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| Enlarge ImageREADY TO SCAN—Postdoctoral Investigator Soraya Moein Bartol and Senior Research Assistant Scott Cramer position an Atlantic white-sided dolphin, which stranded and died, on the WHOI CT scanner bed before imaging, while CT technologist Julie Arruda (front) examines previously generated images. (Photo by Tom Kleindinst, WHOI.) |
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| Enlarge ImageINTERNAL EARS—A 3-D image generated from a CT scan highlights selected tissue groups of a bottlenose dolphin’s head. It shows the relationships of the exterior skin (blue), brain (pink), inner ear bones (red), and specialized auditory fats (orange). The fats form paired lobes inside the head along the jaw and are very similar in shape to the outer ear flaps (pinnae) of bats. (Courtesy of Darlene Ketten, WHOI) |
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| Enlarge ImageVISIBLE HEARING—This 3-D CT scan image of a blue whale’s inner ear (18 millimeters in diameter) shows typical mammalian inner ear structure, including a spiral cochlea and the vestibular system that controls balance. (Courtesy of Darlene Ketten, WHOI) |
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| Enlarge ImageA SECRET SEEN—This 3-D image shows an intact, near-term fetus discovered inside an Atlantic white-sided dolphin that stranded and died. The fetus’s flippers are folded and its ribs are lightly mineralized, but the cross-section reveals fully matured ears. (Courtesy of Darlene Ketten, WHOI) |
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| Enlarge ImageRARE VIEW—CT scan of an entire Kogia (pygmy sperm whale) illustrates the advantages of this instrument. It reveals the skin and outer structure (including fins), and the fully articulated skeleton in its normal configuration, from any selected perspective, without cutting into the specimen. (Courtesy of Darlene Ketten, WHOI) |
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| Enlarge ImageCLOSE TO HER WORK—Wearing fisherman’s cold-water gear, Darlene Ketten (left) stands in the mouth of a stranded humpback whale towed ashore on a Newfoundland beach in 1998. Working as quickly as possible, she and Jon Lien of St. John’s University, Newfoundland, remove biopsy samples and the inner ears to determine if it was injured by nearby explosions for a construction project. (Courtesy of Darlene Ketten, WHOI) |
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Related Multimedia |
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MEGALITHIC TO MINIATURE
The WHOI CT scanner is a unique resource for scientists studying internal structures in animals. Both marine and terrestrial animals have been scanned to let scientists “look inside.” |
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By Darlene Ketten, Senior Scientist
Biology Department
and Kate Madin, Science Writer
Woods Hole Oceanographic Institution On summer nights, if you sit quietly at the edge of a field or watch
the edges of the light pools around street lamps, you will see bats
swooping through shadowy darkness in search of moths or other flying
prey. They detect and catch their targets through echolocation, or
biosonar, the animal equivalent—and precursor—to man-made sonars.
Bats generate signals in their nose and throat that produce echoes,
which the bats monitor to determine the size, shape, speed, and
direction of their prey, as well as any other objects in the area.
Biosonar is also how they navigate in dark caves. Bats' large,
distinctive, convoluted, and mobile ear flaps are critical for the
fine-grain acoustic analysis they do during echolocation.
Now flood that field with seawater and make it not only dark, but
profoundly deep and filled with a myriad of exotic creatures and
objects. That is the dim and complex world in which whales live.
Although whales and dolphins are air-breathing mammals, they spend
approximately 85 percent of their time submerged. Compared to sound,
light does not penetrate water well, and it is not surprising that
whales and dolphins rely primarily on hearing and sound rather than
sight to sense their environment and communicate. The Odontoceti—toothed
dolphins and whales that hunt fish, squid, and other prey—evolved
parallel abilities with bats, actively using clicks and pulsed sounds
for underwater echolocation.
However, there is one very striking difference between bats and
dolphins. The latter appear to have no outer ears. Dolphins and whales
abandoned external ears as a concession to better underwater mobility.
Still, they do have ears buried inside their heads: fascinating ears in
fact, with exceptional range that operate at extraordinary depths.
With the help of a common medical tool—biomedical computerized
tomography, more commonly known as CT and MRI scanning—we are beginning
to get inside the heads of whales and dolphins. Using biomedical
imaging techniques, we can thoroughly explore just how their ears are
constructed—and see how and what they hear.
Into the inner ear
Whale hearing is difficult to study by conventional methods. Whales are
large, elusive, diverse creatures, and research on most species is
substantially restricted because of their endangered status. One
approach to learning how whales hear is by reverse engineering, which
is essentially the clockmaker’s child approach to science. We can
examine stranded animals to determine not only what may have caused
their deaths, but also, literally, what makes them tick.
Virtually all mammals have the same three basic ear components: an
external ear flap, or pinna, is connected via an ear canal to the
middle ear cavity, which has an eardrum and bony lever system for
amplifying sounds, and then an inner ear, which transduces sounds into
neural impulses. In marine mammals such as seals and otters, the pinnae
are reduced to allow them to swim faster; in whales and dolphins, the
sleekest and fastest of marine mammals, these outer ears are gone
completely.
Traditionally, investigating the inner workings of whales and dolphins
has been done by dissection. But to examine the parts, you are
compelled to disassemble the relationship of those parts, which is
fundamental to understanding their effective operation. Even worse,
conventional dissection requires time, especially when the subject
outweighs you by several hundred pounds. By the time you can get to
many structures, they have deteriorated beyond recognition.
We knew there are robust, complex inner ears buried deep in dolphin and
whale heads, but we did not know how sound gets into those inner ears.
Seeding an innovative idea
At WHOI, we took a different approach, or rather, we updated the
traditional one. We still dissect, but our dissections are digital.
Biomedical scanning rapidly and non-invasively reveals in great detail
the internal structure of the object or animal that is imaged. We can
use imaging techniques to see into most living animals. To image rare
and deep-ocean materials, we do not need to remove them from their
protective containers.
Above all, we see the synergy of the structures. For ill or stranded
animals, we can locate and examine pathologies or traumas
non-invasively—precisely what scanners were designed to do for humans.
The idea of using a CT scanner to probe inside marine mammals was a
radical idea a decade ago. In 1998, with funding from the Andrew W.
Mellon Independent Study Award program at WHOI and from The Seaver
Institute, the first large-scale study of marine mammal auditory
systems using computerized tomography was undertaken using CT and MRI
scanners in area hospitals. This study demonstrated the extraordinary
potential of scanning for marine mammal research, since it allowed
high-resolution anatomical surveys of many individual animals in an
unprecedentedly short time.
In 2000, the Office of Naval Research (ONR), and particularly Admiral
Paul Gaffney, former Chief of Naval Research, furthered the effort by
providing start-up funds to install a high-capacity CT scanner at WHOI
that was dedicated exclusively to marine research.
How CT scanners work
CT scanners use X-rays to produce an image of density differences of
internal structures. The denser an object, the less X-ray energy is
transmitted to the detector, and the brighter the object in the image.
For this reason, bone appears white, air looks black, and soft tissues
are varying shades of gray in an X-ray.
In common single plane X-rays, such as chest films, the detector is a
sheet of film that is exposed by a single pulse from the X-ray tube.
Consequently, the output is a flat image in which one structure
overlays another.
CT scanners employ a bank of electronic detectors that monitor the
X-ray attenuations from multiple pulses and positions, as the X-ray
tube moves through an arc around a patient or specimen. This complex,
multi-dimensional matrix of attentuations is then deconvolved to
generate images that represent the attenuations in thin cross-sections.
It is, in a very real sense, a virtual dissection, slice by slice, of
all structures. The WHOI scanner allows us to image slices as thin as
0.1 millimeters and to detect attenuation differences that are several
thousand-fold.
Using scanning techniques to look at whale and dolphin ears, we can
study the geometry and composition of ears and other head tissues from
microscale to macroscale and thereby gain insights into what and how
they hear. We also see sometimes how they were damaged.
The impacts of sound
Sound is energy. The louder a sound an animal can hear, the greater the
potential for damage to its ear. Some loss of hearing from day-to-day
wear and tear is normal; some is excessive and avoidable, as far too
many of us are well aware from exposure to loud music, power tools, or
other intense sound sources.
However, just to complicate matters, not every sound is equally
dangerous to all ears. Because different species have different hearing
capacities, what is imperceptible to one animal may be annoying or even
harmful to another. An ultrasonic dog whistle is imperceptible to
humans but clearly heard by any normal dog or cat.
Even more important, the effects of sound can range from the physical,
with actual damage to parts of the auditory system, to behavioral:
sounds so disturbing that animals abandon normal activity, such as
feeding and breeding, or even alter their migration paths.
Both physical and behavioral effects potentially have serious impacts
on individuals or on entire species. Consequently, understanding
hearing in marine mammals is not just a matter of curiosity, but
fundamental for marine conservation and possibly even for the survival
of some species.
Ships, sonars, and strandings
The ocean is a naturally noisy place. Sounds are generated by
vulcanism, wind, waves, seismic events, and by animals themselves.
However, all human activities in or near the water are adding to this
natural suite of oceanic sound.
In recent years, mass strandings of whales—in Greece in 1995, the
Bahamas in 2000, and the Canary Islands in 2002—have focused attention
on the possible effects of man-made sound in the oceans. In those
cases, multiple U.S. and NATO ships were engaged in exercises employing
multiple and intense sonars in narrow straits.
While the presence of these ships and the exceptional sound field
produced by the exercises clearly coincided with the strandings, we are
not yet able to determine exactly what mechanism led to them. We
examined many of the stranded animals using our scanner system and
found distinctive traumas, but the damage is not strictly acoustic.
Rather, it appears to be more consistent with stress than directly
sound-induced.
In other cases, however, we have found damage to ears, often from aging
or long-term noise exposures that clearly impaired the animals’ hearing
and therefore their ability to function in the wild. At this point, we
do not know precisely what noises are most harmful, either directly or
indirectly, to any marine mammal species, but this is a critical area
of research that we must pursue intensely and rapidly.
The inside story of dolphin ears
One of our first major discoveries answered the original mystery of the
missing external ear: Without external pinnae and no obvious canal, how
does sound enter dolphins’ heads and how does it get to the inner ear?
Researchers had speculated that since dolphin inner ear bones were
located near their jaws, perhaps the soft tissues and bone of the jaw
played a role. Unfortunately, that was hard to prove because fat tissue
in the area deteriorated rapidly, and the relationships between tissues
were disrupted as soon as they were cut during dissections.
CT scanning gave us the first undisturbed images of this region. In
fact, it provided the critical clues: The fatty lobes near the jaw were
connected to the ear and had shapes similar to bat pinnae. In effect,
bats and dolphins seem to have parallel ear evolution. Dolphins have
pinnae that are just as complex and large as bats, but they are
internal—an advantage under water both hydrodynamically and
functionally; these specialized fats have acoustic properties similar
to seawater. Consequently, in terms of both shape and physics of sound
in water, they are the aquatic analog of land mammal outer ears that
were designed to capture and conduct air-borne sound.
The speed of sound in water
Scanning also allowed us to measure the locations of dolphin ears in
situ, which explained why the ears are spread so far apart in dolphin
heads. Dolphin ears are widely separated to accommodate the speed of
sound in water, which is 4.5 times faster than in air.
One clue to determining the location of a sound source is the
difference in arrival time between your ears. Humans have trouble
locating sound sources under water, because, acoustically, our heads
"shrink" nearly five-fold because of the increased speed of sound
through water. As dolphins evolved, they expanded their heads and
inter-ear distances to match sound speeds in water, which explains
their extraordinary ability to localize sound sources three times
better than humans.
Scanning also provided the first data on the inner ear of the true
behemoths of the oceans. Blue and fin whale ears are massive. Their
inner ear bones are approximately the size of a human brain case and
are at least twice as dense. To demineralize these ear bones in order
to dissect them by traditional methods would take more than two years.
With scanning, we can digitally slice them to see inner ear features in
less than one hour.
Anatomy reveals hearing capacity
Although all mammal ears have the same basic parts, there are important
differences among species in some structures that account for
differences in their hearing capacities. No two species have exactly
the same hearing ability. Different animals can detect different
frequency ranges and have different sensitivities at any one frequency.
Most mammals hear frequencies well above the range of human hearing,
termed ultrasonics. Some also hear well at very low frequencies, even
at seismic sounds generated by earthquakes.
To study both normal and abnormal hearing, our laboratory has used the
scanner to image all parts of the auditory system of more than 30
species of marine mammals. Each ear from an unknown hearer is compared
with those from species with well-documented hearing characteristics.
In particular, we construct “maps” of the stiffness and mass of ear
components of animals whose frequency ranges are known and compare the
stiffness and mass of newly imaged marine mammal ears to calculate
their resonant frequencies. Thus, we can determine the critical
commonalities for hearing in all mammals—as well as critical
differences for specialized hearing like echolocation and for hearing
under water instead of in air.
We also make maps this way for the few species of marine mammals for
which hearing has been tested. These are our model controls, as our
maps are consistent with audiograms or hearing curves of the tested
animals. The new ear maps from untested species have led to the
discovery that whales have some of the widest hearing ranges of any
mammal and that some species are capable of hearing at seismic or
hyper-ultrasonic frequencies.
We now know that some species of whales have a 12-octave hearing range,
compared to eight in humans. Some whales hear well down to 16 hertz (or
cycles per second), versus our lower limit of 50 hertz, while others
hear as high as 200 kilohertz. The typical human high-frequency cutoff
for humans is 16 kilohertz. For bats, it is 60 to 70 kilohertz.
This work is coordinated also with other WHOI laboratories doing basic
research on marine mammal sounds, diving, and foraging behaviors, as
well as applied research on acoustic devices to warn highly endangered
species of impending ship strikes. So far, we know there is no single
sound bite that is perceptible or harmful to all marine creatures, but
with luck, we may be able soon to provide guidelines that will help
preserve some of them.
CT scan menagerie
Peering into whale heads—without the loss of tissue and time
that normal dissections cause—was the initial motivation for
using a CT scanner for marine mammal research, but our current scanner
has had more than its share of other types of species and objects. Some
of the specimens scanned here, particularly to assist the work of other
researchers, have been remarkable.
Scan data obtained at the WHOI facility have proven invaluable for
investigating everything from diagnosing sinus infections in live,
sneezing seals to imaging shark balance organs, coral reef fish swim
bladders, flippers of all forms, fractures in great whale jaws, coral
reef growth patterns, pressurized ocean sediment cores, and, most
exotic of all, the complex mineral substructure of deep-ocean chimneys.
Animals as small as grass shrimp have been scanned to assist modelers
to determine how much sound energy large groups of similar
invertebrates, called krill, reflect at different frequencies.
Acoustical oceanographers use such models to determine whether
reflected signals at sea actually represent deep layers of millions of
krill in patches throughout the oceans.
Land creatures that also have been scanned in the last two years
include tigers, hedgehogs, bats, and even an elephant and a
hippopotamus (parts only—they are just a tad too big for a
whole one to fit on the table).
In 2005, the scanner is scheduled to move into a new facility on the
WHOI Quisset campus. Moving the scanner is not trivial; in fact, the
scanner has a good deal in common with the megalithic money on Yap.
Both are giant toroids that, once in place, are daunting to shift.
The scanner move will require two engineers, a rigging crew of up to
six workers, and two weeks of disassembly and reassembly time. Still,
the effort will be worth it, as the new facility incorporates overhead
hoists and tracks connecting the scanner room with surgical and storage
facilities that will allow us to transport, scan, and understand an
even wider range of marine creatures that may come our way. |
Posted: April 19, 2005 [top] |
