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First published online March 27, 2009
Journal of Experimental Biology 212, 1078-1086 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.025619
Biosonar adjustments to target range of echolocating bottlenose dolphins (Tursiops sp.) in the wild
1 Zoophysiology, Department of Biological Sciences, Aarhus University, 8000
Aarhus C, Denmark
2 Murdoch University Cetacean Research Unit, Centre for Fish and Fisheries
Research, Murdoch University, Perth, 6150 Western Australia
3 Fjord and Bælt and University of Southern Denmark, Margrethes Plads 1,
5300 Kerteminde, Denmark
4 Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA
* Author for correspondence (e-mail: Frants.Jensen{at}gmail.com)
Accepted 26 January 2009
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: Tursiops, dolphin, echolocation, biosonar, sound production, automatic gain control
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Odontocetes have adapted to foraging niches within a
diverse range of habitats where they face the challenge of navigating and
finding prey with active sonar under varying noise and clutter conditions.
However, despite a dedicated research effort on trained animals over the past
40 years, we still have a limited understanding of how wild odontocetes adjust
their biosonar outputs to solve the task of locating prey acoustically in a
three-dimensional world with a constantly changing spatial and temporal
relationship between the clicking predator and its echo-generating prey
(Johnson et al., 2008;
Madsen et al., 2005). In
particular, little is known about how odontocetes modify the characteristics
of the echolocation pulse, such as source level and click interval, with
varying range to the target.
For a toothed whale searching for prey, the detection of an ensonified
target depends on the echo-to-noise or echo-to-clutter ratios in the hearing
system. In a noise-limited echolocation situation that requires a given
echo-to-noise ratio for correct detection, the detection range will increase
with increasing source level and decreasing noise levels
(Au, 1993). The received echo
level (EL) generated by the ensonified prey can be evaluated quantitatively
with the sonar equation (Urick,
1983) from the source level (SL), the transmission loss (TL) and
the target strength of the ensonified target (TS)
(Fig. 1). For a single point
target, such as a fish or squid, the returning echo level can be evaluated as:
 | (1) |
):
 | (2) |
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).
Evidence of TVG in the receiver has been found in some bat species who
tighten muscles attached to their middle ear bones just prior to emission of a
sonar cry (Henson, 1965;
Suga and Jen, 1975), followed
by a gradual relaxation and consequent increase in hearing sensitivity over
the next 6.4 ms (Kick and Simmons,
1984). Along with neural attenuation in the midbrain, this
gain-control mechanism provides 6–11 dB attenuation for a time delay
between emitted sound and echo that corresponds to halving the distance
between the bat and target (Hartley,
1992; Kick and Simmons,
1984; Simmons et al.,
1992). Similar mechanisms have recently been found in the false
killer whale (Pseudorca crassidens), possibly as a consequence of the
small time separation between the powerful outgoing click and the weak
returning echo (Nachtigall and Supin,
2008; Supin et al.,
2004; Supin et al.,
2008). By contrast, the harbour porpoise (Phocoena
phocoena) shows no evidence of adjusting hearing sensitivity during
echolocation (Beedholm et al.,
2006). Thus, it seems that some, but not all, terrestrial and
aquatic biosonar systems incorporate TVG in their auditory systems.
While man-made sonars normally do not adjust the source level to the time
delay between pulse emission and echo reception, some bats have been shown to
use such a form of dynamic TVG on the transmission side
(Hiryu et al., 2007;
Kobler et al., 1985). Au and
Benoit-Bird (Au and Benoit-Bird,
2003) and Au (Au,
2004) reported that four species of free-ranging delphinids also
use TVG control on the transmission side of their biosonar systems. They found
that back-calculated source levels from dolphins echolocating on a star-shaped
hydrophone array exhibited a 20 log(R) relationship with target range and
proposed that this is an adaptation to stabilize the returning echo levels
from fish schools with volume reverberative properties in which the echo level
for a constant source level biosonar would increase with 20 log(R). Au and
Benoit-Bird further inferred that this dynamic TVG of lower source level at
short target ranges is a passive biophysical consequence of reducing the
interclick interval (ICI) to decreasing two-way travel time (TWT) as the
source approaches a target (Au and
Benoit-Bird, 2003).
Toothed whales generally use ICI that are longer than the TWT to the target
(Au, 1993;
Teilmann et al., 2002). All
available evidence suggests that the toothed whale sound production system
operates as a pneumatic capacitor that relaxes partially during each click
emission (Cranford and Amundin,
2004; Cranford et al.,
1996; Ridgway,
1980). This means that below a certain ICI, the source level is
expected to decrease with increasing repetition rate
(Madsen et al., 2002). Thus,
if a delphinid decreases the ICIs when approaching a target, and thus
consequently reduces the source level, the result is an adjustment of source
level to target range produced by the physical limitations of the sound
production system. This form of TVG is thus not seen as an active cognitive
process but rather a passive consequence of the ICI to TWT adjustment that is
termed automatic gain control (AGC) (Au and
Benoit-Bird, 2003). However, recordings on foraging toothed whales
using acoustic tags do not support the presence of a simple AGC that reduces
source level with reducing range to a prey target
(Johnson et al., 2008;
Madsen et al., 2005). Rather,
available data suggest that foraging beaked whales employ a bimodal output
mode in which the ICIs and click amplitudes are not adjusted to target range
during search and approach phases (first mode) but where the ICIs and click
amplitudes are reduced dramatically when the whale switches to the buzz phase
(second mode) when the prey is about one body length from the whale
(Johnson et al., 2008;
Madsen et al., 2005).
These conflicting findings show that we do not fully understand how and why
toothed whales adjust their acoustic output as a function of target range. The
AGC hypothesis for the biosonar of free-ranging delphinids echolocating on
hydrophone arrays is based on the work of Au
(Au, 1993) that the ICIs are
linked to the TWT in trained bottlenose dolphins (Tursiops
truncatus). However, it remains unknown whether reduced ICIs actually
entail lower source levels from these animals, and no studies have tested
whether bottlenose dolphins actually do reduce ICI with TWT in the wild.
Finally, it needs to be tested if such effects always lead to a 20log(R) AGC,
as reported for four delphinid species (Au
and Benoit-Bird, 2003).
Here, we use a vertical array of four calibrated hydrophones to test the hypotheses that (1) wild bottlenose dolphins (Tursiops sp.) adjust their ICI to the range between dolphin and array, (2) decreasing click intervals reduce the source level and (3) the click interval reduction gives rise to a 20 log(R) AGC mechanism.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). A coastal
bottlenose dolphin (Tursiops sp.) population of a few hundred
individuals inhabits the nearby coastline and frequently forages in the
recording area.
Recording equipment
A small 6 m aluminium-hulled dinghy was anchored with the engine off and
used as a recording platform. A vertical array of four Reson TC4034
hydrophones (RESON, Slangerup, Denmark), separated by 1.0 m, was suspended
between a surface buoy and a 0.5 kg lead weight. The array support was made of
PVC with an acoustic impedance close to seawater in order to minimize
shadowing and reflections. The hydrophones were connected to a custom-built
four-channel amplifier with 40 dB gain, 1 kHz high-pass filter (2-pole) and
200 kHz low-pass filter (3-pole). The amplified and filtered signals were
digitized with a four-channel, 12-bit analogue-to-digital converter (ADlink
Technology, Chungho City, Taiwan) writing data to a laptop computer
via a PCMCIA interface (Magma, San Diego, CA, USA) sampling each
channel at 800 kHz. The nominal hydrophone sensitivity (calibrated before and
after field experiments to ±1 dB) was –220 dB re. 1 V/µPa,
with an omni-directional receiving characteristic (spherical element) in the
relevant frequency range from 10 kHz to 200 kHz (±2 dB). The frequency
response of the amplification box was corrected for post-processing, giving an
overall flat frequency response of the recording chain (±2 dB) between
1 kHz and 200 kHz, with a clipping level of 194 dB re. 1µPa peak received
level as limited by the peak voltage that can be handled by the ADC.
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5 s) for data storage approximately every
minute.
Signal analysis
All signal analyses were made with custom-written routines in Matlab 6.5
(The Mathworks, Inc., Natick, MA, USA). Because of the highly directional
nature of toothed whale echolocation clicks
(Au, 1993), most recordings did
not yield clicks suitable for analysis. To prevent ambiguities in ICI
measurements, each click series was examined visually and discarded if the
click intervals were very irregular or alternating between being short and
long, indicating that several dolphins might have been clicking
simultaneously. Echolocation clicks in each approach were then located for
further analysis with an automated click-detector set to a minimum detectable
received level (threshold) of 154 dB re. 1 µPa (peak) on the top
hydrophone. If the click could not be located on all channels, the click was
not analyzed further.
Localization
To quantify source parameters, an estimate of the source position relative
to the receivers was found using acoustic localization techniques based on
time-of-arrival differences of the same click on the four receivers
(Wahlberg et al., 2001). The
time-of-arrival differences were determined by cross-correlating the signal
recorded on the top hydrophone with the signals recorded at the other
hydrophones, excluding surface reflections. We calculated a sound propagation
speed of 1520 m s–1 from the Leroy equation
(Urick, 1983) based on an
average measured temperature of 23.5°C and a salinity value of 35 p.p.m.
For each pair of hydrophones, the time-of-arrival difference renders a single
hyperbola as a function of a two-dimensional coordinate set by depth and range
(Fig. 2). Three independent
hyperbolas are generated from four receivers, and the unknown source
coordinates were estimated by solving the three equations with a method of
least-squares (Madsen and Wahlberg,
2007; Spiesberger and
Fristrup, 1990).
The localization precision for an array of this aperture was tested in
shallow water by transmitting artificial dolphin clicks (two cycles, centroid
frequency 70 kHz) at a depth of 3 m using an omnidirectional HS70 hydrophone
(Sonar Products) at measured ranges from the array
(Fig. 3). The RMS error, or
standard error, defined as the root-mean-squared range deviations from the
true range (Villadsgaard et al.,
2007), was below 9% for range estimates within 40 m but increased
significantly beyond this range. Transmission loss [estimated as 20
log(R)+R] for dolphins localized within 40 m would consequently be
estimated with an RMS error of <0.8 dB from the ranging procedure. Given
the combined uncertainty of localization and the calibrated recording system,
the back-calculated sound pressure 1 m from the clicking animals could
therefore be estimated with an uncertainty of <2 dB for source ranges
within 40 m. Accordingly, we only included clicks from dolphins localized at
ranges closer than 40 m in the analysis.
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), and it was manually
verified that ICIs were not calculated incorrectly due to recording several
dolphins at the same time. The range from source to each hydrophone was
calculated from source coordinates with the Pythagorean equation. Received
levels at the hydrophones were calculated as peak–peak (pp) sound
pressure given by the pp amplitude of the click
(Au, 1993). Apparent source
levels (ASLpp) were defined as the back-calculated sound pressure
level 1 m from the source at an unknown angle from the acoustic axis
(Madsen and Wahlberg, 2007;
Møhl et al., 2000) and
calculated according to Eqn 3, in
accordance with previous studies (e.g.
Madsen et al., 2004):
 | (3) |
of 0.025 dB m–1 at 90 kHz (close to the
centre frequency of on-axis Tursiops clicks).
On-axis criteria
When investigating source properties of directional biosonar signals, it is
essential to quantify the signal on or as close to the acoustic axis as
possible (Madsen and Wahlberg,
2007) due to strong off-axis distortion
(Au, 1993;
Madsen et al., 2004).
Insufficient on-axis criteria will include off-axis clicks in the analysis,
leading to underestimated source levels and a lowered frequency emphasis of
the reported on-axis clicks (Madsen and
Wahlberg, 2007). With a one-dimensional array, it is difficult to
ensure that a given click is on-axis, and most recorded clicks will be
recorded at various degrees off the acoustic axis. To maximize the chance of
analysing clicks recorded on or close to the acoustic axis in the horizontal
plane, we identified longer click sequences, here called scans, most likely
associated with the acoustic beam of the animal passing across the axis of the
hydrophone array. Provided that the animal maintains the same source level and
directionality, the click with highest amplitude has the highest likelihood of
being on-axis. In this study, we defined a scan as any sequence of 10 or more
clicks with ICIs less than 1 s. For each scan, we then classified a click as
on-axis and analysed it if it fulfilled the following criteria: (1) the click
could be localized, (2) the click had the highest received level in a scan,
(3) the highest received level was recorded on one of the two central
hydrophones and (4) the received level was higher than the received level of
both the preceding and following click from the same hydrophone. These
criteria will maximize the chance of recording signals that are on-axis in
both vertical and horizontal planes.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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2%) were classified as on-axis from a total of 26
different approaches. Seven well-known individuals from the population were
identified and represented in this sample. None of these animals continuously
visited the recording station throughout the recording sessions, making it
unlikely that a few animals contributed to the bulk of the dataset.
Interclick interval adjustment
Clicks designated as on-axis had a median ICI of 52 ms. A lower limit on
ICIs was imposed by the click detector with a blanking time of 1.9 ms after
each detection, and an upper limit was caused by our definition of a scan as a
series of clicks separated by <1000 ms. The ICI variance was high, with a
standard deviation of 58 ms and values ranging between 17 and 462 ms for
on-axis clicks. The ICI was significantly correlated with range
(Fig. 4B) (linear regression:
ICI=2.2R+30 ms, P<0.05) but with a very large scatter
(r2=0.12). All ICIs for on-axis clicks exceeded the TWT
from the dolphin to the array (1.33 ms m–1) by a median lag
time of 31 ms.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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).
Sample size and scatter
Because of the highly directional nature of high-frequency clicks used for
echolocation, most of our recordings did not contain suitable on-axis clicks,
and only 85 clicks conformed to our on-axis criteria. Previous studies often
accept a large proportion of the dataset (upwards of two-thirds of the
recorded clicks) as on-axis (Au and
Herzing, 2003; Rasmussen et
al., 2002). This provides a large sample size but at the risk of
underestimating the actual source levels by including clicks recorded further
from the acoustic axis of the dolphin
(Madsen and Wahlberg, 2007).
In the present study, we implemented strict on-axis criteria in order to
prioritize accurate source level estimates over sample size.
Both this and previous studies of free-ranging delphinids
(Au, 2004;
Au and Benoit-Bird, 2003) are
based on data with a high scatter. For these studies, the individual identity,
movement pattern and behaviour of a given clicking dolphin is seldom known,
and data will inevitably be based on clicks from many different dolphins
engaged in various activities and recorded at various degrees off the acoustic
axis. Moreover, individual toothed whales are known to adjust source levels of
their biosonar to background noise levels
(Au et al., 1985) and it is
still undetermined whether they adjust signal parameters to the amount of
clutter in their environment, as bats do
(Moss et al., 2006;
Surlykke and Moss, 2000).
Hence, any studies in the wild will tend to exhibit some degree of variation
in the estimated ASLs caused by intraindividual differences and differences in
behaviour.
Interclick interval adjustment
When an echolocating animal approaches a target, the TWT between emission
of the outgoing click and return of the target echo decreases as the animal
approaches the ensonified target. Experiments with trained bottlenose dolphins
in captive settings have shown that ICIs in target detection tasks are given
by the TWT plus a short lag time of 19–45 ms
(Au, 1993). By contrast, a
fundamental problem of studies using hydrophone arrays to study free-ranging
dolphins is that the range between the dolphin and the actual target of
interest is unknown, and instead the calculated range from the dolphin to the
recording array is taken as a proxy by assuming that the array is the target.
However, if dolphins are not echolocating on the recording array but on prey
items or other objects, there should be no evident relationship between ICIs
and dolphin-array range, even if the dolphins do adjust their ICIs according
to the TWT to their chosen target. To address this problem, experimental
designs should preferably include a mechanism to test if dolphins are actually
ensonifying the array as their target of interest. In the present study, we
found no on-axis clicks with ICIs shorter than the TWT
(Fig. 4), which might indicate
that dolphins were attending to either the array or to targets further away.
Since it is difficult to test the second possibility, the following discussion
assumes, as in previous studies (Au and
Benoit-Bird, 2003), that dolphins were ensonifying the array
(referred to hereafter as a target).
We observed a reduction in ICI with decreasing target range in a
2.2x(R)+30.2 ms fashion in line with earlier studies on trained
bottlenose dolphins (Au, 1993)
where the mean ICI increases with the TWT
(Fig. 4B, filled squares). The
relationship between ICIs and TWT displays similar levels of variation to raw
data from target detection experiments with trained bottlenose dolphins
(Turl and Penner, 1989).
Wild porpoises occasionally decrease their ICIs systematically over time
during events that have been interpreted as prey approaches
(Akamatsu et al., 2007).
However, in contrast to bottlenose dolphins, captive porpoises in target
detection tasks appear to use a much more constant ICI (between 50 and 80 ms)
with no apparent range adjustment
(Teilmann et al., 2002).
Similar steady ICIs during search phases are observed for two species of
beaked whales and in sperm whales, which exhibit search or approach phases
with a very long lag time (>300 ms) leading up to the buzz phases
(Madsen et al., 2005). On the
other hand, beaked whale ICIs measured at the start of a buzz are sometimes
correlated with the TWT (Johnson et al.,
2008). Belugas trained for target detection tasks have even been
shown to exhibit a unique type of echolocation in which clicks are sent out in
packets with a high click repetition rate that does not allow the echoes to
return before the next click is emitted
(Turl and Penner, 1989). Thus,
it seems that while the odontocete auditory and neural system may be flexible
enough to handle biosonar range ambiguities that may arise when ICIs are lower
than the TWT (Turl and Penner,
1989), the general approach phase for toothed whales in the wild
involves processing the returning echoes before a new click is emitted.
Effect of interclick interval on acoustic output
Toothed whales generate echolocation clicks by pneumatically accelerating a
pair of connective tissue lips that allow a small volume of pressurized air to
pass from the bony nares to the vestibular air sacs
(Cranford et al., 1996;
Ridgway, 1980;
Ridgway and Carter, 1988). The
current model of toothed whale sound production suggests that this system
operates as a pneumatic capacitor that requires a certain air pressure in the
nasal passage before the muscularly controlled tension in the connective
tissue of the phonic lips is overcome and a click is generated
(Ridgway, 1980;
Ridgway and Carter, 1988). If
the repetition rate of echolocation clicks exceeds a critical rate, the nasal
air pressure may not have time to build up fully before the next click
generation event. This would cause the acoustic output to drop with increasing
clicking rate, a phenomenon that would explain the drop in source level seen
in buzzes with fast repetition rates
(Madsen et al., 2005). This is
the proposed cause of an AGC in delphinid biosonar
(Au and Benoit-Bird, 2003).
Such a correlation between ICIs and source level is evident in harbour
porpoise biosonar operating at high repetition rates with ICIs below 20 ms
(Beedholm and Miller, 2007).
Although we should be careful about addressing causality in our study, the
observed drop in ASL for ICIs below 30 ms supports the contention that the
pneumatic sound generator will start to limit the acoustic output below a
certain ICI (Fig. 5), as found
by Au and Benoit-Bird (Au and Benoit-Bird,
2003). Although more data are needed to address this matter fully,
the present data imply that the highest source levels recorded here can be
generated when the ICIs exceed 30–40 ms.
The source levels reported here are lower than the maximum values of 227 dB
re. 1 µPa (pp) reported for trained bottlenose dolphins rewarded for
long-range target detection (Au et al.,
1974). Hence, the ASLs found in this study may not reflect the
highest source level potential of bottlenose dolphins, but rather the typical
source levels utilized in this specific habitat. It is possible that maximum
source level values would require longer ICIs than the 30 ms we tentatively
propose here, but the source levels in the present study are still comparable
to the source levels of other free-ranging delphinids where apparent effects
of AGC have been observed (Au and
Benoit-Bird, 2003).
If we assume an average lag time of 19–45 ms from detecting the
incoming click echo to emitting the next click
(Au, 1993), a 30 ms ICI would
correspond to a target range of less than 8 m. Blainville's beaked whales
switch from regular clicking (ICI 200–600 ms) to a buzz phase (ICIs
below 20 ms) when they approach within a body length of the prey
(Madsen et al., 2005). The
decrease in source level for ICIs less than 30 ms in bottlenose dolphins might
therefore signify the proximity to this border region between regular clicking
and buzz clicks.
Time-varying gain control
So far we have shown that the recorded bottlenose dolphins decrease their
ICIs when they close in on the recording array and that the ICIs for on-axis
clicks always allow enough time for the array echo to return before sending
out the next click. We have shown that the acoustic output may be limited
biophysically when ICIs decrease below around 30–40 ms. While there is
little evidence for the contention that a link between target range and source
level is dictated by a simple biophysical coupling between output and ICIs
longer than 30 ms, the next question to ask is whether echolocating bottlenose
dolphins may still display a form of TVG control governed by a different
mechanism.
We found a significant decrease in on-axis click source level as a function
of 17 log(R) (Fig. 6), and this
may partly compensate for the increasing echo level when dolphins are
approaching a target. This compensation matches well with previous studies of
AGC in free-ranging delphinids (Au and
Benoit-Bird, 2003). The findings also suggest a likely pneumatic
reduction in source level for ICIs below 30–40 ms, which could give rise
to an AGC mechanism for short ICIs and short target ranges. However, 88% of
our recorded on-axis clicks had ICIs longer than 30 ms but still display a
correlation between range and source level, even though the sound generator
should be able to maintain high outputs biophysically.
One explanation might be that the dolphins actively decrease their source
level during target approach, giving rise to a form of TVG that is not a
passive consequence of pneumatic restrictions in the sound generator for
longer ICIs. Dolphins are well known to adjust their acoustic output to their
surroundings. For example, source levels of free-ranging dolphins are much
higher than those of dolphins held in tanks
(Au et al., 1974;
Madsen et al., 2004) and may
vary depending on ambient noise levels (Au,
1993). An active TVG control mechanism would still allow the
animals to compensate for the decreased two-way transmission loss when
approaching a target and could act to reduce echo level fluctuations from
different types of targets and under different clutter conditions.
How different species of toothed whales stabilize the returning prey echoes
when approaching prey is still an unsolved issue and seems to differ between
species. A trained false killer whale seems to adjust its hearing sensitivity
to fully compensate for the two-way transmission loss while keeping their
source levels constant (Nachtigall and
Supin, 2008). By contrast, harbour porpoises do not seem to
decrease their hearing sensitivity
(Beedholm et al., 2006), and
whether they exhibit TVG in their biosonar output
(Li et al., 2006) remains
unresolved (Beedholm and Miller,
2007).
Another possible explanation is that the apparent AGC at long ranges does
not actually reflect adjustments in the dolphin biosonar but instead arises as
an artefact in the data collection or processing methods. All studies
reporting AGC in free-ranging delphinids have been conducted with either a
single hydrophone and reflections from surface and bottom
(Li et al., 2006) with a
short, star-shaped array (Au and
Benoit-Bird, 2003) or with a linear vertical array (present study)
used to record and localize the clicking delphinids. A limitation of these
setups is that, in order to detect clicks for analysis, the received sound
levels must exceed a certain absolute threshold independent of the
localization range. Subsequently, the received levels are back-calculated to
ASLs by compensating for the one-way transmission loss of 20 log(R)+R
between the dolphin and the recording array. The actual received SPL at the
array may vary because of several factors, including the acoustic output or
source level, the aspect from the delphinid to the recording array, and the
range between the dolphin and the receiver. On-axis criteria are designed to
maximize the probability of analysing clicks recorded close to the acoustic
axis, so that back-calculated source levels reflect the true source levels.
Having insufficient on-axis criteria will increase the amount of off-axis
clicks that are included in the analysis.
To illustrate the effect of insufficient on-axis criteria, we can temporarily relax our on-axis criteria and include all (i.e. both on- and off-axis) clicks received by one hydrophone in the analysis (Fig. 6A). This leads to an underestimate of the true source level, and the data fit closer to a 20 log(R) function. This would imply that dolphins echolocating at targets other than the array still adjust their biosonar to the array in a 20 log(R) fashion. However, the main reason for these perplexing results is that clicks with low source levels recorded from afar will fall below the detection threshold because of a large transmission loss whereas clicks with equally low source levels recorded close to the array are more likely to exceed the received level detection threshold and be included in the analysis. Regardless of the detector type, click detection will always ultimately be limited by a set threshold or by a background or system noise floor in the recordings. The geometric spreading loss model of 20 log(R) used will therefore effectively filter clicks in a fashion that excludes clicks with low SLs at longer ranges and hence bias the data towards a 20 log(R) relationship, irrespective of whether dolphins actually adjust their source levels at all.
In conclusion, we have shown that free-ranging bottlenose dolphins emit echolocation clicks at ICIs that exceed the roundtrip travel time to the target, and with some adjustment to the decreasing TWT as they approach a target. At the regular (non-buzz) echolocation click rates studied here, the acoustic output generated by the pneumatic sound generator is only limited by the repetition rate when the ICI drops below 30–40 ms. This supports the idea of a pneumatic constraint in the sound production system that may account for the large reductions in source level of fast repetition rate buzzes. We observe an apparent AGC of 17 log(R) that is close to the 20 log(R) relationship reported in previous studies. For targets within a few body lengths (when ICIs decrease below 30–40 ms), the adjustment of source levels to target range may be a passive consequence of adjusting ICIs to target range to a degree where the nasal pressure does not have time to build up fully. By contrast, this study suggests that the adjustment of source level to target ranges beyond a few body lengths cannot be explained by pneumatic restrictions in the sound generator. Instead, they may stem from (1) an active, cognitive adjustment of source level to target range to reduce fluctuations in received echo levels or (2) an inherent observer bias caused by using click detectors with fixed received level thresholds and back-calculating source levels with a geometric spreading loss model of 20 log(R). Thus, bottlenose dolphins do adjust their sound production to target range in terms of ICIs, and to some degree also in terms of the biosonar output, but the question of overall TVG in the bottlenose dolphin biosonar remains unclear. This matter should be addressed experimentally in studies with variable target location and constant source-to-array geometry (for example, experiments with phantom echoes) or with onboard acoustic tags on animals that use their biosonars to echolocate on prey rather than recording arrays.
LIST OF ABBREVIATIONS
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Footnotes |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Akamatsu, T., Teilmann, J., Miller, L. A., Tougaard, J., Dietz, R., Wang, D., Wang, K. X., Siebert, U. and Naito, Y. (2007). Comparison of echolocation behaviour between coastal and riverine porpoises. Deep-Sea Res. Part II 54,290 -297.[CrossRef]
Au, W. W. L. (1993). The Sonar of Dolphins. New York: Springer Verlag.
Au, W. W. L. (2004). Echolocation signals of wild dolphins. Acoust. Phys. 50,454 -462.[CrossRef]
Au, W. W. L. and Benoit-Bird, K. J. (2003). Automatic gain control in the echolocation system of dolphins. Nature 423,861 -863.[CrossRef][Medline]
Au, W. W. L. and Herzing, D. L. (2003). Echolocation signals of wild Atlantic spotted dolphin (Stenella frontalis). J. Acoust. Soc. Am. 113,598 -604.[CrossRef][Medline]
Au, W. W. L., Floyd, R. W., Penner, R. H. and Murchison, A. E. (1974). Measurement of echolocation signals of atlantic bottlenose dolphin, Tursiops truncatus Montagu, in open waters. J. Acoust. Soc. Am. 56,1280 -1290.[CrossRef][Medline]
Au, W. W. L., Carder, D. A., Penner, R. H. and Scronce, B. L. (1985). Demonstration of adaptation in beluga whale echolocation signals. J. Acoust. Soc. Am. 77,726 -730.[CrossRef][Medline]
Beedholm, K. and Miller, L. A. (2007). Automatic gain control in harbour porpoises (Phocoena phocoena)? Central versus peripheral mechanisms. Aquat. Mamm. 33, 69-75.[CrossRef]
Beedholm, K., Miller, L. A. and Blanchet, M. A. (2006). Auditory brainstem response in a harbor porpoise show lack of automatic gain control for simulated echoes. J. Acoust. Soc. Am. 119,EL41 -EL46.[CrossRef][Medline]
Cranford, T. W. and Amundin, M. (2004). Biosonar pulse production in odontocetes: the state of our knowledge. In Echolocation in Bats and Dolphins (ed. J. A. Thomas, C. F. Moss and M. Vater), pp. 27-35. Chicago, IL: The University of Chicago Press.
Cranford, T. W., Amundin, M. and Norris, K. S. (1996). Functional morphology and homology in the odontocete nasal complex: implications for sound generation. J. Morphol. 228,223 -285.[CrossRef][Medline]
Hartley, D. J. (1992). Stabilization of perceived echo amplitudes in echolocating bats. I. Echo detection and automatic gain-control in the big brown bat, Eptesicus fuscus, and the fishing bat, Noctilio-leporinus. J. Acoust. Soc. Am. 91,1120 -1132.[CrossRef][Medline]
Henson, O. W. (1965). Activity and function of
middle-ear muscles in echo-locating bats. J. Physiol.
Lond. 180,871
-887.
Hiryu, S., Hagino, T., Riquimaroux, H. and Watanabe, Y. (2007). Echo-intensity compensation in echolocating bats (Pipistrellus abramus) during flight measured by a telemetry microphone. J. Acoust. Soc. Am. 121,1749 -1757.[CrossRef][Medline]
Johnson, M., Hickmott, L. S., Soto, N. A. and Madsen, P. T.
(2008). Echolocation behaviour adapted to prey in foraging
Blainville's beaked whale (Mesoplodon densirostris). Proc.
Biol. Sci. 275,133
-139.
Kick, S. A. and Simmons, J. A. (1984). Automatic gain-control in the bats sonar receiver and the neuroethology of echolocation. J. Neurosci. 4,2725 -2737.[Abstract]
Kobler, J. B., Wilson, B. S., Henson, O. W. and Bishop, A. L. (1985). Echo intensity compensation by echolocating bats. Hear. Res. 20,99 -108.[CrossRef][Medline]
Li, S. H., Wang, D., Wang, K. X. and Akamatsu, T. (2006). Sonar gain control in echolocating finless porpoises (Neophocaena phocaenoides) in an open water (L). J. Acoust. Soc. Am. 120,1803 -1806.[CrossRef][Medline]
MacLennan, D. N. and Simmonds, J. (1992). Fisheries Acoustics. London: Chapman & Hall.
Madsen, P. T., Johnson, M., de Soto, N. A., Zimmer, W. M. X. and
Tyack, P. (2005). Biosonar performance of foraging beaked
whales (Mesoplodon densirostris). J. Exp.
Biol. 208,181
-194.
Madsen, P. T., Kerr, I. and Payne, R. (2004).
Echolocation clicks of two free-ranging, oceanic delphinids with different
food preferences: false killer whales Pseudorca crassidens and Risso's
dolphins Grampus griseus. J. Exp. Biol.
207,1811
-1823.
Madsen, P. T., Payne, R., Kristiansen, N. U., Wahlberg, M.,
Kerr, I. and Mohl, B. (2002). Sperm whale sound production
studied with ultrasound time/depth-recording tags. J. Exp.
Biol. 205,1899
-1906.
Madsen, P. T. and Wahlberg, M. (2007). Recording and quantification of ultrasonic echolocation clicks from free-ranging toothed whales. Deep-Sea Res. Part I 54,1421 -1444.[CrossRef]
Møhl, B., Wahlberg, M., Madsen, P. T., Miller, L. A. and Surlykke, A. (2000). Sperm whale clicks: directionality and source level revisited. J. Acoust. Soc. Am. 107,638 -648.[CrossRef][Medline]
Moss, C. F., Bohn, K., Gilkenson, H. and Surlykke, A. (2006). Active listening for spatial orientation in a complex auditory scene. Plos Biol. 4, 615-626.
Nachtigall, P. E. and Supin, A. Y. (2008). A
false killer whale adjusts its hearing when it echolocates. J. Exp.
Biol. 211,1714
-1718.
Rasmussen, M. H., Miller, L. A. and Au, W. W. L. (2002). Source levels of clicks from free-ranging white-beaked dolphins (Lagenorhynchus albirostris Gray 1846) recorded in Icelandic waters. J. Acoust. Soc. Am. 111,1122 -1125.[CrossRef][Medline]
Ridgway, S. H. (1980). Electrophysiological experiments on hearing in odontocetes. In Animal Sonar Systems (ed. R. G. Busnel and J. F. Fish), pp.483 -493. New York: Plenum Press.
Ridgway, S. H. and Carter, D. A. (1988). Nasal pressure and sound production in an echolocating white whale, Delphinapterus leucas. In Animal Sonar: Processes and Performance (ed. P. E. Nachtigall and P. W. B. Moore), pp.53 -60. New York: Plenum Press.
Simmons, J. A., Moffat, A. J. M. and Masters, W. M. (1992). Sonar gain-control and echo detection thresholds in the echolocating bat, Eptesicus fuscus. J. Acoust. Soc. Am. 91,1150 -1163.[CrossRef][Medline]
Spiesberger, J. L. and Fristrup, K. M. (1990). Passive localization of calling animals and sensing of their acoustic environment using acoustic tomography. Am. Nat. 135,107 -153.[CrossRef]
Suga, N. and Jen, P. H. S. (1975). Peripheral
control of acoustic-signals in auditory-system of echolocating bats.
J. Exp. Biol. 62,277
-311.
Supin, A. Y., Nachtigall, P. E., Au, W. W. L. and Breese, M. (2004). The interaction of outgoing echolocation pulses and echoes in the false killer whale's auditory system: evoked-potential study. J. Acoust. Soc. Am. 115,3218 -3225.[CrossRef][Medline]
Supin, A. Y., Nachtigall, P. E. and Breese, M. (2008). Forward masking as a mechanism of automatic gain control in odontocete biosonar: a psychophysical study. J. Acoust. Soc. Am. 124,648 -656.[CrossRef][Medline]
Surlykke, A. and Moss, C. F. (2000). Echolocation behavior of big brown bats, Eptesicus fuscus, in the field and the laboratory. J. Acoust. Soc. Am. 108,2419 -2429.[CrossRef][Medline]
Teilmann, J., Miller, L. A., Kirketerp, T., Kastelein, R. A., Madsen, P. T., Nielsen, B. K. and Au, W. W. L. (2002). Characteristics of echolocation signals used by a harbour porpoise (Phocoena phocoena) in a target detection experiment. Aquat. Mamm. 28,275 -284.
Turl, C. W. and Penner, R. H. (1989). Differences in echolocation click patterns of the beluga (Delphinapterus leucas) and the bottlenose dolphin (Tursiops truncatus). J. Acoust. Soc. Am. 86,497 -502.[CrossRef]
Urick, R. J. (1983). Principles of Underwater Sound. New York: McGraw Hill.
Villadsgaard, A., Wahlberg, M. and Tougaard, J.
(2007). Echolocation signals of wild harbour porpoises,
Phocoena phocoena. J. Exp. Biol.
210, 56-64.
Wahlberg, M., Mohl, B. and Madsen, P. T. (2001). Estimating source position accuracy of a large-aperture hydrophone array for bioacoustics. J. Acoust. Soc. Am. 109,397 -406.[CrossRef]
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