Hearing measurements from a stranded infant Risso's dolphin, Grampus griseus
Marine Mammal Research Program, Hawaii Institute of Marine Biology, University of Hawaii, PO Box 1106, Kailua, HI 96734, USA
* Author for correspondence (e-mail: myuen{at}hawaii.edu)
Accepted 8 September 2005
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Summary |
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Key words: Risso's dolphin, Grampus griseus, hearing, audiogram, auditory threshold, auditory evoked potential, AEP, envelope following response, EFR, sinusoidally amplitude-modulated tone-burst, SAM
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Introduction |
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Given the importance of the melon for echolocation and acoustic propagation
(Cranford et al., 1996;
Norris, 1968
), the furrow has
been thought to be important for directional propagation of outgoing
echolocation pulses (Philips et al.,
2003
). Although the initial attempts to demonstrate echolocation
behaviorally with a stranded and rehabilitated Risso's dolphin were met with
some difficulty (Nachtigall et al.,
1995
; Philips et al.,
2003
), another Risso's dolphin was eventually trained to
successfully discriminate an aluminum cylinder from a nylon sphere while
wearing blindfolding eyecups (Philips et
al., 2003
). In the previous audiometric work, the clicks emitted
by the dolphin were acquired at mean amplitudes of 193 dB (re. 1 µPa) with
estimated sources levels up to 216 dB (re. 1 µPa; 1 m). Clicks were
predominantly double-peaked with substantial energy at higher frequencies,
some as high as 105 kHz. These findings were particularly interesting given
that previous work which behaviorally measured hearing thresholds with this
same animal subject had shown that the animal could only hear tones with
frequencies higher than 80 kHz when projected at high amplitudes
(Nachtigall et al., 1995
).
The echolocating Risso's dolphin in the 2003 study was a wild-captured
older animal (Philips et al.,
2003). Her lower teeth had been naturally worn down before she was
brought into the laboratory and she was estimated to be over 30 years old. The
range of her high-frequency hearing did not reach to the 150 kHz region, as
seen in other odontocetes (Nachtigall et
al., 2000
), and it was assumed at that time that the species
G. griseus did not hear high frequencies as well as other dolphins.
However, Ridgway and Carder
(1997
) have demonstrated
individual differences in high-frequency hearing in bottlenose dolphins. Four
of eight bottlenose dolphins they studied showed high-frequency hearing
deficits and most appeared to be age related. Older bottlenose dolphins appear
to lose their high-frequency hearing in a manner similar to other mammals,
including humans. Given that the one Risso's dolphin originally tested by
Nachtigall et al. (1995
) was
an older animal, it seems likely that the demonstrated hearing capability of
this individual may not be representative of the species' hearing range.
|
Most odontocete audiograms measured to date have been collected using
behavioral psychophysical procedures in which the animal was kept within a
laboratory setting and trained to respond to the presence or absence of pure
tone stimuli. These measurements are ideally made in quiet laboratory tank
environments but are occasionally made at oceanaria, in sea pens or in
concrete or above-ground tanks. While the quiet laboratory environment is the
ideal baseline setting for determining hearing thresholds, the normal
psychophysical behavioral procedures are expensive and time consuming. This
tends to limit the number of individuals for which audiograms may be obtained.
Auditory evoked potential (AEP) experiments, in which the animal's hearing is
measured by passively receiving the animal's electric potential responses from
the surface of the skin over its head when in the presence of sound stimuli,
provides an opportunity to increase the number of odontocete audiometric
measurements. AEP measurements have been made with stranded dolphins in
rehabilitation facilities (Andre et al.,
2003; Popov and Klishin,
1998
) without prior animal training. A stranded animal
rehabilitation facility also provides an appropriate setting for identifying
hearing deficits that may be caused by overexposure to anthropogenic sound.
Recent increased concern about animals and ocean noise provides ample
motivation for testing the hearing of stranded marine mammals, especially if
the stranded animals are suspected of having been overexposed to noise.
The current study involved an infant Risso's dolphin (G. griseus) that was rescued on the Algarve coast in Southern Portugal. The animal was taken to the Mundo Aquatico Rehabilitation Facility of ZooMarine in Guia, Albufeira. During rehabilitation, the animal's audiogram was measured using the AEP envelope following response (EFR) procedure to estimate hearing thresholds between 4 and 150 kHz.
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Materials and methods |
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Tank and background noise levels
Under the care of the veterinary staff, the Risso's dolphin was housed in a
rehabilitation holding tank. The concrete tank was approximately 3 m deep with
a 5 m inside diameter, and it contained an artificial seawater to a depth of
1.1 m. The tank pumps and filters were turned off at least 15 min before each
session to eliminate air bubbles and to reduce background noise. The tank was
lined with canvas-covered foam pads that prevented the calf from bumping into
the concrete sides and also served to dampen spurious reflections. Ambient
noise level measurements were performed within the pool to determine
background noise levels. However, ambient noise proved to be exceedingly low,
below the sensitivity of the acoustic recording equipment (less than 65 dB re.
1 µPa2 Hz-1 measured across a 40 kHz bandwidth).
Similar low noise situations are a valuable situation for conducting absolute
hearing thresholds (sensu Au et al.,
2002).
The animal's position and sounds received
The animal was held so that its head was 0.5 m from the center of the tank,
1 m from the projecting hydrophone, and held in place by the experimenter
(Fig. 2). By placing a
calibrated Biomon 8261 (sensitivity 182-185 dB and frequency response up to
200 kHz) hydrophone (Santa Barbara, CA, USA) near the dolphin's lower jaw
while the dolphin was in the correct position, both of the projecting
hydrophones were calibrated to determine the received levels before the data
were collected. The size of the infant's head was very small, and when the
calibrated hydrophone was moved around the animal, there was no measurable
variation in received levels around the subject's head. Pure-tones were
created with a Wavetek function generator for the following frequencies: 4,
5.6, 8, 11.2, 16, 22.5, 32, 40, 50, 64, 70, 80, 90, 100, 110, 120 and 150 kHz.
Each of these pure-tone sine waves was transmitted in the tank and the
received peak-to-peak voltage (Vp-p) was measured with the
calibrated hydrophone. This Vp-p was converted to
peak-equivalent root-mean-square voltage (peRMS) by subtracting 9 dB. The
peRMS was taken as the RMS voltage and used to calculate the sound pressure
level (SPL) for that frequency. The spectrum of the received signals was
viewed with a Techtronix TDS 1002 oscilloscope (Beaverton, OR, USA), ensuring
that there were no competing reflections produced from other signals or
reflections in the tank. In this environment, there were no constructing or
destructing interferences observed with the transmitted signal. Had these
sorts of interferences been present in the tank, they would have been apparent
in the pure-tone case, but, even if they had been present, these sorts of
interferences would have been countered by the use of short sinusoidally
amplitude modulated (SAM) tone-bursts.
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Sounds presented to the animal
The acoustic stimuli were SAM tone-bursts created from each pure-tone
carrier frequency for which a threshold was desired. SAM tone-bursts were
presented rather than pure tones because they are optimal for producing clear
AEPs as EFR. The tone-bursts were digitally synthesized with a customized
LabView data acquisition program that was created with a National Instruments
PCI-MIO-16E-1 DAQ card (Austin, TX, USA) implemented into a desktop computer
(Fig. 3). Each of 1000 SAM
tone-bursts was 20 ms long, with an update rate of 200 kHz for carrier tones
less than 70 kHz, and 500 kHz for carrier frequencies equal to or above 70
kHz. The carrier frequencies were modulated at a rate of 1000 Hz, with a
modulation depth of 100%. This modulation rate was chosen based on ideal
measurement modulation rates for similar odontocetes
(Dolphin et al., 1995). A 30 ms
break of no sound was alternated between the 20 ms stimulus presentations. The
stimuli were sent from the computer to a custom-built signal shaping box that
could attenuate the tone-bursts in 1 dB steps. A Techtronix TDS 1002
oscilloscope was used to monitor the outgoing stimuli from the signal shaping
box to the projecting hydrophones.
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AEP measurements taken from the animal when sounds were produced
Rubber suction cups containing gold sensors to pick up the evoked
potentials were easily placed on the animal at the beginning of each session
by the experimenter. Standard conductive gel was used to assure a good
connection between the animal's skin and the 10 mm EEG gold electrodes (West
Warwick, RI, USA). The active electrode was attached 3-4 cm behind the
blowhole, slightly off to the right and over the brain, while the reference
electrode was attached on the back near the dorsal fin. The animal was easily
held at the surface with most of its head underwater
(Fig. 2) to receive sound input
through the major tissue routes to the ears
(Mohl et al., 1999
;
Ketten, 1997
) while the suction
cups, with the embedded electrodes, remained in the air.
An Iso-Dam Isolated Biological Amplifier (Sarasota, FL, USA) amplified the AEP responses from the electrodes by 10 000. The Iso-Dam, as well as a Krohn-Hite Filter Model 3103 (Brockton, MA, USA) with a band pass of 300-3000 Hz, filtered the responses for anti-aliasing protection. The amplified and filtered responses were transferred to an analog input of the same DAQ card in the same desktop computer. The received signal was digitized at a rate of 16 kHz in order to extract the recorded AEP from noise, and the entire trial for each stimulus presentation lasted about 1 min.
Threshold determination
The general procedure used to estimate a hearing threshold for each
frequency was to select a carrier frequency to be modulated, determine the
initial intensity level to be used for that frequency and then present a
series of trials with progressively decreasing stimulus amplitudes. Because
this was the first audiogram of a neonate Risso's dolphin, stimulus
presentation levels were based on a previously published audiogram of an adult
Risso's dolphin (Nachtigall et al.,
1995) and a bottlenose dolphin
(Johnson, 1966
). Stimulus
levels began 20-30 dB above the lowest threshold levels of the preceding
audiograms. Eighteen carrier frequencies were tested ranging from 4 to 150
kHz. The following frequencies were first tested based on the previous Risso's
audiogram: 4, 5.6, 8, 11.2, 16, 22.5, 32, 40, 50, 64, 76, 80, 90, 100, 110
kHz, however it became immediately obvious that the animal heard relatively
well at the highest of these frequencies and therefore an additional three
frequencies, 108, 128 and 150 kHz, were successively added. The initial levels
for these three frequencies were determined by starting 20-30 dB above the
previously obtained threshold. The amplitudes of the transmitted SAM
tone-bursts were reduced in 5-10 dB steps until the amplified evoked potential
responses to the SAM bursts could no longer be distinguished from the
background noise. Step size was based on the intensity of the signal and the
animal's neurological response. An average of nine stimulus intensity levels
was presented for each of the 18 different frequencies. The stimuli were
initially calibrated at each frequency tested using continuous pure-tones at
the position of the animal's head. The received peak-to-peak levels (V) of the
stimuli were measured and used to calculate peRMS (V) and received SPL. These
values were taken as the received level of each stimulus frequency.
When presenting the SAM stimuli, the values were converted to RMS (V) to determine the equivalent received level when presented in SAM tones.
Data analysis
The data obtained for each frequency for each intensity level was an evoked
potential record comprised of at least 1000 averaged evoked responses to the
20 ms SAM and the first 10 ms of the 30 ms quiet interval as depicted in
Fig. 4. Fourier transforms were
calculated for a 16 ms window (shown in
Fig. 4) of the average evoked
response recorded at each intensity level for each frequency in order to
quantitatively estimate the animal's hearing threshold
(Fig. 5). This window contained
a whole number of response cycles to the stimulus. The 256-point Fast Fourier
transforms (FFT) provided response frequency spectra of the data where a peak
reflected energy received, or the animal's physiological following response,
to the 1000 Hz modulation rate. Thus, a larger EFR response was reflected as a
higher peak value. The peak FFT amplitude at the modulation rate was used to
estimate the magnitude of the response evoked by the SAM stimulus.
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Results |
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In determining threshold values, these EFRs were Fourier transformed (FFT) to obtain the frequency spectrum of the animal's evoked response (Fig. 5). The consistent peak at 1000 Hz reflected the animal's EFR, and thus neurophysiological `following' of the carrier tone modulated at an 1000 Hz rate. The strength of the evoked response was reflected in the amplitude of the peak at the modulation frequency; as stimulus level was decreased, the peak amplitude decreased correspondingly. Fig. 5 illustrates a typical peak at 76 kHz carrier frequency that decreases as the stimulus intensity is attenuated. At the lowest stimulus intensity of 55 dB, the peak of the response spectra was no different from the background physiological noise. The intensity of each of the spectrum peaks was plotted as a function of stimulus SPL, and regression lines were drawn to calculate the theoretical zero response value. Therefore, for a stimulus of 76 kHz, the threshold may be seen to be estimated in Fig. 5 to be 55 dB.
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The AEP audiogram's general shape was a typical mammalian -shape
(Fig. 7). At high frequencies,
the slope of thresholds increased steeply beyond 90 kHz at a rate of 95 dB
octave-1. Below 32 kHz, the slope of increasing thresholds was more
gradual, at 16.4 dB octave-1. Poorest sensitivity was measured at
the very low and very high frequencies, 100.3 dB at 4 kHz and 116.9 dB at 150
kHz, respectively. There was an apparent notch in the audiogram at 40 kHz.
Compared with the previously determined behavioral audiogram, the AEP
audiogram was similar in shape. However, the frequency region with the lowest
thresholds, figuratively forming the bottom of the -shape in the AEP
audiogram, was not flat as in the 1995 audiogram, but rather this current
audiogram had a saw-toothed up-and-down shape in the areas of best
sensitivity, similar to those typically seen in odontocetes
(Nachtigall et al., 2000
). The
current AEP audiogram revealed lower thresholds at high frequencies and
conversely higher thresholds at lower frequencies than previously seen in the
Risso's dolphin. Note that the best sensitivity measured in the current work
was 20 dB lower than reported by Nachtigall et al.
(1995
).
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Discussion |
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The data collected from the older animal subject were obtained from a
wild-caught animal tested in the natural environment of Kaneohe Bay of the
island of Oahu, Hawaii. Ambient noise power density plotted in 1 Hz bands
(Nachtigall et al., 1995)
showed that it was likely that the thresholds from the Risso's dolphin were
not absolute thresholds but were instead masked by the ambient noise
conditions. The lowest intensity levels detected by the older animal were
65 dB between 8 and 32 kHz, while the lowest intensity levels heard by
the current infant animal were below 50 dB at much higher frequencies. The
data from this infant were collected in essentially quiet conditions. It
seemed likely that the absolute levels of hearing reported in the two
audiograms were not directly comparable because of the differences in the
background noise conditions under which the different data were obtained.
There was also an obvious difference in the methods for hearing
measurements used in the two investigations. The 1995 audiogram from the older
Risso's dolphin was measured using a standard psychophysical procedure in
which the animal was trained to behaviorally report the presence or absence of
a pure-tone stimulus. The animal was trained to respond, or `go', when a 3 s
tone was presented and to not respond, or `not go', when no signal was
presented. Conversely, the data from this infant dolphin were collected using
AEP procedures that measured the brainstem's EFR to a SAM tone-burst only 20
ms long. Recent work comparing these two procedures
(Yuen et al., 2005) indicated
that odontocete AEP thresholds may be higher than thresholds gathered with the
psychophysical behavioral procedure due to the fact that the AEP stimuli are
much shorter than the assumed Risso's dolphin temporal integration time
(Johnson, 1966
). By contrast,
most behavioral audiograms are based on stimuli that are one or two seconds
long, providing ample time for temporal integration, and thus provide lower
thresholds.
While the AEP procedure usually produces less-sensitive threshold
measurements, this threshold and stimulus duration relationship was reversed
when comparing the 1995 and present Risso's dolphins' audiograms at the
frequencies above 20 kHz. The AEP study with the young animal produced lower
thresholds than the previous Risso's dolphin behavioral study with the older
animal. The other striking difference between the audiograms of the young and
old Risso's dolphins was the difference in the range of high-frequency
hearing. While the older Risso's dolphin heard relatively well, for example 74
dB threshold at 80 kHz, it heard quite poorly at the likely unmasked frequency
of 100 kHz with a threshold of 124 dB. When those thresholds were compared
with the current infant's thresholds of 54 dB at 80 kHz, 50 dB at 90 kHz and
66 dB at 108 kHz, the audiogram of this infant animal included lower,
more-sensitive hearing thresholds. This difference might be explained by the
age differences and the occurrence of presbycusis in older animals.
Presbycusis is the reduction in sensitivity at higher frequencies and the loss
of hearing at very high frequencies with increasing age. Ridgway and Carder
(1997) found that bottlenose
dolphins showed age-related hearing loss, especially with higher frequencies,
in a manner similar to many other mammalian species. The difference in the
infant Risso's dolphin's ability to hear high frequencies may have resulted
from the age difference of the two subjects tested. It is likely that not only
was the older animal in the 1995 study masked by the noise of Kaneohe Bay, but
it probably also suffered from high-frequency hearing loss associated with
age. This finding supports the idea that the previously reported audiogram for
a single older Risso's dolphin probably underestimated the best hearing
sensitivity for this species.
The older animal did show lower behavioral thresholds than the younger
animal's AEP thresholds for frequencies below 20 kHz. Unmasked behavioral
hearing measurements of Pseudorca crassidens, another globicephalinid
odontocete, at similar frequencies (Thomas
et al., 1988) are quite similar to those measured for the older
Risso's in Kaneohe Bay. The older Risso's thresholds below 20 kHz are above
the Bay noise levels (Nachtigall et al.,
1995
) and may, in fact, represent typical Risso's hearing for
lower frequencies. Thus, the elevated thresholds shown for the younger
Risso's, here in a quiet environment for frequencies below 20 kHz, may
represent the simple methodological difference between measurements taken with
short AEP signals and longer behavioral stimuli
(Yuen et al., 2005
).
Another interesting feature of the peak sensitivity range of the infant's
audiogram is that the shape of the audiogram nicely matches the center
frequencies of the Risso's dolphin click structure noted in both laboratory
(Philips et al., 2003) and
field (Madsen et al., 2004
)
studies of Risso's echolocation. The center or peak frequencies of the clicks
most often fell in the 30-100 kHz range, which is the same range of peak
sensitivity shown in the infant Risso's audiogram. The click data from the
echolocation studies showed frequencies that were high in comparison with the
1995 older Risso's data but fit very well with the new data. There is,
therefore, a very nice match between the frequency emphasis of the biosonar
signals in the wild and the frequency range of best hearing in the young
animal with presumed normal hearing.
It was also notable that this infant Risso's dolphin heard quite well at
higher frequencies, with a threshold of 116.9 dB at 150 kHz. When compared
with other odontocete species, the auditory sensitivity of this animal at that
frequency is comparable with thresholds measured from the harbor porpoise,
Phocoena phocoena (Kastelein et
al., 2002), the striped dolphin, Stenella coeruleoalba
(Kastelein et al., 2003
), and
the bottlenosed dolphin, Tursiops truncatus
(Johnson, 1966
;
Au et al., 2002
). However, when
this infant Risso's audiogram is compared with the only other audiogram
collected from another species representing the same subfamily, the false
killer whale measured by Thomas et al.
(1988
), an interesting
difference once again may be noted. The false killer whale's high-frequency
cut-off occurred just above 100 kHz, not at 150 kHz as was found with the
infant Risso's dolphin. Although Thomas et al. assumed the hearing of their
measured adult false killer whale was normal, it seems likely, based on this
experience measuring a very young Risso's dolphin, that further measurements
of other young false killer whales (and other young members of that subfamily,
including pilot whales and melonheaded whales) might also show good
high-frequency hearing up to 150 kHz, as has been shown in the other
odontocete species.
Given the recent odontocete strandings associated with intense sound, it seems reasonable to diagnostically test the hearing of stranded dolphins and whales that may have been exposed to loud noise. Traditionally, animal psychophysical audiograms have taken years to train and to complete. This audiogram of the infant Risso's dolphin was gathered over 4 days and was partially obtained in order to diagnostically ascertain that this infant Risso's dolphin did not have hearing damage due to possible overexposure to intense sound. This animal heard high-frequency sounds (above 100 kHz) much better than anticipated. If, however, assumptions about normal hearing had been made by examining the peak frequencies measured from the biosonar of wild Risso's dolphins, the high-frequency hearing would have been predicted. Future diagnostic examinations of the hearing of stranded odontocetes might benefit from considering the center and peak frequencies of the recorded echolocation signals. In this case, they were a better predictor of the high-frequency components of the audiogram of a young Risso's dolphin than was the measured audiogram of an older Risso's dolphin.
Of the >83 species of whales and dolphins in existence
(Rice, 1998), audiograms have
been measured for only 12 species. The electrophysiological AEP procedure of
measuring the hearing thresholds of stranded odontocetes is a reasonable
approach for both diagnostically testing individual animals and for expanding
our knowledge base and scientific evidence of the hearing characteristics of
cetaceans. This work is the first published complete audiogram on a neonate
marine mammal, demonstrating that AEP audiograms are particularly efficient in
collecting hearing information on untrained animals, notably infants and
stranded individuals.
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Acknowledgments |
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