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First published online March 16, 2007
Journal of Experimental Biology 210, 1116-1122 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02734
Polar bear Ursus maritimus hearing measured with auditory evoked potentials
1 Marine Mammal Research Program, Hawaii Institute of Marine Biology,
University of Hawaii, HI, USA
2 Institute of Ecology and Evolution of the Russian Academy of Sciences,
Moscow, Russia
3 Kolmården Djurpark, Kolmården, Sweden
4 National Marine Fisheries Service, Pacific Islands Regional Office,
Honolulu, HI, USA
* Author for correspondence (e-mail: nachtiga{at}hawaii.edu)
Accepted 25 January 2007
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Summary |
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Key words: bear hearing, polar bear, evoked potential
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Introduction |
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; National
Research Council, 2000;
National Research Council,
2003; National Research
Council, 2005) has prompted a great deal of work on the hearing of
aquatic and semi-aquatic mammalian species
(Au et al., 2000;
Wartzok and Ketten, 1999;
Richardson et al., 1995;
Tyack et al., 2006;
Nachtigall et al., 2005). The
polar bear Ursus maritimus is the only bear species classified as a
marine mammal (Rice, 1998),
but there has been no audiometric examination of their hearing. According to
the most comprehensive review of animal hearing studies
(Fay, 1988), and a search of
the literature published since, in fact no measurements have been completed on
the hearing of any bear.
One way to estimate the hearing of a species is to examine the calls of its
prey and its response to those calls. Ringed seals Phoca hispida and
bearded seals Erignathus barbatus are prominent in the diet of polar
bears (Stirling, 2002). In
some areas, the predator–prey relationship between ringed seals and
polar bears is so interrelated that a count of the population of one of them
can indicate the population level of the other (Stirling and Øritsland,
1995). Polar bears' preferred prey items are the newborn pups and subadults
(Stirling and McEwan, 1975),
and they primarily hunt seals in areas of moving pack ice, which include known
important locations of seal birth lairs
(Smith, 1980).
Four types of vocalizations made by ringed seals can be heard at all times
of day in the Arctic spring: (1) low-pitched barks, (2) high pitched yelps,
(3) low and high pitched growls and (4) short descending chirps
(Stirling, 1973). Sonograms of
the recorded sounds indicated that most of the energy was relatively low
frequency below 2 kHz, with some harmonics up to 8 kHz.
The behavioral responses of polar bears to the calls of ringed seals
recorded under water and then presented to the bears in air were measured
(Cushing et al., 1988), and
elicited similar responses from two recently captured bears. The bears erected
their ears, lifted their heads, visually scanned the room and then began
sniffing. As the ringed seal calls continued to be played the bears became
active, paced their cage, groaned and chuffed, then pawed and chewed at their
cage bars. All of these behaviors were observed only rarely in the baseline
behavioral examinations prior to the presentation of ringed seal sounds,
indicating that the bears responded to their primary prey's underwater
vocalizations, presented in air, in a manner that indicated some importance of
in-air hearing in detecting and locating their under-ice prey. Cushing's
observations suggest that if polar bears could hear the underwater
vocalizations of the ringed seals they might use seal vocalizations as a
method to locate their favorite prey. It has also been noted
(Stirling and Thomas, 2003)
that the distinct trills of bearded seals might also provide a prominent cue
for polar bear localization of these animals. A measurement of bear hearing
would assist in the quantification of this sensory system during foraging
behavior.
Polar bears are distributed throughout the Arctic in 19 populations,
comprising an estimated total of 20 000–25 000 bears
(Marine Mammal Commission,
2006). There is increasing concern now over the effects of climate
changes and human activities in the Arctic on current polar bear populations
(Amstrup, 1993;
Schrope, 2001). In particular,
human activity may potentially impact the behavior of polar bears through the
introduction of sound into an environment in which, until recently,
anthropogenic noise was almost completely absent
(Stirling, 1990). The effects
of anthropogenic noise can best be predicted if a baseline of bear hearing
capabilities is first established, and this requires hearing measurement.
The hearing of large marine mammals has typically been measured with
trained captive animals using psychophysical techniques
(Nachtigall et al., 2000).
Polar bears are large and aggressive, even in controlled environments, so
traditional behavioral audiometry is difficult to perform. Therefore,
obtaining data on the hearing capabilities of polar bears presents a
challenge. There have been a number of recent measurements of large mammal
hearing using auditory evoked potential (AEP) audiometry
(Supin et al., 2001;
Yuen et al., 2005;
Nachtigall et al., 2005) and
this technique is used in the present study to determine the hearing
sensitivity of polar bears. This AEP procedure can be used successfully, even
when animals are anesthetized, so when three polar bears had to be
anesthetized for veterinary examination in Kolmården Djurpark (Sweden),
we used the opportunity to examine their ability to hear in air.
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Materials and methods |
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Experimental, facilities, procedure, and anesthesia
During experimentation, each animal was isolated in an indoor secure
enclosure and was anaesthetized by using a combination of
Zalopine® (medetomidin-HCl, 10 mg ml–1; Orion
Pharma, Orion Corp., Espoo, Finland), 3.5–5 mg total initial dose per
animal, and Zoletil® forte vet (tiletamin-HCl+zolazepam-HCl,
Virbac S.A. BP 27, 06511 Carros CEDEX, France), 350–600 mg total initial
dose per animal, delivered with a 3 ml blowdart (Dan-Inject ApS, Sellerup
Skovvej 116, DK-7080 Børkop, Denmark) into the lower front leg.
Combinations of these drugs are successfully used to anesthetize and
temporarily immobilize a variety of large mammals, including grizzly bears
(Reynolds and Verhoef, 2000),
brown bears, gray wolves (Arnemo,
2006) and koalas (Unwin,
2004). Their effects on mammalian hearing per se have not
been previously established.
Background noise monitoring
Ideally audiometry is conducted within very low-noise background conditions
like those found in a sound-proof booth. As is common with most marine mammal
hearing studies (Nachtigall et al.,
2000; Kastak et al.,
2005) these conditions were unavailable and therefore all the
measurements were carried out in a background of low ambient noise. Control of
background noise level was handled by monitoring and noise was measured next
to the animal's head using a Bruel and Kjaer 2231 sound level meter
(Nærum, Denmark) within a frequency range of 0.125–32 kHz. In
order to estimate the noise spectral compositions, 100-ms samples of the noise
taken from the analog output of the sound level meter were digitized at a
sampling rate of 64 kHz by a DAQ-6062E data acquisition card (National
Instruments,
http://www.ni.com)
installed in a standard laptop computer, stored in computer memory, and
Fourier-transformed off-line.
Stimuli
The sound stimuli to be heard and measured were short tone pips of a
carrier sinusoid frequency enveloped by a one-cycle cosine function
(Fig. 1A) specifically designed
to optimize hearing measures using auditory evoked potentials. The carrier
frequencies varied from 1 to 22.5 kHz by half-octave steps, i.e. 1, 1.4, 2,
2.8, 4, 5.6, 8, 11.2, 16 and 22.5 kHz. The envelope cycle duration was 5.6
times longer than the carrier cycle but was not longer than 2 ms. The
frequency spectrum of this waveform is presented in
Fig. 1B. With the used envelope
duration, the pip frequency bandwidth (at a level of 0.5 of the spectrum
magnitude, i.e. –6 dB) in octave measure was
log2[(1+1/5.6)/(1–1/5.6)]=0.52, i.e. almost exactly a
half-octave, except for the pips of the lowest frequencies (1–2 kHz),
which were 2 ms long and, respectively, ±0.5 kHz wide. Stimuli were
digitally synthesized at a sampling rate of 128 kHz, digital-to-analog
converted by the DAQ-6062E card, amplified, attenuated, and played through a
high-frequency piezoelectric speaker (`tweeter') positioned at a distance of
25 cm from the right ear of the animal, the speaker axis being directed to the
ear (Fig. 2). Frequency
response irregularity of the speaker was up to 30 dB within a range from
1–22.5 kHz, but not more than 10 dB within any half-octave band except
at the lowest part of the frequency range (1–2 kHz) where it reached 16
dB/octave. However, even at the steepest frequency–response
irregularity, the acoustic signal spectrum shifted by not more than 6% (0.08
octave) relative to the electric signal
(Fig. 1B). Stimulus intensity
was measured by a calibrated microphone positioned at the speaker axis at the
distance of 25 cm.
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Threshold evaluation
To find a hearing threshold at each carrier frequency, AEPs were recorded
in response to stimuli of intensities decreased by 5 dB steps, starting with
an intensity provoking a well-developed response and continuing to a level
incapable of provoking an AEP detectable in noise. In order to better extract
an AEP waveform from the background physiological electrical noise and
quantitatively estimate its amplitude, cross-correlation analysis was used
(Supin et al., 2001).
Cross-correlation functions (CCF) between the evaluated record and a standard
AEP waveform were computed, using a definite AEP to a high-intensity stimulus
of the same frequency as a standard. A CCF was computed for a 10 ms window of
the original record, from 2.5 to 12.5 ms after the stimulus, and within a lag
range of ±2 ms. The magnitude of the CCF peak was specified in terms of
the root mean squared (RMS) of the searched-for waveform within a 10 ms
analyzed window. The CCF peak magnitudes were plotted as a function of
stimulus intensity expressed in dB and were approximated by straight
regression lines. The intersections of the regression lines with the
zero-magnitude levels were accepted as the threshold estimates.
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The AEP amplitude was intensity-dependent. However, in general it was rather low. Even at the highest available intensities (110 dB in Fig. 4), the AEP amplitude did not exceed 0.5 µV. At lower intensities, the amplitude was even less. Therefore, although as low background noise at around 30 nV RMS was achieved in the records, a detection of low-amplitude AEPs in noise was problematic.
AEP thresholds
Examples of cross-correlation functions (CCF) between the low-amplitude AEP
waveforms (presented in Fig.
4A) and a standard AEP waveform are shown in
Fig. 4B. For computation, the
AEP waveform evoked by the highest intensity (110 dB) of the same frequency
was used as a standard. All the exemplified CCFs had a positive peak at or
near the zero lag. Peak magnitude diminished with decreasing intensity, thus
reflecting the diminishing AEP amplitude. The CCF peak position at the lag
scale was also intensity dependent: its delay increased as the intensity
decrease, thus reflecting the increase of the AEP latency.
To find the AEP threshold, CCF peak magnitudes (marked by dots in Fig. 4) were used as evaluates of the AEP amplitude. The CCF peak magnitudes were plotted as a function of stimulus intensity expressed in dB (Fig. 5). In a near-threshold intensity range, these functions could be satisfactorily approximated by straight regression lines (r2=0.94 in Fig. 5). The intersection of the regression line with the zero-magnitude level was accepted as a threshold estimate. In the example presented in Fig. 5, this estimate was 68.3 dB.
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Using this technique of threshold evaluation, AEP thresholds were measured at frequencies ranging from 1 to 22.5 kHz in half-octave steps. However, at the frequency of 1 kHz AEP the response amplitude was not large enough, even at the highest available intensity, to draw the regression line. So the audiograms (thresholds as a function of sound frequency) were only obtained at frequencies from 1.4 kHz and higher. The audiograms obtained for the three subjects are presented in Fig. 6A. An averaged audiogram is presented in Fig. 6B.
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). It
is difficult to estimate how well a species hears from a single subject
because there is always individual variability, regardless of the species
(Yost, 1994). Although there
was some data scatter and inter-individual variation among the thresholds of
the three bears, this variation mostly did not exceed 10 dB at any given
threshold and some were remarkably uniform like that obtained at 4 kHz
(Fig. 6) – all three
bears showed a threshold near 70 dB. These thresholds can be compared, for
example, to similar thresholds measured in noise within a sound-proof booth
for two semiaquatic carnivores, a California sea lion and a Northern Elephant
seal (Southall et al., 2003).
The sea lion and northern elephant seal presented with 4 kHz masking tones of
35 and 40 dB showed thresholds of 60 dB and 63.5 dB, respectively, somewhat
similar to the polar bear mean threshold of 70 dB at 4 kHz obtained in
fluctuating noise conditions around 40–50 dB
(Fig. 3).
Correction of the data for temporal summation and comparison with the ambient noise
As indicated earlier, we did not have the opportunity to measure the bear
hearing in a sound-proof booth. All the measurements were done in a background
of ambient noise. So the question arose as to whether the obtained thresholds
were real absolute hearing thresholds or thresholds masked by ambient noise.
To answer the question, the obtained thresholds had to be compared to the
background noise level.
The critical band widths in bears are unknown. However, it can be supposed that they are on the same order as those of other mammals, i.e. 10–20% of the central frequency (0.14–0.26 octave). This is of course less than the stimulus bandwidth of 0.5 octave used herein. In this situation, a direct comparison between the stimulus and noise is possible using the noise intensity in bands of the same width as the stimulus bandwidth (half-octave bands), because a critical band extracts one and the same fraction of energy from both the 0.5-octave stimulus and a 0.5-octave band of noise.
For a correct comparison, however, one must take into consideration that
the stimuli were short pips, probably shorter than the limit of temporal
summation in the bear's auditory system, whereas the background noise was not
limited in duration. Therefore, a correction had to be done for incomplete
temporal summation of the stimuli. The temporal summation limit has, of
course, never been measured in bears because the hearing of bears has never
been measured (Fay, 1988), but
in the majority of mammals that have been investigated, including carnivores,
the temporal summation limit is normally between 100 and 1000 ms
(Fay, 1988). So by analogy, a
similar limit may be expected in bears. We assume a conservative intermediate
value of 300 ms as a temporal summation limit. Our stimuli were cosine
enveloped, i.e. the envelope was defined as: 0.5[1–cos(2
t/T)], where t is time and T is the cosine
cycle duration. For this envelope form, the equivalent rectangular duration
(ERD) is:
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The cosine cycle duration T lasted from 2 ms (at frequencies of 1.4–2.8 kHz) to 0.25 ms (at 22.5 kHz), so the stimulus ERD varied from 0.75 to 0.094 ms, respectively. Thus applying the temporal summation limit of 300 ms, the correction should be from 26 dB (for a 0.75 ms stimulus) to 35 dB (for a 0.094 ms stimulus). The resulting corrected thresholds for a temporal summation limit of 300 ms are shown in Fig. 6B along with the original averaged thresholds. Of course, we do not know whether the temporal summation limit in the bear was really 300 ms; however, if it ranged between 100 and 1000 ms, the correction would not differ by more than ±5 dB.
Significance of the threshold data
A major part of the threshold-vs-frequency function corrected for
temporal summation is at or near the lower boundary of the area of the ambient
noise (Fig. 6). These
thresholds are therefore logically masked thresholds in the ambient noise
rather than real absolute hearing thresholds. Thus, we cannot state that we
obtained a real absolute threshold audiogram of the polar bear. But, our
inability to find absolute thresholds does not mean the data presented above
were not informative; most marine mammals hearing studies have been conducted
in the presence of background noise. And, the absolute thresholds of hearing
cannot be higher than the masked thresholds, thus the obtained data indicate
that the absolute thresholds of hearing of polar bears are certainly below
these levels. Thus, we can conclude that the bear hearing sensitivity is
rather good within a range of 11.2–22.5 kHz: absolute thresholds are
lower than 27–30 dB. Absolute thresholds without a noise background have
not been published or estimated for pinnipeds, but absolute sensitivities at
levels very similar to the polar bear are likely based on the masked hearing
thresholds shown for the animals in Southall et al.'s work
(Southall et al., 2003).
It is important to note that the bear thresholds are also rather low within
a rather wide frequency range, up to the highest tested frequency of 22.5 kHz
where the threshold is below 30 dB. So the frequency range of the polar bear's
hearing is wider than this frequency, i.e. wider than in humans, which is less
than 20 kHz (for a review, see Yost,
1994). Thus we can state that polar bears possess an acute and
wide-frequency-range hearing ability. Given the relatively low frequencies of
the measured vocalizations produced by seals
(Stirling, 1973) and heard by
the bears in air (Cushing et al.,
1988), we had no a priori reason based on foraging and
the calls of their prey to expect that the bears would hear such a wide range
of frequencies, but they did. Perhaps there is simply an overall advantage in
the use of high frequencies for auditory localization. An awareness of the
polar bear's acute and relatively wide-frequency hearing should cause people
to operate with caution where there may be an impact of anthropogenic noise on
polar bears. Certainly these results call for additional research on the high
frequency hearing of all bears.
Two questions come to mind when evaluating these evoked potential data as
true hearing data: (1) are evoked potential thresholds the same as those
obtained when an animal is perceiving the sounds and reporting them, and (2)
are measurements obtained from a bear anesthetized with
Zalopine® and Zoletil® a true indication of its
hearing abilities? The definition of hearing usually requires some sort of
perception on the part of an animal or human, and thus in the strictest sense
auditory-evoked potential studies do not directly measure hearing
(Stevens, 1970). Recent work,
however, directly measuring hearing on whales and dolphins and comparing
traditional behavioral and AEP procedures, has shown that the methods produce
directly comparable results (Yuen et al.,
2005; Houser and Finneran, 2006). If these findings can also be
applied to the polar bear, then it seems reasonable to assume that the AEP
measures have at least given a clear first measure of polar bear hearing. The
data indicate that polar bears hear very well, particularly in the range
between 11.2 and 22.5 kHz. If Zalopine® and
Zoletil® disrupted the ability to measure auditory evoked
potentials, these sorts of data would not have been obtained.
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