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First published online June 29, 2006
Journal of Experimental Biology 209, 2726-2733 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02306
Acoustic radiation from the head of echolocating harbor porpoises (Phocoena phocoena)
1 Marine Mammal Research Program, Hawaii Institute of Marine Biology, P.O.
Box 1106, Kailua, HI 96734, USA
2 Sea Mammal Research Co., Harderwijk, The Netherlands
3 College of Oceanic and Atmospheric Sciences, Oregon State University,
Corvallis, OR 97331-5503, USA
4 Biology Department, San Diego State University, San Diego CA 92182,
USA
* Author for correspondence (e-mail: wau{at}hawaii.edu)
Accepted 3 May 2006
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Summary |
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 TOP Summary IntroductionMaterials and methodsResultsDiscussion and conclusionsReferences |
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Key words: harbor porpoise, Phocoena phocoena, echolocation signals, sound pressure level, melon, lipid, contact hydrophone
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussion and conclusionsReferences |
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). In the harbor porpoise (Phocoena phocoena), a low
density path connects the phonic lips (formerly referred to as the MLDB or
monkey lips/dorsal bursae complex) to the posterior portion of the melon to
couple sounds into the melon and eventually into the water
(Cranford, 1988;
Cranford et al., 1996).
Varanasi and Malin were among the first to study the chemical composition of
the melon lipid (Varanasi and Malin,
1971); they found that it was composed mainly of triacylglycerol
and wax esters. Since then, a number of studies have been performed on the
chemical, acoustical and mechanical properties of melon lipids for a variety
of odontocete species (Blomberg,
1974; Litchfield et al.,
1971; Litchfield et al.,
1979; Litchfield et al.,
1973; Varanasi et al.,
1975; Varanasi and Malin,
1972; Varanasi et al.,
1983). The topography of lipid fractions is thought to be at the
functional apex of the refractive process in the beam formation
(Norris, 1968). The air sacs
and the upper jaw play a role in directing sounds towards the melon and
refraction of the sounds propagating in the melon shape the beam that emerges
from the animal's forehead (Aroyan et al.,
1992). These lipids are also found in the lower jaws of
odontocetes and probably function to focus the received sound beam
(Norris, 1968;
Aroyan, 2001). Sound velocity
measurements of tissue samples from a dolphin melon indicated a graded sound
velocity profile, with a low velocity core near the midline of the melon and
increasing velocity outwards toward the surface of the melon
(Litchfield et al., 1973;
Norris and Harvey, 1974). A
low-density core that likely corresponds to the lowvelocity pathway through
the melon has been shown in X-ray computer tomography (CT) scans
(Cranford, 1988;
Cranford et al., 1996). Sounds
propagating in an inhomogenous sound velocity structure will be governed by
Snell's law so that as sound propagates through a medium of changing sound
velocity, the sound will refract or bend towards the lower velocity region
(Urick, 1983). In the
dolphin's melon, the refraction should be towards the low-velocity core,
causing sounds to be focused and projected in a beam that is directional in
both the vertical and horizontal planes (Au
et al., 1999). The focusing is not sharp but is sufficient to
produce a transmission beam that is approximately 16° in both the
horizontal and vertical planes.
|
). The
density structure of the animal's head was obtained from a CT scan in the
parasagittal plane, from which the corresponding velocity structure was
estimated. Aroyan et al. showed that the melon structure, along with the
different air sacs and the skull, all played a part in focusing the sound
propagating from the nasal region of the animal through the melon into the
water. However, the elevation angle of the resulting beam matched closely the
elevation angle measured with a live bottlenose dolphin only when the source
was assumed to be in the vicinity of the phonic lips and the melon was
included in the numerical simulation (Au et
al., 1986). Elegant as this simulation study was
(Aroyan et al., 1992), the
study was theoretical and certain assumptions were made on the relationship
between the sound velocity and density of tissues in the head of the
Delphinus. The analysis was also done in a single parasagittal plane
making it a two-dimensional problem, but in reality the propagation in the
dolphin's head is a three-dimensional (3D) process and acoustic energy
reflected in the other planes could influence the resulting beam. Finally, it
was tacitly assumed that the air sacs of the dead dolphin would be the same as
a live phonating animal. However, the sound production process is very dynamic
(Dormer, 1979), with air being
pumped into the various sacs causing the shape and volume to be continuously
modified, making it extremely difficult to simulate.
The purpose of this study was to obtain empirical data on the pattern of
acoustic emissions from the porpoise head, and to consider how the melon or
other structures in the head might affect the click emission pattern. The
empirical data were obtained by measuring the sound field of echolocation
signals on the surface of head of two harbor porpoises. Although the
echolocation beam pattern of Phocoena phocoena has already been
measured (Au et al., 1999), it
is difficult to relate those results to the sound field on the head and to
determine where the axis of the beam is located on the head of the animal.
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Materials and methods |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussion and conclusionsReferences |
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). During the acoustic measurements the porpoise were kept in
two small enclosures (2 mx4 m) on one end of the floating pen structure.
Daan was approximately 5 years old, weighing 35 kg and measuring 135 cm in
length, whereas Jordy was about 2 years old, weighing 24 kg and measuring 120
cm in length.
Four specially constructed `suction cup' hydrophones were used to measure
echolocation signals, a technique first used by Diercks et al.
(Diercks et al., 1973). Each
hydrophone consisted of a cylindrical piezoelectric element similar to the
elements used in the Brüel and Kjaer 8103 hydrophones, but enclosed
within a suction cup constructed of degassed polyurethane compound (Uralite
3138). Each piezoelectric cylinder was made of PZT (lead zirconate titanate)
material with an outer diameter of 6.35 mm, a wall thickness of 1.15 mm and a
height of 6.35 mm. The diameter at the base of a suction cup when attached to
the porpoise measured 2.8 cm. The hydrophones were attached to the porpoises
in the three different configurations shown in
Fig. 1. The reference
hydrophone, denoted as R, was always placed at the same position for each of
the three array configurations. The suction cups were place on the animal
underwater to ensure that air was not trapped in the cups. The position of the
hydrophones during each trial was photographed to confirm their positions. A
trainer loosely held each porpoise by having her arms extended underneath the
animal, which was totally submerged while it scanned its environment with
echolocation clicks. A trial was accepted only if all the suction cups
remained on the animals throughout the trial. The suction cups were removed
after each trial.
The hydrophones were calibrated in a test tank using a sound projector and
a calibrated hydrophone for frequencies up to 150 kHz in 10 kHz increments,
and in 5 kHz increments for frequencies between 130 and 150 kHz. The average
sensitivity for frequencies between 130 and 150 kHz, frequencies typical of
Phocoena echolocation signals (Au
et al., 1999), was -219 dB re. 1 µPa for hydrophone-1, -218 dB
for hydrophone-2, -217 dB for hydrophone-3 and -219 for hydrophone-4. Accurate
hydrophone calibration was necessary since we considered the differences in
levels measured by each hydrophone. The response of all the hydrophones
dropped off rapidly at a rate of approximately 12 dB per octave beyond 140 kHz
so that the hydrophones also functioned as antialiasing filters.
Echolocation signals were digitized with two Gage-1210 (Montreal, QC, Canada), 12 bit dual simultaneous sampling data acquisition boards that were connected to a `lunch box' computer via two EISA slots. The data acquisition system operated at a sample rate of 500 kHz with a pre-trigger capability. When the computer signaled the Gage-1210 to collect data, four channels of acoustic signals were simultaneously and continuously digitized with the results going into separate circular memories on each Gage-1210 board. When an echolocation signal was detected by the reference hydrophone, it triggered the data acquisition board. 128 pre-trigger points and 128 post-trigger points were collected for each channel and saved to the computer. A maximum of 100 clicks were collected for each trial and the procedure was continued until a minimum of 300 total clicks were collected for each hydrophone geometry and each animal.
The shape and dimensions along the surface of each animal's head were measured when the porpoises were removed from the water for their weekly physical examination. The curvature of the head was measured by depressing a flexible shape-retaining `French' curve on different parts of the head and tracing the shape on a sheet of paper. The measurements were used to scale the animals to a CT scan of the same species of a similar size and age. The positions of the hydrophones were mapped on the 3D images in order to correlate the acoustic data with the anatomy.
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussion and conclusionsReferences |
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; Møhl and
Andersen, 1973; Wiersma,
1982). However, there were some lower amplitude components
following the main pulse (see Fig.
2) that were similar to measurements made in the near-field of a
bottlenose dolphin (Au, 1993).
The peak frequency for the 300 signals measured by the reference hydrophone in
the line configuration was 139.2±3.4 kHz for Daan and 138.6±6.2
kHz for Jordy (means ± s.d.).
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).
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The peak-to-peak acoustic pressure (mean ± s.d.) expressed in dB measured by the reference hydrophone was 180±6 dB re 1 µPa for Daan and 176±5 dB for Jordy. There was a significant effect of animal on click amplitude (one-way ANOVA, P<0.001, d.f.=1, F=1143). The higher amplitude signals emitted by Daan were consistent with Daan being larger and heavier than Jordy: 34 kg compared to 25 kg, respectively. The variation in the acoustic pressure probably reflects a natural variability in the sound production mechanism and also the variability in the relative amplitude of the signals measured by each hydrophone on a click-to-click basis.
The reference hydrophone always received the emitted signal before the
other hydrophones in the line configuration, for both animals. The relative
time between the reception of the signal by the reference hydrophone and the
other hydrophones was estimated by determining the cross correlating function
of the signal received by the reference hydrophone and the other hydrophones.
If we designate the digitized signal received by the reference hydrophone as
s2(k) and the digitized signal of another hydrophone as
si(k), where is k is the index of the digitized signal and
is equal to 1, 2,...n, and i denotes the specific hydrophone and has
values of 1, 3, 4, then the cross-correlation function of the two signals can
be expressed as
 |
where j is the number of samples si is being
delayed and can have values of 1, 2,... n,. The cross correlation
function is determined for a number of j values and the best time
estimate of the delay is at the j-value at which the correlation
function is maximum (Spiesberger and
Fristrup, 1990). The results of the time difference measurements
are given in Table 1, where
2-i is the time of arrival difference of the signal at
the reference hydrophone 2 and the i-th hydrophone. A one-way ANOVA analysis
and post-hoc Tukey test revealed that time differences
2-4 and 2-3 were not
statistically different in both animals but 2-1 was
significantly different from the other two time differences for both animals
(P<0.05, d.f.=2, F=142 for Daan and F=14 for
Jordy). The results for both animals show relatively good consistency, with
hydrophone-2 receiving the signal first, followed by hydrophone-1 with a delay
between 14.5-15.5 µs, and the signals arriving at hydrophones -3 and -4
being delayed between 19.1-21.4 µs.
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The results obtained with the T1 and T2 configurations are shown in Fig. 4B. For each array configuration, the mean value of each hydrophone output was referenced to the mean sound pressure level measured by the reference hydrophone. The reference hydrophone measured the highest voltage for each configuration and its level was set to 0 dB. The results of the two configurations were then combined so that a more complete appreciation can be obtained on how sound varied on the head of the porpoises. Fig. 4A shows two CT scans, the top one showing a horizontal slice through the phonic lips and the bottom scan showing a parasagittal slice with the color dots indicating the approximate position of each hydrophone.
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There were several instances in the data in which there were changes in the relative amplitudes of the signals with respect to the reference hydrophones that occurred on consecutive clicks. Examples of such changes with the porpoise Daan for three consecutive clicks observed with the line array geometry are shown in Fig. 5 and for the T1 array geometry in Fig. 6. The changes in the relative amplitude of the signals can best be seen by comparing the signals received by hydrophones -1, -3 and -4 with that received by hydrophone-2 (the reference hydrophone). In Fig. 5, the amplitude of the signal detected by hydrophone-1 decreased progressively relative to the signal detected by hydrophone-1 for the three consecutive clicks. In Fig. 6, the amplitude of the first click detected by hydrophones -1 and -2 is almost equal. However, the second click on hydrophone-1 is lower than that of hydrophone-2. The third click on hydrophone-1 is even lower compared to hydrophone-2. Since the hydrophones are fixed in position, the changes in the relative amplitude can only have occurred because of changes in the trajectory that the signals follow to each hydrophone, probably caused by the manner in which the signals were produced and the positional conformation of the air sacs. The interclick intervals were in the 20-40 ms range so that mechanical adjustment of the melon was highly unlikely. Similar examples of changes can be obtained for the porpoise Jordy.
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Discussion and conclusions |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussion and conclusionsReferences |
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The acoustic pressure dropped off rapidly for hydrophone positions away
from the region of maximum value higher up the forehead (towards the
blowhole), as indicated by the 12 dB reduction in the level detected by
hydrophone-3 compared to hydrophone-2 for Daan and 17 dB for Jordy in
Fig. 3. This dramatic reduction
in the acoustic level may be explained by the presence of a dense connective
tissue blanket or theca (Cranford et al.,
1996), which surrounds the posterior aspect of the melon and
extends beyond the blowhole anteriorly, creating a megaphone-like funnel that
envelops the posterior aspect of the melon and sound generation apparatuses.
The dense connective tissue theca provides a significant impedance mismatch
that could channel sound forward and shield the hydrophones above that
region.
The CT scan image in Fig. 3
show the assumed sound source to be much closer to hydrophones -3 and -4 than
both the reference hydrophone and hydrophone-1, yet the reference hydrophone,
which was aligned with the low-velocity core of the melon, always received the
emitted signal first for both animals, followed by hydrophone-1. This can only
happen if the propagation pathways to hydrophones -3 and -4 were much longer
than the pathway to the reference hydrophone, suggesting that the signals
received by hydrophones -3 and -4 were probably reflected off either an air
sac or the top of the upper jaw or both, and the signals received by the
hydrophones -1 and -2 travel in a more direct manner through the head of the
porpoises. Unfortunately, the signals received by hydrophones -3 and 4 were
attenuated, making it difficult to unequivocally determine if the signals are
phase inverted as they should be if they reflected off an air sac. The reason
for the apparent absence of a direct pathway from the source to hydrophones -3
and -4 is unclear but may be related to the previously mentioned dense theca
of connective tissue surrounding the posterior portion of the melon. The 256
µs of pre-trigger points based on the channel monitoring the reference
hydrophone would allow for the acquisition of any direct signals from the
region of the sound generator to hydrophones -3 and -4. It is beyond the scope
of this study to examine the different pathways that the signals travel
through the head of the porpoises. Such an examination of pathways would
probably require a CT scan, preferably of a live porpoise, and some sort of
numerical simulation of the sounds propagating in the porpoise head as was
done for the common dolphin (Aroyan et al.,
1992). Suffice it to state here that the time of arrival
difference results suggest that acoustic propagation within the head of a
porpoise is complex and not well understood.
The results in Fig. 4, along with the time of arrival data, suggest that sounds propagating through the melon of the porpoises are being channeled by the melon and that the region of maximum acoustic pressure on the surface of the porpoise head approximately coincides to a low density path from the phonic lips through the center of the melon to the surface of the head.
The averaged peak-to-peak acoustic pressure measured by the reference hydrophone was 4 dB greater for Daan than for Jordy. Daan consistently emitted higher amplitude signals than Jordy. Daan was longer (135 cm versus 120 cm) and heavier than Jordy (34 kg versus 25 kg), suggesting a significant effect of animal size and weight on click amplitude. It is reasonable to speculate that higher amplitudes may have been related to the ability to recruit greater muscle mass by the larger animal to generate signals. The variation in the acoustic pressure may also reflect natural variability in the sound production mechanism.
It should be emphasized that our measurements were in the near-field of the
porpoises' head and therefore the signals will be distorted when compared to
what is obtained in the far-field (Au et
al., 1978). There are secondary components in the waveforms that
are probably the results of reflections of the signal within the head of the
animals. Therefore, we resisted any temptation to perform detailed analysis of
the frequency characteristics of the signals, except for determining the peak
frequency obtained by the reference hydrophone in the line array
configuration. The relationship between what is measured in the near-field to
what is radiated into the far field is a subject that has not received much
attention.
One of the difficulties in measuring echolocation signals in free-ranging
dolphins and porpoises is the uncertainty whether or not changes in either the
shape or amplitude of the received signals are caused by changes in the
orientation of the animal with respect to the hydrophone. In our situation,
the suction cups were stationary so that any variations in the relative
amplitude of the signals probably occurred within the animals. Using two
simultaneous high-speed video endoscopic recordings, Cranford observed that
clicks were produced in Tursiops truncatus by pushing air across the
phonic lips, setting the associated tissue complex into vibration
(Cranford, 2000). In some
situations, the right phonic lips were vibrating with the left being
relatively quiescent while in other situations, the left phonic lips were
vibrating with the right remained motionless. There were also occasions in
which pulses of air actuated both the left and right phonic lips. In each of
these situations, the clicks would propagate through the head along different
trajectories. Furthermore, air has been observed to pass through different
portions of a pair of phonic lips while the animal produced a single click
train. Unfortunately, the results of this study alone are inadequate to
suggest the most probable cause of the variations in the relative amplitude of
the echolocation signals.
Our measurements have provided empirical confirmation of the melon focusing
hypothesis proposed by Norris and coworkers
(Norris, 1968;
Norris and Harvey, 1974). The
foreheads of the porpoises in this study, as with all odontocetes, were very
smooth with few clear and useable landmarks. Therefore, our hydrophone
placements could only be within about ±0.5 cm accuracy. Furthermore,
the diameter of the suction cups did not allow for any two adjacent elements
to be nearer than about 2.8 cm. While other structures in the head of
odontocetes including the skull and air sacs play a role in the formation of
the sonar beam (Aroyan et al.,
1992; Goodson et al.,
2003), our results indicate the important role of the melon and
the connective tissue theca in channeling the sound as it exits the head of a
porpoise, forming a directional echolocation beam.
We have determined the general location where sound exits the head and have also shown that echolocation signals can propagate along slightly different trajectories within the head, probably because of the manner in which the signals are produced. Therefore, the transmission beam pattern will also vary on a click-to-click basis if the signal trajectory varies. This study has provided the first data to suggest that the porpoise can make fine adjustments to the transmission beam by manipulating the manner in which the signals are produced and propagated through the head.
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Acknowledgments |
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