experimentation and postmortem analyses of dolphin cranial
anatomy have resulted in our current understanding of the
acoustics and biomechanics of dolphin echolocation.
characterized not only the physics of echolocation (e.g.
echolocation pulse length, source levels, transmit beams) but
has also identified the detection and discrimination capabilities
that it imparts to the dolphin (Au, 1993). Hearing sensitivity,
frequency and amplitude discrimination have also been
discerned via psychoacoustic means, providing additional
characterization of auditory system function (Nachtigall et al.,
2000). Physiological experimentation coupled with anatomical
investigation has revealed mechanisms of sound production in
the nasal system (Dormer, 1974; Ridgway et al., 1980) and
sound conduction to the dolphin ear (Bullock and Ridgway,
of psychoacoustic and physiological
in particular, has
1972; McCormick et al., 1970). Postmortem anatomical
investigations have been crucial to inferring the role of specific
anatomical structures to sound production and reception
processes (Cranford, 2000; Ketten, 2000), but establishing
definitive quantitative and qualitative relationships between
structure and function has been a difficult task. It remains a
substantial impediment to a comprehensive understanding of
the biomechanics of delphinid sound production and reception.
Reports on the postmortem investigation of delphinid
anatomy date back to the 18th century (Hunter, 1787), with
more comprehensive, multi-species reports on cetacean cranial
anatomy surfacing during the past century (e.g. Fraser and
Purves, 1960). These postmortem studies have revealed
numerous anatomical variations on the terrestrial mammal
theme that are important to sound generation and sound
reception in an aquatic environment. In delphinids, the fusion
The Journal of Experimental Biology 207, 3657-3665
Published by The Company of Biologists 2004
Bottlenose dolphins were submitted to structural (CT)
and functional (SPECT/PET) scans to investigate their in
vivo anatomy and physiology with respect to structures
important to hearing and echolocation. The spatial
arrangement of the nasal passage and sinus air spaces to
the auditory bullae and phonic lips was studied in two
dolphins via CT. Air volume of the sinuses and nasal
passages ranged from 267.4 to 380.9·ml. Relationships of
air spaces to the auditory bullae and phonic lips support
previous hypotheses that air protects the ears from
echolocation clicks generated by the dolphin and
contributes to dolphin hearing capabilities (e.g. minimum
angular resolution, inter-aural intensity differences). Lung
air may replenish reductions in sinus and nasal passage
air volume via the palatopharyngeal sphincter, thus
permitting the echolocation mechanism to operate at
depth. To determine the relative extent of regional blood
flow within the head of the dolphin, two dolphins were
scanned with SPECT after an intravenous dose of
99mTc-bicisate. A single dolphin received
740·MBq of 18F-2-fluoro-2-deoxyglucose (FDG) to identify
the relative metabolic activity of head tissues. Substantial
blood flow was noted across the dorsoanterior curvature
of the melon and within the posterior region of the lower
jaw fats. Metabolism of these tissues relative to others
within the head was nominal. It is suggested that blood
flow in these fat bodies serves to thermoregulate lipid
density of the melon and jaw canal. Sound velocity is
inversely related to the temperature of acoustic lipids
(decreasing lipid density), and changes in lipid
temperature are likely to impact the wave guide
properties of the sound projection and reception
pathways. Thermoregulation of lipid density may
maintain sound velocity gradients of the acoustic lipid
complexes, particularly in the outer shell of the melon,
which otherwise might vary in response to changing
Key words: CT, PET, SPECT, scan, cranium, hearing, echolocation,
lipid density, bottlenose dolphin, Tursiops truncatus.
Structural and functional imaging of bottlenose dolphin (Tursiops truncatus)
Dorian S. Houser1, James Finneran2, Don Carder2, William Van Bonn2, Cynthia Smith2, Carl Hoh3,
Robert Mattrey3and Sam Ridgway2,3,*
1BIOMIMETICA, La Mesa, CA 91942, USA,2Space and Naval Warfare Systems Center, San Diego, CA 92152, USA
and 3School of Medicine, University of California, San Diego, CA 92103, USA
*Author for correspondence (e-mail: firstname.lastname@example.org)
Accepted 22 July 2004
of middle and inner ear into the tympano-periotic complex, the
migration of the bullar complex from the skull, the presence of
air sinuses around the bulla (Dudok van Heel, 1962; Fraser
and Purves, 1960; Ketten, 2000), the presence of phonic lips
(Cranford, 2000; Evans and Prescott, 1962), an isovaleric-rich
fat body in the forehead known as the melon (Varanasi et al.,
1975; Varanasi and Malins, 1971) and hollow lower jaws filled
with acoustic lipids (Varanasi and Malins, 1970a,b) are a few
notable adaptations favoring effective sound utilization in the
ocean. The functional role of these adaptations has been
inferred by assessing the spatial and structural relationship
between anatomic components of the auditory and phonation
system (e.g. Cranford et al., 1996), variation in design relative
to terrestrial species (e.g. Dudok van Heel, 1962; Norris, 1964;
Reysenbach de Haan, 1956), the physiological response of the
system following anatomical manipulation (McCormick et al.,
1970) and the biochemical composition of pertinent structures
(Varanasi et al., 1975). These inferences, considered in relation
to the results of psychoacoustic experiments (e.g. Brill, 1991)
and physiological responses to manipulation of the system,
form the basis for our current understanding of delphinid
hearing and phonation.
The availability of computed tomography (CT) and
magnetic resonance imaging (MRI) devices has stimulated
more investigation to determine relationships between
anatomical structures within the cetacean head by allowing
internal anatomy to be viewed without laborious anatomical
dissection. These imaging modalities have been used with
postmortem specimens to study the brain of the bottlenose
dolphin (Tursiops truncatus) and the white whale
(Delphinapterus leucas; Marino et al., 2001a,b,c) as well as the
in situ auditory anatomy and sound-producing structures of
several cetacean species (Cranford, 1988; Cranford et al.,
1996; Ketten, 1994; Ketten and Wartzok, 1990). As with
necropsy procedures, functional properties of tissues are
inferred from their biochemical composition, morphology and
relationship to other tissues. Unfortunately, postmortem
specimens often have to be frozen and then thawed for
scanning, and such freezing and thawing may produce tissue
distortion and permit the draining of fluids into air cavities with
the breakdown of cell membranes and fracturing of capillaries.
Furthermore, changes that begin after death can produce
changes in tissue density, gas bubble generation from bacteria,
swelling, rigor mortis and other distortions (Mackay, 1966).
Tissue changes following death may therefore lead to spurious
conclusions about tissue function. In vivo measurements made
with CT and MRI can address these issues since such
measurements preclude cavity and tissue deformations and
biochemical changes of tissues that follow death.
Functional information of auditory and sound production
tissues may be obtained through the use of functional
scanning techniques [e.g. single photon emission computed
tomography (SPECT) and positron emission tomography
(PET)]. By following the distribution of administered
radiopharmaceuticals and radionuclides, these scanning
techniques allow certain aspects of the physiology of a subject,
its organs and tissues, to be observed. In conjunction with in
vivo CT and/or MRI measurements, consideration of functional
information can provide a more comprehensive understanding
of tissue function and structure than can be achieved through
postmortem analysis alone.
The current study presents the first CT scans of living
bottlenose dolphins and demonstrates the utility of in vivo
anatomical analyses. It also presents the first functional
scanning of a bottlenose dolphin; both PET and SPECT scans
are used to couple information about cranial blood flow and
metabolism within the dolphin to anatomical information
gained via CT imaging. Results of this study provide new
insight into dolphin anatomy and physiology that are pertinent
to understanding the role of certain anatomical features in both
hearing and echolocation.
Materials and methods
Three bottlenose dolphins (Tursiops truncatus Montagu
1821), two males (WEN and FLP) and one female (CIN), were
used in both structural (CT) and functional (SPECT and PET)
scanning procedures (Table·1). All three animals were trained
to cooperate in the experiments by sliding out of the water and
onto a cushioned mat at the trainer’s signal. Each animal was
trained to remain still once on the mat. Rewards of fish were
given by the trainers for animal cooperation in remaining still
for all procedures. The animals were transported to the
scanning facilities in a covered van and were accompanied by
at least one attending veterinarian as well as the animal’s
trainers. Four to six additional experienced animal care
assistants were also present at all times. On arrival at the scan
facility, dolphins were transferred to a specially created,
padded gurney for movement into the scanner room. All
experiments were conducted in accordance with a protocol
approved by the Institutional Animal Care and Use Committee
of the Navy Marine Mammal Program, Space and Naval
Warfare Systems Center, San Diego, CA, USA as well as the
University of California, San Diego, CA, USA.
Two dolphins (CIN and WEN) were transported to Vital
Imaging of La Jolla, located approximately 12·miles from their
D. S. Houser and others
Table 1. Age and physical attributes of subjects used in structural and functional imaging scans
Animal I.D. Sex Age (years) Mass (kg)Length (cm) Scan type
CT, SPECT, PET
Scanning of bottlenose dolphin cranial anatomy
holding enclosures in San Diego Bay. Each dolphin received
0.3–0.55·mg·kg–1of diazepam to reduce any anxiety attendant
with the scan. X-ray CT was performed using an electron beam
scanner (Imatron, San Francisco, CA, USA) to study the cranial
morphology of the dolphin. Volume acquisition mode was used
to image the entire head. With this mode, X-ray data are acquired
helically by rotating an X-ray source [130·KeV (kilo-electron
volts) at 600·MAS (mAmpSec)] collimated to 3·mm around the
object at 100·ms per revolution. Multiple X-ray projections are
then obtained over a 270° arc while the object is translated
through the gantry at 25·mm·s–1. Each data set (projections
acquired from a single revolution) is used to reconstruct a single
cross-sectional image representing the internal organs located
within a transverse plane that is slightly more than 3·mm thick.
Because the object translated 2.5·mm per revolution, a series of
3·mm-thick images are then made available that are separated
by 2.5·mm. The slight overlap was chosen to produce smooth
three-dimensional (3-D) or multiplanar reconstructions of the
imaged region. Image data were saved in DICOM format and
stored to disk until processed.
SPECT was used to monitor blood flow in the head tissues
of two dolphins. The SPECT scanner utilizes a gamma
camera to acquire gamma rays that are emitted from
radiopharmaceuticals administered to a subject prior to
scanning. Gamma ray photons can be mapped into a two-
dimensional (2-D) space; however, a SPECT camera can
acquire images from multiple angles around the patient so that
a 3-D image of the activity can be reconstructed. Technetium
(99mTc) bicisate is a radiopharmaceutical with a high first pass
blood extraction and slow clearance in brain tissue. This
property makes it useful in the mapping of blood flow since
the relative image intensity in a region of brain tissue reflects
the underlying blood flow to that region. 99mTc-bicisate is
a common diagnostic radiopharmaceutical for vascular
irregularities of the human brain.
Dolphins (WEN and FLP) were administered 99mTc-bicisate
(Syncor International Inc., Pasadena, CA, USA) to determine
the distribution of blood flow within the brain and other soft
tissues of the head. Two hours prior to SPECT imaging, the
dolphins received a 1850·MBq intravenous injection of 99mTc-
bicisate. Subjects were placed quiescent in a quiet, darkened
room for 15·min following injection and were then transported
to the Department of Nuclear Medicine at the University of
California, San Diego Medical Center. Images were acquired
on an ADAC Forte SPECT camera (Milpitas, CA, USA) with
the dolphins placed on a specially engineered bed, allowing
them to be properly cooled with water. The imaging acquisition
consisted of 30·s per stop for a total of 64 angled stops divided
between the two imaging heads. This resulted in a total scan
time of approximately 32·min. After image reconstruction, the
images were converted to the DICOM 3.0 format.
PET was used to estimate the relative metabolism of dolphin
cranial tissues. The PET scanner uses a circular array of
detectors to measure photons produced from positron-emitting
radiopharmaceuticals that have been administered to a subject
prior to scanning. As in SPECT imaging, 3-D images of
radiopharmaceutical distributions can be generated where the
intensity of the image represents the relative concentration of
the radiopharmaceutical accumulated in the tissue. 18F-2-
fluoro-2-deoxyglucose (FDG) is an analog of glucose and is
often used in PET scanning to estimate glucose uptake by
tissues and is commonly used in the detection of cancerous
tissues because of the relatively higher metabolic rate of
cancerous tissue to non-cancerous tissue.
A single dolphin (WEN) was administered 740·MBq of FDG
(Syncor International Inc.) by intravenous injection ~2·h prior to
scanning to map the relative metabolic activity of tissues within
the brain and other soft tissues of the head. As in the SPECT
procedure, the animal was kept in a quiet, darkened room for
40·min post-injection of the ligand. The dolphin was then
transported as outlined above to the Vital Imaging Facility in
Sorrento Valley, CA, where the PET scan took place. Images
were acquired on a Seimens HR+ PET scanner (Knoxville, TN,
USA) with the dolphin on the same specially engineered bed
used in the SPECT scan. A 15-min transmission scan was first
acquired for attenuation correction. The emission scan consisted
of eight frames of 4-min acquisitions to allow for any subject
movement. This resulted in a total scan time of approximately
55·min. The images were converted from the ECAT 7.2 format
to the DICOM 3.0 format for further processing.
Data acquired from all of the imaging modalities were
processed using Analyze 4.0/5.0, created by the Biomedical
Imaging Resource of the Mayo Clinic (Robb, 1999; Robb and
Barillot, 1989; Robb et al., 1989). All data were converted to
AVW format (native Analyze format) and volumes made cubic
(equivalent voxel dimensions) through the use of linear
interpolation. A threshold was applied to data from the CT
scans according to tissue density (represented by X-ray
attenuation in Houndsfield units), and binary representations of
isolated tissues were created and formed into object maps.
Objects were created for the skull, brain, tympano-periotic
complex, surface of the dolphin and air spaces of the sinus
cavities, nasal passages and larynx. Spatial relationships
between structures were observed by visualizing the objects
while suppressing the display of non-objectified tissues. The
volume of air contained in the sinuses and nasal passages was
calculated by multiplying the voxel density of the sinus/nasal
passage object by the calibrated voxel dimensions.
Data from the PET and SPECT scans were co-registered
to CT images to localize regions of metabolically active
tissues and regions of blood flow. Primary registration was
accomplished through application of an automated surface-
matching algorithm within Analyze. This algorithm was
applied to filled binary objects created from extractions of the
brain from both the structural and functional images. Co-
registration was achieved by manually fine-tuning the resulting
transform matrix after application to the
original PET/SPECT and CT image volumes
collected from the same animal. PET and
SPECT data were also mapped to 24-bit RGB
data representations to facilitate visualization
of the image volumes.
Fig.·1 demonstrates the spatial relationship
between the skull and the sinus cavities, nasal
passages and laryngeal airspace. Fig.·2
demonstrates the same relationship but
includes the auditory bulla, brain and spinal
cord and remaining soft tissues of the head.
Note the external landmarks (i.e. eye, mouth
slit and blowhole) for reference of the internal
placement of structures imaged in Fig.·1. Skull
asymmetry is evident, as the midline of the
skull, defined from the rostral bifurcation of
the upper jaw, passes through the right bony
nasal passage (Fig.·1C,D). The nasal passages
and vertex of the skull are shifted left of the
midline, as is typical of odontocete species
(Cranford et al., 1996). Most of the sinuses
and nasal passageways are contiguous,
although small discontinuous pockets of air
were identified. The nasal passages form the
major body of air within the cranium and, in
combination with the contiguous sinus spaces,
comprised an air volume of 267.4·ml in CIN
(Fig.·3A) and 368.7·ml in WEN (Fig.·3B). The inclusion of
distinct air spaces separately compartmentalized from the
contiguous air space, but excluding laryngeal air, increased the
cranial air volume to 290.3·ml and 380.9·ml, respectively.
Utilizing the convention of Fraser and Purves (1960), the
inflated sinus complex was distinguishable as the primary
pterygoid sinus, the mesial and optic lobes of the pterygoid
sinus and a middle ear complex consisting of the middle,
posterior and peribullary sinuses (Fig.·3). The cranial air space
was compartmentalized by the nasal plugs dorsally and the
contracted palatopharyngeus muscle around the tip of the
larynx below. Accessory and vestibular air sacs were not
inflated in WEN, but partial inflation of the pre-maxillary air
sacs was observed in CIN. Air spaces directly abutted the
tympano-periotic complex such that a bone–air interface
existed (Fig.·4). Coverage was most complete on the dorsal,
medial and posterior surfaces of the tympano-periotic complex,
with the dorsal surface being almost completely covered by a
layer of air (Fig.·4A,B). Air coverage of the lateral, ventral and
anterior surfaces of the bulla was less complete; soft tissue
connections are known to occur at these sites.
Uptake of 99mTc-bicisate is indicative of regional blood
D. S. Houser and others
Fig.·1. Spatial and morphologic relationship of the contiguous cranial air space (red) to
the skull (white) of WEN. Panels correspond to the (A) ventral, (B) lateral, (C) anterior
and (D) dorsal views. Discontinuous cranial air spaces, excluding the laryngeal air space
(also in red), are not shown.
Fig.·2. Spatial and morphologic relationship of the contiguous cranial
air space (red) to the skull (white), auditory bulla (yellow), brain and
spinal cord (light brown) and other soft tissues (blue) of the head of
the bottlenose dolphin WEN. Discontinuous cranial air spaces,
excluding the laryngeal air space, are not shown.
Scanning of bottlenose dolphin cranial anatomy
flow, and substantial uptake was noted in the brain, melon and
posterior region of the lower jaw, suggesting extensive blood
flow within these tissues (Fig.·5). Uptake by the melon was
greater than four times that of the blubber and surrounding soft
tissues (based upon the number of counts recorded at each site),
and the maximum intensity within the melon was 196% that
of the maximum intensity measured in the brain. (Caution must
be exercised when interpreting the difference in intensity
Fig.·3. Regional identification of the bony nasal passages and sinus complex (according to Fraser and Purves, 1960) in (A) CIN and (B) WEN.
The objects in the figure represent the actual air space not the tissue boundaries of the air space. Compartmentalization of the cranial air space
results from the constriction of the nasal plug and the palatopharyngeus muscle. NP, nasal passages; PtS, primary pterygoid sinus; PtS OL, optic
lobe of the pterygoid sinus; PtS ML, mesial lobe of the pterygoid sinus; MEC, middle ear complex; PmS, pre-maxillary sac; PaS, constriction
of the palatopharyngeal sphincter.
Fig.·4. Relationship of middle ear complex and other cranial air spaces (red) to the tympano-periotic complex (yellow) in the dolphin WEN.
Views are from the (A) dorsal, (B) ventral and (C) lateral perspectives.
between the melon and brain as resulting from greater blood
flow in the melon than in the brain. 99mTc-bicisate is soluble
in lipid and it is unknown whether the lipid composition of the
melon results in a disproportionate uptake of 99mTc-bicisate
relative to the brain for the same rate of blood flow.)
Distribution of ligand in the region of the melon was greatest
in the dorsoanterior portion of the melon, forming an almost
shield-like vascularization that followed the forehead contour
(Fig.·6). The greatest amount of ligand uptake in the dorsal
region of the melon was immediately sub-dermal while the
greatest uptake in the anterior portion of the melon was
approximately 4.5·cm subdermal, posterior to the junction of
the forehead and rostrum. This region presumably contains an
increase in connective tissue proliferation, as has been
observed in other odontocete species (Cranford et al., 1996).
Three PET scans were taken of subject WEN; however, the
field of view (FOV) was incapable of capturing both the
complete melon and brain within the same scan. The uptake of
FDG was demonstratively greater within the brain than in any
other tissue whereas little to no uptake of FDG was observed
in portions of the melon that were within the scan FOV
(Fig.·7). Uptake was observed in the region of the peribullary,
middle and posterior sinuses and appeared to be consistent with
the passage of neural fibers from the brain to the ears (Fig.·8).
The melon is a structure rich in short- and medium-chain
fatty acids, particularly isovaleric acid, which is preferentially
accumulated relative to its distribution in the blubber (Varanasi
and Malins, 1971). The distribution of lipid species throughout
the melon is heterogeneous and, because variations in the ratio
of wax esters to triacylglycerols alter ultrasonic sound speeds
(Varanasi et al., 1975), presumably contributes to the melon’s
ability to collimate outgoing echolocation clicks. The lower
jaws of the dolphin are hollow and thin, with a particularly thin
area, known as the ‘pan’, existing at the posterolateral region
of the jaw. Similar to the melon, the mandibular canals are also
filled with fat bodies, rich in isovaleric acid, which extend from
D. S. Houser and others
Fig.·5. Multiple views of regional 99mTc-bicisate uptake in the dolphin WEN. The degree of uptake is directly related to the intensity of the
region. Greatest uptake occurs in the brain, melon and bilaterally in the posterior region of the lower jaw. (A) Dorsally, uptake in the brain and
melon are apparent. (B) Laterally, the melon (left), brain (top-center) and posterior region of the lower jaw (right) are apparent. (C) Ventrally,
uptake in the lower jaw is notable bilaterally.
Fig.·7. Sagittal midline section
from the dolphin PET series
displaying substantial uptake of
FDG within the brain and nominal
uptake by the melon (lighter, more
intense regions correspond to
greater uptake). The PET scan
image was taken from the dolphin
Fig.·6. Sagittal midline view of 99mTc-bicisate uptake in the melon
and brain of the dolphin WEN. Uptake of 99mTc-bicisate increases as
the color scale progresses from blue to red. Greatest uptake occurs in
the frontal region of the melon, suggesting that blood flow across the
melon is distributed dorsally and anteriorly.
Scanning of bottlenose dolphin cranial anatomy
the posterior of the jaw to make contact with the periotic
complex (Varanasi and Malins, 1970b, 1971). The distribution
of 99mTc-bicisate is indicative of perfusion to both the melon
and fat bodies in the posterior region of the lower jaw, but lack
of uptake of FDG suggests that the melon and fat bodies of the
lower posterior jaw are not metabolically active structures. The
latter finding is not that surprising given that fat bodies tend to
be relatively metabolically inert and that their function as
collimator or wave guide is primarily derived from their lipid
It has been proposed that sound refraction can be altered in
porpoises by small variations in the chemical composition of
the melon, which subsequently impact sound speed through the
melon (Varanasi et al., 1975). Variations in ultrasonic speeds
of the inner core (1273–1376·m·s–1) and outer shell
(~1682·m·s–1) of the melon of the bottlenose dolphin support
this notion (Norris and Harvey, 1974). Similarly, temperature-
regulated variations in lipid density should affect the bulk
modulus and shear modulus of the melon and fat bodies of the
lower jaw as well as the sound speed through these tissues.
Sound speed measured through the melon of a deceased
dolphin was inversely related to temperature of the melon
(Fitzgerald, 1999), and although those sound speed
measurements are not likely to be equivalent to measurements
recorded in a living animal, the trend will probably be the
Variation in blood flow in response to changing water
temperatures may stabilize thermal gradients within the lipid
complex of the melon and jaw fats by varying heat availability
to these regions. Preservation of thermal gradients within the
melon appears particularly feasible given the greater
distribution of blood flow over the dorsoanterior portion of the
melon, a region that is in close contact with water. A
temperature change in the outer shell would alter the sound
speed gradient between the outer shell and core of the melon
and affect the propagation of echolocation clicks. If no
mechanism existed to control the temperature-dependent sound
speed gradient of the melon, dolphins experiencing variation
in water temperatures would also experience a potentially
problematic variation in the collimation of outgoing
echolocation clicks. Thus, the ability to stabilize the
temperature of the melon would be useful in preserving click
propagation characteristics and would be advantageous to
dolphin species that inhabit environments with seasonal or
regional variations in water temperature.
Ligamentous suspension of the bulla provides for acoustic
isolation of the ears from the skull (Fraser and Purves, 1960;
Ketten and Wartzok, 1990; Reysenbach de Haan, 1956).
Similarly, the presence of air around the bulla contributes to
acoustic isolation of the ears by providing a sound-reflective
barrier between them. The almost complete dorsomedial
coverage of the bulla with air should contribute to the animal’s
ability to differentiate time of arrival differences by impeding
conduction through soft tissues that exist between the ears. In
combination with other air spaces in the head, this should allow
dolphins to capitalize on spectral differences in received
signals due to shadowing and may contribute to minimum
auditory angular resolution in the vertical and horizontal planes
(Popper, 1980; Purves and Van Utrecht, 1963; Renaud and
Popper, 1975). Position, geometry and volume of the air spaces
within the head of the dolphin are important components of
both the sound production and reception process and care
should be given to their properties when developing models of
biosonar production and hearing in dolphins (e.g. Aroyan,
Anatomical evidence supports the notion that echolocation
clicks are generated by the phonic lips (Cranford et al., 1996;
Evans and Prescott, 1962) that lie just superior to the nasal
plug. The dorsal and medial air coverage of the bulla, nasal
cavity air, the laterally projecting air-filled pterygoid sinuses,
and the skull of the dolphin protect the ear from the production
of echolocation clicks by acting as acoustic reflectors in the
direct path to the ears. However, isolation of the bulla is not
complete, as auditory-evoked potentials are elicited in response
to a dolphin’s own echolocation clicks and have been elicited
by transmitting synthetic clicks into the melon of a dolphin
Fig.·8. Representation of co-registered and fused PET and CT scans taken from WEN. Uptake of FDG increases as the color scale progresses
from blue to red. The brain is the predominant uptake site of FDG, but distributed uptake occurs throughout the peribullary, middle and posterior
sinuses. From left to right, sequential images start with a midsaggital section and progress laterally to the right of the animal. Metabolic activity
is notable within the ear cavities lying ventrolateral to the brain.
(Bullock and Ridgway, 1972; Supin et al., 2003). For projected
clicks, the magnitude of the evoked response is ~20·dB less
than that obtained by projecting a click through the lower jaw,
which is commonly believed to be the primary receive channel
for echoes returning from objects ensonified by a dolphin’s
biosonar pulses (Brill, 1991; McCormick et al., 1970).
As depth of diving increases, the increasing hydrostatic
pressure diminishes the inspired air volume in accordance with
Boyle’s Law. Thus, air within the cranial air spaces will reduce
in volume with increasing depth of diving (Ridgway et al.,
1969). The internal carotid artery of T. truncatus (and other
delphinoids) runs into the middle ear and terminates in the
corpus cavernosum carotidis, which is thought to be an erectile
tissue (Purves, 1966; Ridgway, 1968). Distension of the corpus
cavernosum presumably occurs during diving and reduces the
air volume of the sinus space. Purves and Van Utrecht (1963)
found that a thin layer of crystallized salt existed around the
ossicles of demineralized specimens of T. truncatus, even
though the corpus cavernosum was apparently engorged to its
fullest extent. It therefore appears that, at full distension, the
corpus cavernosum and peribullar plexus surrounding the
middle ear permit the presence of a thin layer of air.
Functionally, this would maintain acoustic isolation of the ears
at depth. Additionally, some amount of air may be required to
permit mechanical motion of ear components (e.g. round
window movement; McCormick et al., 1970).
The nasal passages imaged in the dolphins were
compartmentalized by closure of the nasal plug dorsally and
constriction of the palatopharyngeus around the tip of the
larynx below. The nasal passages are connected to the air
sinuses of the head via the Eustachian tube. This air is
required to drive the pneumatic click source through
pressurization of the nasal cavity (Ridgway et al., 1980).
While diving, there is an approximate 0.1·MPa increase in
pressure for every 10·m that the dolphin dives, and the
volume of air within the sinus and nasal air space will decline
in proportion to increasing air pressure. Volume reductions
in this air space should impact the ability to generate
echolocation pulses, thus requiring a mechanism to replenish
the air volume and ensure that a pressure differential across
the phonic lips can be maintained. Under diving conditions,
the palatopharyngeus may mediate exchange between air in
the nasal passages and sinuses and air in the lung (Ridgway
et al., 1980). Lung collapse obviates alveolar gas exchange
at ~70·m depth (Ridgway and Howard, 1979), but movement
of air from the lung, bronchi and trachea into the nasal
passages and sinus cavities may compensate for a reduction
in air volume within those anatomical spaces.
Given that a critical volume of air is likely to be required for
click and whistle production and for acoustic isolation of the
ears, a theoretical maximum dive depth at which echolocation
pulse generation and hearing capability are maintained relative
to near-surface functionality can be predicted. Lung volumes
between 7 and 11·liters have been estimated for the bottlenose
dolphin (Ridgway et al., 1969). Assuming a lung volume of
9·liters, and using the calculated air volume of the sinuses and
nasal passages within the dolphin WEN, a maximum dive depth
at which both echolocation and hearing capabilities are
preserved relative to near-surface functionality can be estimated
through the application of Boyle’s Law. Further assuming that
the nominal amount of air required to preserve echolocation and
hearing functionality is equivalent to the volume of air
measured in the sinuses and nasal passages at the surface, the
maximum depth at which functionality is preserved in the
dolphin WEN is calculated to be ~236·m, or 2.5·MPa of
pressure. Depending on the technique used, the lung volumes
of bottlenose dolphins have been estimated to range from 49 to
71·ml·kg–1(Irving et al., 1941; Ridgway et al., 1969) and
probably demonstrate an isometric relationship with mass
similar to that observed in terrestrial mammals (Schmidt-
Nielsen, 1984; Kooyman, 1973). If so, then it seems reasonable
that dolphins with larger masses would have a greater depth of
diving at which echolocation remains possible, providing them
with potential advantages to foraging at depth.
The maximum depth of functional echolocation estimated
for WEN is underestimated if the nasal passages are the only
cavities requiring air for pressurization of the pneumatic click
source, i.e. the sinus space may be diminished to the maximum
extent possible through complete distention of the corpus
cavernosum and vascular spaces lining the pterygoid sinuses.
A reduction in the amount of air required for click generation
and hearing will increase the theoretical depth limit at which
these functions are preserved. Similarly, if the total lung
volume is underestimated, then the maximum depth of normal
functionality will also be underestimated. Support for a lesser
air volume requirement or greater gas store exists in the
observed echolocation of dolphins to depths of up to 300·m
(Ridgway et al., 1969). Nevertheless, a maximum depth should
exist at which echolocation ceases to be feasible due to a
reduction in the volume of gas inspired prior to descent.
In the present study, recent anatomical and physiological
data from bottlenose dolphins that were collected with
structural and functional biomedical imaging modalities have
provided new insight into the internal anatomy of the head,
relative to the cranial air spaces, and identified extensive blood
flow in relatively metabolically inert fat bodies. Both of these
findings have ramifications to the understanding of dolphin
hearing and echolocation. Air in the sinuses and nasal passages
is likely to contribute to the hearing capability of the dolphin
while simultaneously providing the gas necessary to power the
pneumatic source of biosonar pulses. It is speculated that a
reduction in the volume of this air that occurs during descent
of a dive is replenished by the passage of lung air into the nasal
passages via the palatopharyngeus muscle. Blood flow over the
melon and within the posterior regions of the lower jaw is
speculated to function as a thermoregulatory control of lipid
density. Thermal regulation of lipid density within both the
melon and jaw fats should maintain sound speed gradients
within these fatty channels, thus preserving the wave guide
action of these sound projection and reception pathways.
D. S. Houser and others
3665 Download full-text
Scanning of bottlenose dolphin cranial anatomy
The authors would like to thank J. Corbeil and the staff of
Vital Imaging and the Department of Nuclear Medicine at the
University of California, San Diego Medical Center for their
assistance in performing scans. The authors would also like to
thank the Biomedical Imaging Resource of the Mayo Clinic,
Rochester for their assistance with ANALYZE, and the
animal care and training staff of the Space and Naval Warfare
Systems Center for their assistance in the training, transport
and care of the subjects WEN, CIN and FLP.
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