the vibrissae, the seal was still able to maintain the same
speed. However, this was not a good test of Montagna's hypotheSiS because the seal was able to see the sequence of
hoops even after the vibrissae were removed and thus had
other pOSSible speed-sensing cues.
The one all-or-nothing experiment that showed an important role for the vibrissae was a static recognition task.
Sonafrank et al. (1983) reported that a blindfolded seal attracted to a hole though the ice using an acoustic cue would
ascend directly up through the center of the hole when its
vibrissae were Unimpeded. However, when the blindfolded
seal also had its vibrissae restricted, it still found the hole
through the acoustic stimulus just as effectively but bumped
into the under side of the ice just lateral to the hole. When
finally in the hole, apparently through trial and error, it ascended more slowly to the surface than when the vibrissae
were free. A blindfolded seal with free vibrissae but without
an acoustic cue would swim directly under an open hole and
not detect it. The vibrissae apparently were unable to provide the seal with usable information on the differences in
the reflected pressure wave from the ice and the open hole.
Sirenians
The dugonghas the most developed sensory hairs ofany marine mammal (Kamiya and Yamasaki 1981). These hairs are
present over the entire surface ofthe body, being most dense
on the muzzle. A similar pattern is seen in hair distribution in
manatees. Marshall and Reep and coworkers (Marshall et al.
1998, Reep et al. 1998) have recently completed studies ofthe
bristles, hair, and bristlelike hair ofthe facial region ofFlorida
manatees. The bristles appear to be modified vibrissae. They
are used in tactile exploration ofthe environment and appear
quite sensitive to touch (Hartman 1979, Marshall et al. 1998).
The bristles are different from vibrissae, however, in that
they can be actively everted and used in a grasping fashion
during feeding and manipulation ofobjects. The manatee is
unique among marine mammals in its ability to use its vibrissae or bristles in a prehensile manner. There appears to
be a one-to-one relationship between the number ofperioral
bristles and the number ofneuronal clusters in the region of
the cerebral cortex devoted to tactile sensation from the face
(Marshall and Reep 1995, Reep et al. 1998).
MagnetiC Detection
Water has almost no effect on magnetic flux denSity. Thus
magnetic sensors should be equally effective underwater as
in the air. Interest in animal use ofthe earth's magnetic field
was stimulated by Keeton's (1971) finding that the orientation ability ofhoming pigeons could be disrupted by attaching magnetic coils to the heads ofthe birds on days when the
sun was not visible. A number of studies stimulated by this
finding gradually deVeloped methodological and theoretical criteria that should be kept in mind when evaluating the
pOSSibility of biomagnetism in marine mammals. Magnetite is the material that has been consistently implicated in
magnetic field reception in species easier to work with
than marine mammals. Magnetite can be formed through
biochemical processes within the body, but unfortunately
ferromagnetic materials are also ubiquitous industrial pollutants, and great care must be exercised in determining the
origin of any "magnetite" detected in an animal. One way
of distinguishing functional magnetite from contamination
is through considerations of the size and characteristics
of magnetite needed to function as a magnetic detector.
Marine Mammal Sensory Systems
Kirschvink and Walker (1985) argued that single-domain
crystals are the most likely form of magnetite to be used in
magnetosensation. A second consideration is the chemical
composition of the magnetite. Magnetite with few oxides
other than iron oxide is more likely derived from biochemical reactions within the animal, whereas magnetite with oxides ofrare earth metals, such as titanium and manganese, is
more likely of geologic origin (Walker et al. 1985). A third
consideration is the consistency oflocation of magnetite in
the same tissues of each specimen from the same species or
higher taxa.
The magnetic material found in cetaceans most fully
meets the third criterion. Magnetic material was found in
the dura matter in the area ofthe falx cerebri and the tentorium cerebelli (Bauer et al. 1985) in three odontocete species,
bottlenose dolphins, Dall's porpoise, Cuvier's beaked whale
(Ziphius cavirostris), and one mysticete, the humpback
whale. The dura is the tough outer membrane covering the
brain. The falx cerebri is the region ofthe dura separating the
cerebral hemispheres, and the tentorium cerebelli is the region of the dura separating the cerebrum and the cerebellum. These are the locations where magnetic material has
been found in adult cetaceans. Any conclusions regarding
the role ofthis magnetic material in magnetoreception must
be tempered by noting that the amount ofmagnetic material
in the dura appears to increase with age (Bauer et al. 1985).
The falx cerebri and tentorium cerebelli are the areas of the
dura that show increasing ossification with age (Nojima
1988), and magnetite is known to provide strucmral support
by increasing the hardness of chitin in teeth (Kirschvink and
Lowenstam 1979). Thus, magnetite in this region may be
more related to the ossification ofthese tissues than to a magnetic sensory system.
The amount of magnetic material isolated from cetaceans to date has not been sufficient to confirm it as Single
domain magnetite or even to identify it conclusively as magnetite (Bauer et al. 1985). The magnetic material does not,
however, appear to be contamination with the probable exception ofthe first report in Tursiops (Zoeger et al. 1981). It is
difficult to dissect animals as large as cetaceans using nonmagnetic tools and to carry out the dissection in a clean environment to avoid contamination.
Although the anatomical smdies remain equivocal, there
is correlational evidence that some cetaceans are using magnetic information to guide their movements. Klinowska
(1985, 1986) compared locations in the United Kingdom
where dead stranded cetaceans were found and where live
strandings took place. She found that all cases oflive strandings took place at points where local lows, or valleys, in the
magnetic fields intersected the coast or islands. There was no
159
such correlation between strandings of dead cetaceans,
which had presumably been washed ashore by currents, and
the magnetic field orientation. Because of reversals of the
magnetic field over geological time and the spreading ofthe
ocean sea floor, there are alternating bands ofmagnetic orientation running north to south parallel to the mid-ocean
rift where the sea floor spreading originates (Vine 1966). If
whales were able to sense these alternations in the magnetic
field, they could use these patterns as north-south highways
on their annual north-south migrations. An indicator of
magnetic field dip would provide information on pOSition
along the north-south axis, and if they could keep track
of how many reversals they crossed, they could use this information for east-west positioning (Kirschvink and Walker 1985).
Kirschvink and colleagues (Kirschvink et al. 1986,
Kirschvink 1990) have extended and confirmed Klinowska's
(1985, 1986) United Kingdom smdy to the United States. The
following species were Significantly more likely to strand at
sites where geomagnetic lows intersected the coastline:
long-finned pilot whale (Globicephala melaena), short-finned
pilot whale (G. macrorhynchus), striped dolphin, Atlantic
spotted dolphin (Stene/la frontalis), Atlantic white-sided dolphin(Lagenorhynchus acutus), common dolphin, harbor seal,
sperm whale, pygmy sperm whale (Kogia breviceps), and fin
whale.
In contrast to the results of Klinowska and Kirschvink,
Brabyn and Frew (1994) found no correlation between magnetic field orientation, minima, or gradients and the locations oflive strandings in New Zealand. A possible explanation for the different results is the absence of a consistent
orientation ofthe magnetic contours around New Zealand
compared to the sea floor of the North Atlantic off the east
coast ofthe United States and around the United Kingdom.
Attempts to demonstrate senSitivity to magnetic fields in
laboratory experiments have been unsuccessful with cetace~ (Bauer et al. 1985). This result is not surprising when
compared to studies with more tractable laboratory animals.
A key feamre ofsuccessful experiments is the freedom ofthe
animals to move extensively within the altered magnetic
fields. Under these conditions, which are difficult to duplicate for marine mammals, laboratory demonstrations of
magnetoreception have been successful in salamanders
(Phillips and Adler 1978), honeybees (Walker et al. 1989), and
tuna (Walker 1984).
Walker et al. (1992) looked at free-swimming fin whales
and found that migrating animals were associated with lows
in the geomagnetic gradient or intensity. Because of the
great difficulty in obtaining substantial numbers of pure
anatomical specimens and in conducting laboratory ex-
160
DOUGLAS WAR TZOK AND
DARLENE R.
KETTEN
periments demonstrating magnetoreception, correlational
studies rather than definitive studies will continue to be the
norm.
Summary
Marine mammals are acoustically diverse, with wide variations not only in ear anatomy, but also in frequency range
and amplitude sensitivity. In general their hearing is as acute
as that of land mammals, and they have wider ranges. Although marine mammals exhibit habitat- and size-related
hearing trends that parallel those of land mammals in that
larger species tend to have lower frequency ranges than
smaller species, the majority ofspecies have some ultrasonic
capability and there are multiple specialized, auditory adaptations in odontocetes that provide large species exceptional
high frequency hearing capabilities. Both mysticetes and
odontocetes appear to have soft-tissue channels for sound
conduction to the ear. Sirenians may have analogous adaptations. It remains unclear whether pinnipeds use soft-tissue
channels in addition to the air-filled external canal for sound
reception. Comparisons of the hearing characteristics of
otarids and phocids suggest that there are at least two types
of pinniped ears, with phocids being better adapted for underwater hearing. Sea otter ears are the most similarto those
ofland mammals ofall marine mammal ears that have been
investigated, but they do have some aquatic-related features,
and it is not known how well they hear underwater. No data
are available on polar bear hearing.
All marine mammals have middle ears that are heavily
modified structurally from those in terrestrial mammals in
ways that reduce the probability of barotrauma. The end
product is an acoustically sensitive ear that is simultaneously
adapted to sustain moderately rapid and extreme pressure
changes, and which appears capable of accommodating
acoustic power relationships several magnitudes greater
than in air. It is possible that these special adaptations may coincidentally prOvide acoustically protective mechanisms
that lessen the risk ofinjury from high intensity noise, but no
behavioral or psychometric studies are yet available that directly address this issue.
Visual adaptations parallel the extent to which marine
mammals have returned to the marine environment. Although light is extinguished more quickly in water than in
air, there is sufficient light that vision is an important sensory
modality for marine mammals at almost all depths they inhabit. The lens in the eyes ofcetaceans has become more like
a fish lens to accommodate for the loss offocusing power of
the air-cornea interface. Sirenians, despite of their long history as a fully marine species, have not made as many adaptations to achieve acute underwater vision as have cetaceans.
Just as in audition, pinnipeds have compromised full underwater adaptation to allow for functional vision in air as well.
One result ofthese compromises is that although pinnipeds
can see well in air in bright light, acuity decreases with declining light levels. The polar bear has a basically terrestrial
eye. The sea otter has developed a unique accommodation
mechanism to prOVide good visual acuity in air and underwater. All marine mammals carefully studied have both rod
and cone retinas, but few studies have ascertained ifthey can
detect colors. The most likely reasons for the multiple pigment systems is to be able to maximize sensitivity and detection over a wide range ofdepths and light levels.
Olfaction has declined as adaptation to a marine environment has increased, and is apparently nonexistent in cetaceans, rudimentary in sirenians, and still an important
modality, particularly for behavioral interactions, in pinnipeds. The little work that has been done in taste sensation
indicates that most tested species can detect the various categories oftastes defined by humans. Gustatory tests are difficult to conduct and quantify for species liVing in water. Also,
it is difficult to define ecologically relevant gustatory discriminations for marine mammals.
Cetaceans have greatest tactile sensitivity near the blowhole where detection ofthe air-water interface is important.
Tactile sensitivity over the trunk of the body appears to be
sufficient to provide the sensory input needed to actively
damp turbulence, but how the afferent and efferent pathways link and are used to achieve this goal remains an open
question. The vibrissae of pinnipeds are extensively developed, richly innervated, and as well-represented cortically as
are the hands of some primates. They provide the animal
with information about contour and texture, but seem to be
less adapted for the transmission ofphasic information such
as speed sensing.
Magnetic sensation has been investigated primarily in
cetaceans. There is evidence that the movements of several
cetacean species correlate with geomagnetic patterns. Evidence ofa mechanism for detection ofgeomagnetism is very
weak.. Magnetite has been identified in the brains of several
species, in the same regions of the dura matter, but the increase in concentration with age, which parallels the ossification ofthese structures, raises questions as to the function
ofmagnetite in these areas. It is likely that most progress on
working out the exact mechanisms of magnetic sensation
will likely take place in species more tractable than marine
mammals.
One irony of sensory system research is that the more
tools we invent to explore animals and their senses the
greater the hints we receive that our reach is still too short.
How extensive is our research arm currently? We know marine mammals use frequencies we cannot hear, but techno-
Marine Mammal Sensory Systems
logically we can detect and transduce their frequency range
into something we can analyze. Tools that help us probe and
visualize how marine mammal sounds are produced and
processed, like fast biomedical imaging, are helpful but still
comparatively limited. All marine mammals carefully studied are sensitive to about the same range of visual wavelengths as humans. Consequently, vision studies can be
conducted more straightforwardly on marine mammals because there is no need to transduce the frequencies they see
into ones we see. Chemosensation may be reduced in marine
mammals, but we should also consider that we may simply
not yet have asked the proper questions or developed adequate tools to measure responses in terms we understand.
The anatomical sophistication and the extensive cortical
space allotted to vibrissal sensory processing implies a more
important role than we have yet determined. Our greatest
shortcoming is that we cannot yet measure or observe reliably and frequently in the truly relevant environment for marine mammals: at depth in a free-ranging animal. Until we
do, we cannot truly understand what is happening in any marine mammal's ear, eye, or brain, and what transpires in the
real world ofmost marine mammals, the open ocean and the
deeps, will remain a mystery.
Notes
1. The conventional unit offrequency, the Hertz, abbreviated Hz, is
named after a nineteenth century German physicist and is equal to 1
cycle Isec, or 1 cps. kHz is an abbreviation for kiloHertz, or 1000 cps.
2. All phYSical constants were obtained from the CRC Handbook of
Chemistry and Physics, 66th edition (Weast 1985) unless otherwise
noted.
3. Like sonic, the airborne sound reference pressure is based on a
human metric. The lowest sound level the normal human ear deteCts
at 2 kHz is a diffuse field pressure of20 llPa, which has an acoustic
power density ofapproximately 1picowatt/m2 • Therefore, the
common human threshold in air for 2 kHz, which is at or near the
most sensitive frequency in a normal human ear, is 20 log (20 llPa I 20
llPa) = 20 log 1 = 0 dB re 20 llPa, or 0 dB SPL. In some older literature, dB SPL is used when decibel values reported were based on
ambient pressure as reference, which is generally stated in the text.
4. An octave is a doubling offrequency. For any initial frequency (j),
the octave range is 2f, but because the scale is nonlinear, the center
'frequency is 1"'2'''. Because octaves are self-referential, two animals
may have radically different hearing ranges in terms offrequency,
but equal octave spans (e.g., 30-15,000 Hz vs. 100-50,000 Hz; nine
octaves in each case).
5, Typical values for human critical ratios (CR) at speech frequencies
are 10 to 18 dB.
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