Hearing deficits measured in some Tursiops truncatus,
and discovery of a deaf/mute dolphin
Sam H. Ridgway and Donald A. Carder
Biosciences Division, Naval Command, Control and Ocean Surveillance Center, RDT&E Division,
Code D3503B, 49620 Beluga Road, Room 200, San Diego, California 92152-6266
~Received 22 April 1996; accepted for publication 14 June 1996!
Eight bottlenose dolphins Tursiops truncatus ~four male, four female! were trained to respond to
100-ms tones. Three male dolphins ~ages 23, 26, and 34! exhibited hearing disability at four higher
frequencies—70, 80, 100, and 120 kHz even at 111–135 dB re:1 mPa. Two females ~ages 32 and
35! responded to all frequencies as did a male ~age 7! and a female ~age 11!. One female ~age 33!
responded to all tones at 80 kHz and below; however, she failed to respond at 100 or 120 kHz. One
young female dolphin ~age 9! exhibited no perception of sound to behavioral or electrophysiological
tests. This young female was not only deaf, but mute. The dolphin was monitored periodically by
hydrophone and daily by trainers ~by ear in air! for 7 years until she was age 16. The animal never
whistled or made echolocation pulses or made burst pulse sounds as other dolphins do.
@S0001-4966~97!02812-9#
PACS numbers: 43.80.Lb, 43.80.Ka, 43.80.Jz @FD#
INTRODUCTION
Audiograms have been done on several species of the
cetacean superfamily Delphinoidea ~Au, 1993; Richardson,
1995!. Most of these species are represented by only one or
two young animals. All of these animals, with the exception
of one killer whale, Orcinus orca ~Hall and Johnson, 1971!,
had good sensitivity from 60–120 kHz. The first detailed
audiogram of the bottlenose dolphin, Tursiops truncatus,
yielded a threshold of 42 dB re: 1 mPa ~10214 W m2! at 60
kHz with about a 20-dB increase at 120 kHz and a very steep
increase thereafter, to a maximum of 150 kHz ~Johnson,
1967!. Johnson’s animal was 9 years old.
During an acoustic response time task ~Ridgway et al.,
1991!, we tested the hearing of eight Tursiops ~four males,
four females! at levels that were expected to be 60–80 dB
above threshold, based on earlier delphinoid audiograms
mentioned above. One of our experimental dolphins, a male
aged 26, had been tested 13 years earlier by Ljungblad et al.
~1982!. The animal had been shown to have good hearing at
this earlier date. Although this dolphin ~IAY!, at age 13 in
the early 1980s, had thresholds 5–10 dB higher than the
male age 9 used by Johnson ~1967!, Au ~1993! has pointed
out that this difference could possibly be accounted for, in
part at least, by the differences in test methodology.
Until we first presented this at the Denver meeting of the
Acoustical Society ~Ridgway and Carder, 1993a!, no tests of
hearing had been done with older ~.25 years! dolphins of
either sex. During the past 33 years with the Navy marine
mammal program, we have observed sound production and
some related behavior in about 200 bottlenose dolphins ~cf.
Ridgway, 1983!. Recently, we had the opportunity for the
first time to observe a dolphin that was both deaf and mute.
I. MATERIALS AND METHODS
Age and sex of each of the experimental dolphins are
given in Fig. 1. The oldest male was age 34 at the time of the
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J. Acoust. Soc. Am. 101 (1), January 1997
test and had been with our laboratory since 1962. During the
1960s and 1970s, he had demonstrated apparent good hearing and echolocation ability, although an audiogram had
never been done. Health and medication records were kept
on all the dolphins since their initial acquisition or birth.
Among the animals we tested, records on animal MAU, for
example, go back to 1962. The potential for ototoxicity has
always been a consideration for dolphin medication, however, two of the animals had received aminoglycosides
~Anon, 1994! for infections. Animal MAY was given gentamycin ~600 mg twice daily! for seven days in 1980, six years
prior to the hearing tests. Dolphin SLA was given one injection of penicillin/streptomycin in 1968 and a single injection
of amakacin and penicillin G in 1992.
The dolphins listed in Fig. 1 were trained to whistle or
burst pulse when a stimulus tone ~St! was delivered through
an underwater hydrophone located 1 m in front of the animal. This training was similar to that reported previously
~Ridgway and Carder, 1988; Ridgway et al., 1991!. We noticed that when a dolphin whistled, there was a characteristic
movement along the left posterior margin of the nasal plug
of the closed blowhole. Burst pulse sounds generally resulted
in a somewhat different movement, more to the right side of
the dolphin’s blowhole. Our trainers quickly induced dolphins to repeat vocalizations by tapping with a finger or manipulating the area of the blowhole where movement or any
escaping air concurrent with sound had been detected. After
whistles or burst pulse sounds were reliably elicited in this
manner, the signal was transferred slowly to a simple stroke
to the dolphin’s melon. Then, with the dolphin underwater in
front of the trainer, the melon stroke was paired with a tone
until the animal reliably gave the vocalization each time the
tone was presented through the hydrophone.
The animals were trained to station on a plastic bite
plate 1.0 m underwater and remain stationary until an underwater buzzer ~bridge or S2 signal that informs the animal
that a fish reward will soon follow! was sounded. Initially,
590
FIG. 1. The animal identifier, sex, age, and indication of correct responses
to 100-ms, 111-dB tones for eight bottlenose dolphins Tursiops truncatus
employed in this study.
the dolphin was given an S2 and rewarded each time it vocalized after a tone. Gradually the reward schedule was reduced until the animal made up to 20 responses in a row. The
S2 was given immediately after the last correct vocal response in the series. The S2 was followed by a reward of one
to several fish when the dolphin returned to the surface to
breathe. The longest period the animal was required to remain on the underwater station was two minutes; however,
both the time the animal was required to remain on the underwater station, and the number of tones presented during
this time were varied in a random fashion. For catch ~no
stimulus! trials, the dolphins were sent down to the station
but no tones were presented. After the dolphin had remained
stationary and silent for periods varying between 30 and 120
s, the S2 was given and the animal surfaced for reward.
Improper responses, i.e., leaving the station before the S2,
vocalizing prior to or in the absence of the stimulus, or giving the wrong vocalization, were not reinforced with fish.
A trial series or testing dive ~TD! was started when the
trainer signaled the animal to go down to the plastic bite
plate 1.0 m under the surface ~Fig. 2!, and 1.0 m from the
stimulus hydrophone ~an F42B for frequencies of 5–70 kHz;
an LC-10 for frequencies of 80–120 kHz!. During the earlier
stages of training, 20% of the TDs were catch trials which
were inserted randomly in the series of TDs. When the false
alarm rate decreased to 5% or less of the correct response
level, catch trials were reduced to 10% of TDs.
Tone stimulus ~St! duration was 100 ms with a 2-ms
gradual rise in intensity at onset and decline on termination.
The findings of Johnson ~1968! suggested to us that this
duration was adequate. With three of the older males, some
tests were done with 300- and 450-ms tones. Frequencies
were 5, 10, 20, 40, 50, 60, 70, 80, 100, and 120 kHz. Stimuli
were 111 dB, increasing in 6-dB steps to 135 dB in cases
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FIG. 2. Responses of two bottlenose dolphins to high-frequency tones.
Points ~circles with dot! for Salty at age 9 from Johnson ~1967!, points
~filled circles! for IAY at age 13 from Ljungblad et al. ~1982!. All triangles
from present study.
where the animal did not respond to the baseline level. With
the dolphin at 1.0-m depth and 1 m from the St hydrophone
~Fig. 2!, the trainer waited a variable period then pushed a
switch starting a randomly variable St block. The computer
selected Sts from a file in random initial delay and interval
~1.1–2.1 s in 0.1-s steps! and offered Sts via a St generator as
long as the trainer held the switch button down. Thus, the
trainer could give several Sts in a row in the randomly variable sequence from the computer file, then let up on the
switch and interpose a period without Sts before pressing the
switch again for more Sts. Randomness in St delivery was
maintained both by the computer program and by the trainer’s switch press out of sight of the dolphin. Animal responses ~ARs5whistle or burst pulse! were received by another hydrophone, digitized, and stored for confirmation of
correct response. Each AR file with 20–200 Sts was edited
on a CRT display of a 700-ms St window. No-AR trials,
noisy trials, and wrong ARs were identified, and a database
was constructed. The baseline stimulus of 111 dB re: 1 mPa
generally exceeded background noise in San Diego Bay by
about 50–80 dB in the 60–120 kHz range ~also see Au et al.,
1985!.
In addition to attempts at applying the above procedures,
the apparently deaf dolphin SIB was trained to respond to a
45-kHz underwater locating beacon1 ~model DK355L!, a
‘‘pinger’’ that was lowered into the water. The source level
of the pinger was 160 dB re: 1 mPa and it produced one
10-ms pulse each second. After the animal had learned to
take fish from the trainer’s hand, the pinger was dipped into
the water and the animal was rewarded for approaching it.
S. H. Ridgway and D. A. Carder: Dolphin hearing deficits
591
Gradually, the animal came to the pinger whenever it was
put into the water.
Further, hearing of SIB was tested by evoked potential
audiometry ~Ridgway et al., 1981!. Tones and clicks at various intensities, repetition rates, and durations were presented
via the same hydrophones mentioned above and positioned
both 1 m in front of the animal and adjacent to the lower jaw,
or attached by suction cup to the lower jaw ~Moore et al.,
1995!.
II. RESULTS
A. Responses of eight hearing dolphins of various
ages
Results were obtained from the eight dolphins at various
frequencies between 5 and 120 kHz ~Fig. 1!. At the baseline
level of 111 dB re: 1 mPa, all dolphins responded at better
than 90% correct responses to frequencies of 5, 10, 20, 40,
and 50 kHz, with the exception of one old male, MAU, that
dropped to just over 50% at 50 kHz, 111 dB. The results at
frequencies of 60, 70, 80, 100, and 120 kHz varied considerably between the different animals. One female and three
male dolphins under age 20 at the time of testing and two
females over the age of 30 demonstrated a capability for
responding to all the frequencies at a correct response rate
over 90%, and most over 95%. All of the males over age 23
showed varying degrees of inability to respond to tones of 60
kHz, and above.
The degree of hearing deficit with respect to frequency
varied somewhat in the three old males and the one old female that demonstrated a hearing deficit. One male, IAY,
responded consistently to tones of 60 kHz but responded to
no tones of 70 kHz, and higher even when St duration was
increased to 450 ms. The single old female that demonstrated
a hearing deficit, dolphin SLA, also had a sharp hearing cutoff but at a higher frequency of 100 kHz. Two older males
had a more gradual or incomplete hearing deficit. At 70 kHz,
MKA responded to .75% at 135 dB and .50% at 129 dB
but was ,5% at 111 dB. At 80, 100, and 120 kHz, his
correct response level dropped to less than 5% ~near false
alarm rate! at all intensities under 135 dB re: 1 mPa, and at
this level his correct performance was just under 25%. Correct response level was not increased significantly when tone
duration was extended to 300 ms.
Figure 2 shows thresholds at the higher frequencies of a
male dolphin age 9 ~Salty! studied by Johnson ~1967! compared with IAY at age 13 ~Ljungblad et al., 1982!, and our
findings on IAY at age 26 when the dolphin failed to respond
to tones 40–50 dB above his threshold established by Ljungblad et al. ~1982! 13 years earlier.
B. Behavioral observations of the deaf dolphin (SIB)
The first unusual behavior was noticed soon after SIB
was brought to our facility in San Diego Bay. We noticed
that when SIB was apparently asleep, she adopted a posture
that was different from any dolphin we had ever observed.
We called this a ‘‘spar buoy’’ posture since the dolphin’s
rostrum was pointed straight overhead, and its tail hung
straight down as the animal bobbed in the water.
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Most dolphins in our program are trained to respond to a
pinger or other acoustic device. This facilitates movement of
animals around our dolphin pod complexes, and the pinger is
used as a recall device when the animals are released in the
bay or in the open sea. During initial training, soon after the
dolphin was collected in the Mississippi Sound in 1984, SIB
along with six other dolphins in her group appeared to respond normally when the pinger was dipped into the water.
After the task was moved into the open bay, when SIB was
away from other dolphins, and, especially as the distance
over which the dolphin was required to respond was increased, trainers began to suspect that SIB was relying on
vision instead of hearing the sound of the 45-kHz pinger.
When SIB was separated from other dolphins in the group,
and the pinger was inserted in such a way that the dolphin
could not see the action, she did not respond.
C. Other tests of hearing and sound production for
SIB
Next, our trainers tried to elicit sound from SIB by the
methods mentioned above. Neither whistles or burst pulse
sounds could be elicited. The only sounds made by SIB were
low Bronx cheer like sounds as the nasal plug fluttered during forced exhalations through a partially open blowhole.
We had noticed that when dolphins are separated from
their group, they sometimes increase the rate of vocalization,
especially the production of whistles. Twice, SIB was placed
in a portable netting enclosure 53433 m and slowly moved
away from the group in San Diego Bay. Sound was monitored continuously by hydrophones ~B&K 8103 with a B&K
charge amplifier, and a Racal tape recorder with a frequency
response at least as high as 150 kHz! for 3 h during each
period of separation. No whistles, burst pulses, or echolocation pulses were recorded.
Finally, we attempted the electrophysiological approach
which we have applied in the past to screen hearing in more
than a dozen dolphins ~Seeley et al., 1976; Ridgway, 1980;
Ridgway et al., 1981!. With both tone and click presentations from 1–120 kHz from hydrophones attached to the
lower jaw, near the lower jaw, or in the water in front of the
dolphin, no auditory evoked potentials were obtained, even
to stimuli as high as 141 dB re: 1 mPa.
III. DISCUSSION AND CONCLUSIONS
Humans underwater can hear very high frequency tones
by bone conduction ~Deatherage et al., 1954; MacKay,
1984!, but there is no pitch discrimination above 15 or 20
kHz or above that person’s hearing range. It would be interesting to know if the two older male dolphins, MAU and
MKA, that showed some responses to the highest intensity
tones ~135 dB!, retained any pitch discrimination at the frequencies from 60–120 kHz.
Although two out of four of our dolphins with hearing
deficits had been treated with aminoglycosides for infections
during their many years with our program, the short course
of treatment, and the presence of normal kidney function as
S. H. Ridgway and D. A. Carder: Dolphin hearing deficits
592
indicated by clinical screens, suggest to us that such treatment did not cause the high-frequency hearing loss we observed.
Because a high percentage of the human population
~males more than females! show hearing loss with age ~Ries,
1982!, it should not be surprising that other mammals share
this deficit. Although our older dolphins with high-frequency
hearing loss produce echolocation pulses, we have not studied them in echolocation tasks. We suspect that echolocation
requiring fine discrimination in the presence of noise would
be degraded. Au ~1993! has shown that in Kaneohe Bay,
where background noise in the 20–100 kHz range is dominated by snapping shrimp, dolphins shift their echolocation
click peak frequency above 100 kHz. Our old dolphins with
high-frequency hearing deficits would likely be at a disadvantage in such an environment.
For our old dolphins, survival is not dependent on the
use of echolocation in the sea. Tursiops do survive in the
wild to advanced ages. One extreme example of a female
estimated to be age 52 has been reported ~Scott et al., 1996!.
We suspect that high-frequency hearing loss may well be a
consequence of dolphin aging in the wild as well.
Although dolphin hearing and echolocation characteristics have received much more attention than other sensory
abilities ~cf. Au, 1993!, Tursiops has good vision, some
chemoreception, and good tactile senses ~Nachtigall, 1986!.
The sense of touch is especially well developed ~Ridgway
and Carder, 1993b!. After we determined that SIB was deaf,
it became apparent from observing the dolphin’s behavior
that she had become adept at employing the other dolphins in
the group to derive information that the others all received
by the acoustic sense. For example, when the recall pinger
was placed in the water, she probably became immediately
aware of it by observing the behavior of other dolphins. Only
when SIB was removed from the immediate presence of
other dolphins, and the pinger insertion hidden from view,
did we determine that the dolphin could not hear the pings.
When SIB was collected from the Mississippi Sound
~Cat Island near Gulfport, MS! in 1984, she was a robust and
apparently healthy animal within the weight range expected
for the population ~Ridgway and Fenner, 1982!, We suspect
SIB was able to survive, and maintain good nutrition not
only by using senses other than audition, but by observing
other dolphins. The mutual survival benefits of dolphin
schools have been discussed by several authors ~Norris and
Dohl, 1980; Connor and Norris, 1982; Bradbury, 1986; Würsig, 1986!.
We showed that dolphin calves produce echolocation
pulses by about 60 days of age ~Carder and Ridgway, 1984!;
however, we have recorded shrill whistles from calves within
ten minutes after birth. Because SIB produced none of the
usual dolphin sounds, we suspect that she may have developed deafness near or even before birth.
We do not know whether the unique ‘‘spar buoy’’ resting and sleeping posture of SIB was related to deafness or
vestibular dysfunction. We noted this unusual behavior at the
outset; however, we did not immediately suspect deafness.
We now surmise that the unusual posture may have been
related to the deaf and mute condition. Among the possible
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causes for her condition are infections. Severe infections can
damage the vestibular system as well as the cochlea. A generalized infection affecting the cranium and nasal sinuses
such as meningitis could result in such damage. When these
dolphins with hearing loss die, histologic examination may
shed light on the cause of this deafness.
ACKNOWLEDGMENTS
We thank Tricia Kamolnick who was in charge of all the
dolphin training for our high-frequency response experiments. William Root of San Diego State University designed
our computer programs and Michelle Reddy assisted with
manuscript preparation. Whitlow Au, Ted Cranford, Bernd
Würsig, and Patrick Moore made helpful suggestions concerning the manuscript. This work was supported in part by
the Office of Naval Research.
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