Testing the odontocete acoustic prey debilitation hypothesis:
No stunning results
Kelly J. Benoit-Bird
College of Oceanic and Atmospheric Sciences, Oregon State University, 104 COAS Administration Building,
Corvallis, Oregon 97331, and
Hawaii Institute of Marine Biology, University of Hawaii, PO Box 1106, Kailua, Hawaii 96734
Whitlow W. L. Au
Hawaii Institute of Marine Biology, University of Hawaii, P.O. Box 1106, Kailua, Hawaii 96734
Ronald Kastelein
SEAMARCO, Julianalaan 46, 3843 CC Harderwijk, The Netherlands
共Received 19 January 2006; revised 9 May 2006; accepted 12 May 2006兲
The hypothesis that sounds produced by odontocetes can debilitate fish was examined. The effects
of simulated odontocete pulsed signals on three species of fish commonly preyed on by odontocetes
were examined, exposing three individuals of each species as well as groups of four fish to a
high-frequency click of a bottlenose dolphin 关peak frequency 共PF兲 120 kHz, 213-dB peak-to-peak
exposure level 共EL兲兴, a midfrequency click modeled after a killer whale’s signal 共PF 55 kHz,
208-dB EL兲, and a low-frequency click 共PF 18 kHz, 193-dB EL兲. Fish were held in a 50-cm
diameter net enclosure immediately in front of a transducer where their swimming behavior,
orientation, and balance were observed with two video cameras. Clicks were presented at constant
rates and in graded sweeps simulating a foraging dolphin’s “terminal buzz.” No measurable change
in behavior was observed in any of the fish for any signal type or pulse modulation rate, despite the
fact that clicks were at or near the maximum source levels recorded for odontocetes. Based on the
results, the hypothesis that acoustic signals of odontocetes alone can disorient or “stun” prey cannot
be supported. © 2006 Acoustical Society of America. 关DOI: 10.1121/1.2211508兴
PACS number共s兲: 43.80.Ka, 43.80.Nd 关JAS兴
I. INTRODUCTION
The idea that odontocete cetaceans can use sound to
debilitate their prey was first proposed by Bel’kovich and
Yablokov 共1963兲 and later reviewed by Norris and Mohl
共1983兲. Odontocetes, or toothed whales, a group of approximately 70 species in six families, are predators that feed on a
range of prey including cephalopods, crustaceans, fish, birds,
and other marine mammals. As a group, they rely on sound
for orientation, navigation, communication, and predator and
prey detection 共Reynolds and Rommel, 1999兲. It has been
proposed that loud, impulsive sounds made by cetaceans in
the vicinity of prey can stun, disorient, and debilitate their
prey, rather than just being used to find prey.
Support for the prey-stunning hypothesis includes observations of dolphins in laboratory and field settings. Data that
sperm whales have intact squid lacking any bite marks in
their stomachs led Norris and Mohl 共1983兲 to suggest that
the squid, rapid swimmers that are highly maneuverable,
must be immobilized by the whale before consumption. A
number of observations 共summarized in Marten et al., 2001;
summarized in Norris and Mohl, 1983兲 that fish appeared
lethargic and fish schools were depolarized by feeding dolphins in both captive and wild circumstances have been considered consistent with prey stunning by dolphins, though the
mechanism has not been tested.
Evidence to support the prey-stunning hypothesis also
comes from results that show acoustic signals can indeed
1118
J. Acoust. Soc. Am. 120 共2兲, August 2006
Pages: 1118–1123
cause a loss of buoyancy control, abdominal hemorrhage,
and even death in fish. Explosives including TNT and dynamite with exposure levels between 229 and 234 dB and
black powder with an exposure level between 234 and
244 dB have been shown to cause debilitation 共Hubbs and
Rechnitzer, 1952兲. Spark discharges with exposure levels between 230 and 242 dB can cause similar effects on fish 共Zageski, 1987兲, though negative results have been reported for
some cephalopods 共Mackay and Pegg, 1988兲. An airgun exposing fish to an average of 216 dB peak-to-peak has been
shown to cause death and debilitation in fish after multiple
exposures over several hours 共Marten et al., 2001兲. Acoustic
stunning of some fish has also been shown from highamplitude pure tones 共Hastings, 1995兲. Most of the acoustic
signals that have experimentally shown to cause prey debilitation have rapid rise times 共several tens of microseconds or
less兲 and high pressures 共⬎210 dB peak-to-peak兲, as do dolphin clicks. However, most of the received threshold levels
shown to cause responses to these sounds are 10 to 25 dB
above the maximum intensity recorded for dolphin clicks
共Au, 1993兲. In other words, they contain about 300 times
more energy than a single echolocation click. Only repeated
exposure to the airgun every 15 s for 4 h caused debilitation
at received sound levels reported for dolphin sounds.
Perhaps the most interesting evidence towards potential
prey stunning by odontocetes comes from a very different
animal taxa. Snapping shrimp produce broadband, impulsive
sounds that reach source levels of 220 dB peak-to-peak
0001-4966/2006/120共2兲/1118/6/$22.50
© 2006 Acoustical Society of America
共Schmitz et al., 2000兲. Snapping shrimp have been shown to
stun their prey using a single snap 共Herberholz and Schmitz,
1999兲. Although it is not known if the mechanism for stunning by snapping shrimp is the sound itself or the mechanical
stress caused by the cavitating bubble or the jet of water,
these are some of the first data to suggest that a biologically
created sound, rather than anthropogenic sounds, could cause
debilitating effects on prey and serve a predatory function.
While the hypothesis that odontocete signals can directly
cause debilitation in their prey has not been directly tested,
the hypothesis has been attractive to both scientists and the
popular media. In the last decade, Norris and Mohl’s 1983
synthesis of the hypothesis has been cited 35 times. Some of
these papers invoke acoustic prey stunning as a mechanism
to explain their results despite the lack of direct support for
the mechanism. Media coverage of papers that have discussed the prey-stunning hypothesis 共Cranford, 1999; Marten
et al., 2001兲 has included dramatic headlines such as “Killer
clicks” 共New Scientist, 31 January 2001兲 and “Porpoise stun
gun” 共Science Frontiers No. 29: Sep–Oct 1993兲. The Santa
Cruz County Sentinel 共26 April 1998兲 summarized one study
saying, “mysterious monsters are killing fish with murderous
death beams.” The general acceptance of the hypothesis by
both professional and lay people led us to attempt a direct
test of the hypothesis that odontocete acoustic signals can
debilitate or disorient prey.
II. METHODS
A. Study area
The experiment was conducted in an outdoor tank at the
field station of the Netherlands National Institute for Coastal
and Marine Management 共RIKZ兲 at Jacobahaven, Zeeland,
The Netherlands in a freestanding rectangular tank 7.0 m
long and 4.0 m wide with a water depth of 2.0 m. The tank
rested on a 3-cm-thick layer of hard-pressed Styrofoam to
reduce contact noise from the environment and was covered
by a canopy to improve the clarity of video recordings. The
water in the tank was pumped directly from the nearby Oosterschelde 共a lagoon of the North Sea兲. The salinity was 30%–
33%, the pH 7.9–8.1, nitrogen concentration ⬍5 mg/ l, and
nitrate concentration ⬍0.1 mg/ l. The water was circulated
via a sand, UV light, and carbon filter. To make the environment inside the tank as quiet as possible, the filter unit had a
low-noise “whisper” pump. To reduce contact noise entering
the pool, the pump and filter unit were also placed on hardpressed rubber. Water parameters 共temperature, salinity, oxygen, and nitrate兲 were measured daily and remained well
within the boundaries suitable for normal activity of the fish.
B. Subjects
We tested the effects of simulated odontocete clicks on
three species of fish: Atlantic herring 共Clupea harengus兲, sea
bass 共Dicentrarchus labrax兲, and Atlantic cod 共Gadus
morhua兲. The Animal Welfare Commission of the Netherlands government stipulated that the fish used must feed
readily in captivity, so they had to come from aquaria,
though all were originally wild-caught. Sea bass and cod
were fed to satiation each day after the sessions on a diet of
J. Acoust. Soc. Am., Vol. 120, No. 2, August 2006
FIG. 1. Experimental setup. The fish is enclosed in monofilament enclosure
next to an acoustic transducer. While in the cage, the subjects were videotaped from above and from the side.
raw fish. Herring were similarly fed a diet of Trouvit pellets
size no. 00 共Nutreco Aquaculture兲. Fish were returned to the
aquaria following the experiment to comply with animal care
regulations.
Fish species were chosen to represent a variety of swimbladder types because of the hypothesis that the mechanism
of fish debilitation is the interaction of the acoustic signal
with air-filled cavities in the fish. The herring species has a
modified form of the primitive swimbladder as a physostome, with air bladder extensions to the lateral line and labyrinth 共Blaxter et al., 1979; 1981兲. Species in this family have
been shown to be especially sensitive to sound including
high frequencies 共Mann et al., 1997兲 and the Pacific herring
共Clupea pallassi兲 and American shad 共Alosa sapidissima兲
have even been shown to respond to echolocation signals
共Mann et al., 1998; Wilson and Dill, 2002兲. We hypothesized
that the herring was the most likely candidate for stunning
because of these anatomical adaptations. Sea bass is a euphysoclistous fish; they are physostomous as juveniles but
physoclistous as adults 共Chatain, 1986兲. Cod have the most
derived swimbladder form, a completely closed physoclist
bladder. The swimbladder has also been shown to play a role
in the hearing abilities of cod 共Sand and Enger, 1973兲. If
debilitation occurred, the variety of swimbladder types used
could help elucidate the mechanism of acoustic interaction
with the fish.
C. Experimental setup
For testing, fish were placed inside a 0.5-m-diameter,
0.3-m-high cylindrical monofilament enclosure supported by
a plastic ring on the top and bottom 共Fig. 1兲. This allowed the
fish to swim freely while keeping the subjects positioned in
front of the transducer producing the stimulus. The enclosure
was suspended 1 m below the water’s surface with the
acoustic transducer placed immediately adjacent to the enclosure, making the subject fish, on average, 0.25 m away
from the source of the stimuli. Two underwater video cameras were focused on the net enclosure, one looking directly
down on the enclosure from above, and one looking from the
side, directly across from the transducer. These cameras alBenoit-Bird et al.: Acoustic prey stunning by odontocetes
1119
FIG. 2. Acoustic stimuli used in the experiment were three synthetic odontocete echolocation signals recorded using the calibration hydrophone. The
waveforms 共time-amplitude plots兲 of each signal are shown on the left, and
the spectra 共frequency-amplitude兲 plots on the right.
lowed us to observe the behavior of the fish without causing
disturbance, and permitted us to make sure the fish was centered in front of the acoustic transducer when the stimulus
was presented. The size of the enclosure was a compromise
between allowing fish movement and controlling exposure
level. Previous studies of stunning have observed loss of
buoyancy control and changes in small-scale swimming behavior which this size enclosure should not limit.
Individual fish or fish in groups of four were placed
inside the enclosure and allowed to acclimate to their new
conditions for at least 30 min. The behavior of the fish was
recorded using the two video cameras for 5 min prior to the
presentation of the acoustic stimuli and 5 min postexposure
for comparison. The hypothesis was that fish would be dramatically affected by the presentation of clicks so we looked
for changes in activity level that would indicate avoidance or
loss of swimming ability as well as changes in tilt or roll
angle of greater than 30 deg, indicating loss of buoyancy
control. We also looked for fish survival for 1 week following the experiments as an indication of long-term internal
damage. We were prepared to immediately euthanize any fish
that appeared to be in extreme distress immediately following acoustic exposure.
D. Stimuli
A variety of odontocete species have been hypothesized
to debilitate their prey with echolocation clicks, so we simulated clicks of three different species in our experiment. The
clicks as recorded by a calibration hydrophone are shown in
Fig. 2. Clicks were produced using a function generator computer plug-in board with a sampling rate of 1 MHz. We measured the source level and the exposure level of each signal
using a calibrated B&K 8103 hydrophone placed at a variety
of ranges from the transmit transducer; the results are shown
in Fig. 3. The first signal we tested, a bottlenose dolphin
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J. Acoust. Soc. Am., Vol. 120, No. 2, August 2006
FIG. 3. The measured sound-pressure level of each of the three signals as a
function of range from the source transducer. The levels the fish were exposed to at the center of the cage, indicated by the paired lines, were calculated based on these curves.
共Tursiops truncatus兲 click, had a peak frequency of 120 kHz
and a source level of 203 dB re : 1 ␮Pa peak-to-peak, exposing fish in the middle of the cage to levels of
213 dB re : 1 ␮Pa peak-to-peak. This signal was produced
using a custom-built planar transducer consisting of a 1–3
composite piezoelectric element of 6.4 cm diameter. This
transducer has a 12.5-deg beamwidth in the far field, and
though its beamwidth in the near field is unknown, subject
fish were often directly in front of the transducer during the
experiment, exposing them to the highest possible sound levels. The second signal, a killer whale 共Orcinus orca兲 click
共Au et al., 2004兲, had a peak frequency of 55 kHz and had a
source level of 200 dB re : 1 ␮Pa peak-to-peak, exposing
the fish to a level of 208 dB re : 1 ␮Pa peak-to-peak. The
final, low-frequency click had a peak frequency of 18 kHz
and a source level of 187 dB re : 1 ␮Pa peak-to-peak, exposing the fish to 193 dB re : 1 ␮Pa peak-to-peak 共Fig. 3兲.
Both of these lower-frequency signals were produced using a
custom-built transducer consisting of three piezoelectric ceramic spheres having diameters of 5.0, 3.8, and 1.3 cm and
stacked in a column. Each sphere has a different resonance
frequency and the three were driven in parallel so that the
transducer has a low directivity index. The frequency range,
duration, amplitude, and energy flux density of each of the
three simulated clicks were comparable to the clicks produced by a range of odontocete species, providing comparable acoustic exposure to natural clicks, and thus should
affect the subjects in the same way as natural clicks.
Benoit-Bird et al.: Acoustic prey stunning by odontocetes
Clicks were presented to three individual sea bass and
three individual cod as well as groups of four individuals of
each species in two ways. The first was at static, regular
pulse rates of 100, 200, 300, 400, 500, 600, and 700 clicks/
second for exposure times ranging from a minimum of 7 s
up to 1 min. This type of click presentation is most similar to
regular echolocation by odontocetes at close ranges 共less
than 0.4 m, Evans and Powell, 1967兲. We also presented
clicks in modulated pulse “sweeps.” Clicks repetition rate
increased from 100 to 700 clicks/ s over either 1.1, 2.2, or
3.2 s. This click pattern is similar to the “terminal buzz”
produced by echolocating animals as they make the final
approach to a target 共Au, 1993兲. We presented this signal
type to three individuals cod and three individual herring as
well as to a group of four cod and a group of four herring.
E. Behavioral parameters
To observe effects on buoyancy control, the video data
were used to determine the tilt and roll angle of each fish in
both individual and group tests every minute for the 15 min
pre- and postsound exposure. To determine if fish avoided
the sound’s source, the percent of time each fish spent in
each quadrant of the cage was recorded for the pre- and
postexposure observation periods. To measure fish movement, the number of times each fish crossed between the
quadrants of the cage was compared from pre- and postexposure periods.
FIG. 4. The distribution of fish roll 共top兲 and tilt 共bottom兲 angles before and
after exposure to the acoustic stimulus. An angle of zero represents a vertical
orientation. There were no significant differences between pre- and postexposure periods and no significant effects of species, number of animals in
the cage, or signal type, so all stimuli and fish species results are pooled in
this graph.
F. Statistics
Tilt and roll angle of each fish in both individual and
group tests every minute for the 15-min pre- and postsound
exposure was compared using a repeated-measures analysis
of variance 共ANOVA兲. A series of paired t-tests was used to
compare the pre- and postexposure quadrant residence time
for each fish to determine if fish avoided the transducer. To
measure fish movement, the number of times each fish
crossed between the quadrants of the cage was compared
from pre- and post-exposure periods using a paired t-test.
III. RESULTS
No clear changes in behavior were observed during the
relatively short ensonification period. To observe effects on
buoyancy control, the video data were used to determine the
tilt and roll angle of each fish in both individual and group
tests every minute for the 15-min pre- and postsound exposure 共Fig. 4兲. A repeated-measures ANOVA revealed no significant differences between pre- and postexposure angles
and showed no interaction of this with signal type, the number of fish in the cage, or species 共Tables I and II, p ⬎ 0.05兲.
To determine if fish avoided the sound’s source, the percent of time each fish spent in each quadrant of the cage was
recorded for the pre- and postexposure observation periods.
A series of paired t-tests was used to compare the pre- and
postexposure quadrant residence time for each fish 共Table
III兲. No significant differences were observed in any of the
four quadrants 共p ⬎ 0.05兲. This suggests that there was no
avoidance of the sound’s source.
To measure fish movement, the number of times each
fish crossed between the quadrants of the cage was compared
from pre- and postexposure periods using a paired t-test. No
TABLE I. Repeated-measures ANOVA for fish roll angle pre- and postexposure to acoustic stimuli.
Source
Pre vs post
*Signal
*Group size
*Species
*Signal *Group size
*Signal *Species
*Group size *Species
*Signal *Group size *Species
Error 共pre vs post兲
J. Acoust. Soc. Am., Vol. 120, No. 2, August 2006
SS
df
MS
F
p
31.61
1095.51
57.13
30.19
886.39
1676.07
1.10
635.66
9664.05
1
18
1
2
13
36
1
12
168
31.61
60.86
57.13
15.09
68.18
46.56
1.10
52.97
57.52
0.55
1.06
0.99
0.26
1.19
0.81
0.02
0.92
0.46
0.40
0.32
0.77
0.29
0.77
0.89
0.53
Benoit-Bird et al.: Acoustic prey stunning by odontocetes
1121
TABLE II. Repeated-measures ANOVA for fish tilt angle pre- and postexposure to acoustic stimuli.
Source
Pre vs post
*Signal
*Group size
*Species
*Signal *Group size
*Signal *Species
*Group size *Species
*Signal *Group size *Species
Error 共pre vs post兲
SS
df
MS
F
p
196.23
5893.71
213.63
1085.74
5231.02
10284.76
183.00
5910.46
54943.68
1
18
1
2
13
36
1
12
168
196.23
327.43
213.63
542.87
402.39
285.69
183.00
492.54
327.05
0.60
1.00
0.65
1.66
1.23
0.87
0.56
1.51
0.44
0.46
0.42
0.19
0.26
0.68
0.46
0.13
significant difference was observed 共mean difference
=0.0044± 0.0016 95% CI, t = 0.62, df= 170, p = 0.43兲.
We did not have any mortality or even slight abnormal
behavior of our subjects, indicating no severe internal injuries from the testing.
IV. DISCUSSION
We did not observe any measurable changes in the behavior of any of the species of fish in any of the conditions
we tested either during or following exposure to odontocete
clicks. There were no noticeable changes in swimming activity, no apparent loss of buoyancy control that would be indicated by tilting or rolling of the fish, and no movement away
from the transducer. In order for prey stunning by regular or
terminal buzz clicks to be a viable mechanism for fish capture by odontocetes, the fish would need to be dramatically
and noticeably affected by the acoustic signals, which was
not apparent in our results. In addition, we did not have any
mortality of the tested fish, which might indicate internal
damage from the acoustic signals.
We tested a large number of variables including the frequency of the signal, pulse rate, and pulse sweeping. Our
choice of the three signal types was to ensure that a wide
frequency range was covered in the event that stunning
might have a frequency dependency. These signals also covered the full range of frequencies employed by odontocetes
from the relatively low frequency in the range used by the
sperm whale to the high-frequency bottlenose dolphin. Fish
in our experiment were subjected to very high levels of
sounds for exposure times that are long relative to odontocete acoustic behavior during foraging.
Norris and Mohl 共1983兲 proposed that the final click
sweep, or terminal buzz, was the most likely signal to induce
fish stunning. These non-“usual” clicks have very short in-
terclick intervals 共Madsen et al., 2005; 2002兲 with between
50 and 200 clicks per second. The clicks in this terminal
phase as the odontocete closes in on the prey are typically
lower in amplitude than “regular” echolocation clicks, by
about 15 dB. Our terminal buzz signals reached 700 pulses
per second for 7 s to 1 min, with a maximum amplitude of
213 dB re : 1 ␮Pa. We can describe a pulsed odontocete signal, p共t兲, using the normalized waveform method of Au
共1993兲 as
A pp
sN共t兲,
2
p共t兲 =
共1兲
where A pp is the peak-to-peak amplitude in ␮Pa and sN is the
normalized waveform. The energy flux density of a single
click will be
e=
A2pp
4␳c
冕
T
sN共t兲2dt =
0
A2pp
1
u. ,
4
␳c
共2兲
where u=the integral of the square of the normalized waveform and T is the duration of the waveform. The total energy
flux density for N clicks will be simply
eT = N
A2pp
1
u. .
4
␳c
共3兲
In the extreme experimental condition of 700 clicks per
second for 7 s to 1 min time period, we exposed fish subjects
to over 8 to 70 关from Eq. 共3兲兴 times more acoustic energy
than would an odontocete emitting terminal buzz signals
with a peak-to-peak SPL of 213 dB 共4.5⫻ 1010 ␮Pa兲 at a rate
of 200 clicks per second for 3 s 共Madsen et al., 2005兲. Even
if we assume an odontocete emitting terminal buzz signals at
twice the amplitude 共9 ⫻ 1010 ␮Pa兲 at the same repetition
rate and duration, our extreme case would represent 2 to 17
TABLE III. Paired sample t-tests comparing pre- and postexposure time spent in each quadrant of the cage by
each fish. All species were pooled in this analysis.
95% Confidence interval of the difference
Quadrant
A
B
C
D
1122
Mean paired differences
Lower
Upper
t
df
p
−0.0034
−0.0060
0.0007
0.0087
−0.0118
−0.0127
−0.0073
−0.0049
0.0050
0.0007
0.0087
0.0223
−0.80
−1.78
0.17
1.27
170
170
170
170
0.43
0.08
0.86
0.21
J. Acoust. Soc. Am., Vol. 120, No. 2, August 2006
Benoit-Bird et al.: Acoustic prey stunning by odontocetes
times more acoustic energy. In most of our experimental conditions, the fish subjects were exposed to more acoustic energy than would be expected for animals in the wild based on
the observations of wild odontocete foraging.
We tested these signals on multiple individuals of different sizes representing three species commonly consumed by
odontocetes. These fish were selected based on their potential as prey species, their swimbladder morphology, and their
availability in captivity. It has been proposed that acoustic
signals can interact with the air-filled swimbladder to result
in stunning. We chose a physoclistous, euphysoclistous, and
physostomous fish species to be able to test for this effect,
though no differences in response were exposed. We also
tested any group effects by exposing groups of four individuals of a single species together. We did not observe any
changes in coordination or coherence of individual fish
within the groups.
If stunning does occur in the wild, its induction may
require a stress other than or in addition to the acoustic signal. Perhaps additional sensory cues are required. For example, perhaps the fish are stressed or stunned by seeing a
large predator or by the pressure wave created by the dolphins as they approach their prey. Another possible explanation is that the odontocete acoustic behavior that induces
stunning is different than has been described by previous
studies. For example, the “bang” sound reported by 共Marten
et al., 2001兲. These relatively long, high-amplitude sounds
were recorded in the wild and in the laboratory. However,
their source, the phonation system or a body movement like
a tail slap, is not known. Despite the use of signals near the
maximum source levels recorded for odontocete clicks, we
could not induce stunning or even disorientation in the fish
tested. Our results do not support the hypothesis that odontocetes use their clicks alone to induce stunning in prey.
ACKNOWLEDGMENTS
We thank Sander van de Huel for assistance conducting
the experiments. Jan van der Veen, Sea aquarium “het Arsenaal,” The Netherlands, lent us most of the study animals,
and Gerard Visser, Michaël Laterveer, and Peter van Putten
共all of the Oceanium Department of Blijdorp Zoo兲, provided
the herring and transported them to the study site. Gijs Rutjes
共Coppens International兲 provided some of the sea bass. We
thank Mardi Hastings for valuable discussions about this
work and Brigitte Kastelein and the volunteers of SEAMARCO for logistical support. The facilities of the research station were made available thanks to Dick Vethaak 共RIKZ兲,
Roeland Allewijn 共RIKZ兲, and Wanda Zevenboom 共North
Sea Directorate兲. This work was supported by the U.S. Office
of Naval Research and the Netherlands Ministry for Agriculture, Nature, and Food Quality 共DKW-program 418: North
Sea and Coast. This project complied to the Dutch standards
for animal experiments 共Chris Pool, head of the Committee
J. Acoust. Soc. Am., Vol. 120, No. 2, August 2006
for Animal Experiments of RIKZ兲 and was conducted under
University of Hawaii Animal Care Protocol 04-019. This is
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