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First published online June 13, 2008
Journal of Experimental Biology 211, 2079-2086 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.015081
The responses of Atlantic cod (Gadus morhua L.) to ultrasound-emitting predators: stress, behavioural changes or debilitation?
1 Zoophysiology, Department of Biological Sciences, University of Aarhus, Bldn.
1131, 8000 Aarhus C, Denmark
2 Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA
* Author for correspondence (e-mail: henriette{at}post.au.dk)
Accepted 16 April 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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),
and changes in behaviour and in life history strategies
(Lima and Dill, 1990).
Predators can thus potentially cause stress and behavioural changes in a much
greater number of prey than they successfully track and catch
(Ripple and Beschta,
2004).
The use of intense ultrasound to echolocate fish and squids has been
employed by toothed whales since the Oligocene between 37 and 28 million years
ago (Fordyce and Barnes, 1994).
Therefore, a significant evolutionary pressure
(Clarke, 1996) has been present
that may have induced the development of ultrasound detection in fish that,
like the Atlantic cod (Gadus morhua), are preyed upon by toothed
whales (Santos et al., 2001).
Such ultrasonic interfaces in the sensory arms race between predators and prey
have been documented for bats and moths
(Miller and Surlykke, 2001),
and also suggested for toothed whales and their prey
(Astrup, 1999;
Wilson et al., 2007).
Recently, on an evolutionary timescale, humans have been added to the list
of ultrasound-emitting predators that target cod. The Atlantic cod has been a
very important fish in world fisheries for more than five centuries
(Jónsson, 1994;
Øiestad, 1994), and are
now commonly sought using echosounders with source level sound pressures up to
230 dB re. 1 µPa (pp) (Simmonds and
MacLennan, 2005) – comparable in peak pressure with the
maximum levels produced by toothed whales
(Au, 1993). If Atlantic cod has
developed ultrasonic hearing in response to predation from echolocating
toothed whales (Astrup, 1999),
any ultrasound detected above a specific threshold should elicit an
anti-predator response and therefore also be a source of potential short- or
long-term stress. Artificial ultrasonic sound sources, such as echosounders
would then be expected to have similar negative effects on cod, possibly along
with ultrasound pingers used to reduce the by-catch of small cetaceans
(Kastelein et al., 2007).
Most cod stocks in the north Atlantic have undergone severe decreases in
numbers (Garrod and Schumacher,
1994) and strict management has been implemented in an attempt to
sustain population numbers. Although this management has mostly focused on
reducing catches through minimizing quotas, stress and behavioural changes
have received little attention. These issues should be taken into
consideration as they have implications for both recruitment
(Morgan et al., 1999) and
vulnerability to diseases (Pickering and
Pottinger, 1989; Schreck,
1996).
In fact, Astrup and Møhl (Astrup
and Møhl, 1993) did report that Atlantic cod can be
conditioned to detect high intensities of ultrasound and suggested that this
capability evolved to detect and avoid echolocating toothed whales
(Astrup, 1999). Through
conditioning with mild electrical shocks, they determined the detection
threshold to be 203 dB re. 1 µPa (pp) for an echosounder pulse at 38 kHz,
and on those grounds estimated that a cod should be able to detect an
approaching toothed whale at a range of 10–30 m
(Astrup and Møhl, 1993).
Atlantic cod in the North Sea are commonly found at depths less than 30 m and
echosounders should thus be detectable by cod throughout the entire water
column when ensonified by the beam of the downward-directed transducer. From
the findings of Astrup and Møhl
(Astrup and Møhl, 1993),
it follows that ultrasound-detecting cod should react to ultrasound-emitting
predators if this capability has evolved as an anti-predator response. Such
anti-predator responses have recently been documented for another family of
fish: the ultrasound-hearing shad (Alosinae) species
(Mann et al., 2001;
Mann et al., 1998;
Wilson et al., 2008). In
addition, much stronger effects of ultrasound have been proposed by Norris and
Møhl (Norris and Møhl,
1983) who advanced the hypothesis that very high intensities of
ultrasound might have a momentary debilitating effect on fish that could
facilitate capture.
In this study, we test these hypotheses on the effects of high-intensity ultrasound on cod and discuss the findings in the light of toothed whale echolocation and fisheries acoustics. We test the effects of intense ultrasound in terms of a short-term stress response, behavioural responses and acoustic debilitation. It is demonstrated that intense ultrasound does not elicit short-term stress or anti-predator responses, and that very high sound intensities have no apparent debilitating effect on Atlantic cod. Contrary to previous studies, it is concluded that intense ultrasound most probably plays no role in predator–prey interaction between cod and their ultrasound-emitting predators.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). The experiments took place in the period October 2006 to July 2007 on Atlantic cod caught in the North Sea off Denmark. Heart rate and debilitation experiments were carried out in a 3x4x6.5 m sea water tank (Figs 1 and 2) at the North Sea Museum in Hirtshals. Behavioural experiments were conducted at the Fisheries and Maritime Museum in Esbjerg in a 3.35x3.5x10 m exhibition aquarium. All cod were allowed to recover in holding tanks at least 1 month prior to experimentation, and all displayed normal behaviour and were feeding prior to the experiment.
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The fish were anaesthetized in a 0.4 mmol l–1 benzocaine (Sigma) solution and placed ventral side upwards on an operating desk. Teflon-coated stainless steel electrodes (125 µm in diameter) were placed on either side of the heart by inserting a syringe holding the tip of the electrode under the pelvic girdle and pushing it anteriorly approx. 2 cm. When the electrode was in place, a loop was made on the electrode just where it penetrates the skin. A suture was made through the loop on both electrodes, thus keeping them in place and, regardless of behaviour of the fish, preventing it from pulling the electrodes out during the experiment.
The fish was woken from anaesthesia through artificial gill ventilation by
moving the fish back and forth in the water. As soon as the fish was able to
ventilate the gills on its own in a stable manner, it was placed in the test
restrainer, where it was left to recover for 15–24 h
(Axelsson, 1988). Heart rate
data were collected using an AcqKnowledge MP 100 data-acquisition system
sampling at 200 Hz (BioPac systems, Santa Barbara, CA, USA). The ECG signal
was amplified using a custom-built pre-amplifier. After the recovery period,
the fish were exposed to one of two experimental treatments. Five fish were
exposed to a set-up in which the test restrainer was placed 1.05 m in front of
a Simrad EK-38/22E echosounder transducer. Using an Agilent 33220A arbitrary
waveform generator and a custom-built amplifier, 50 kHz sound pulses with a
duration of 10 ms and a repetition rate of 10 pulses s–1 were
generated, mimicking a pulse type commonly used by echosounders
(Simmonds and MacLennan,
2005). The received sound pressure level at the fish in the
restrainer was measured to be 213±1 dB re. 1 µPa (pp) using a
calibrated Reson TC 4034 hydrophone (Fig.
3). The exposure period was 30s, yielding a sound exposure level
(SEL) of 184 dB re. 1 µPa2 s (1.6 J
m–2)
for a single pulse and 209 dB re. 1 µPa2 s for the entire 30 s
exposure period. To ensure that the fish were fit and able to display a
reaction that would be detectable in their heart rate, they were either
exposed to one of two different stimuli: one of the experimenters becoming
visible to the test animal or exposure to a low-frequency acoustic stimulus (a
knock on the mount holding the restrainer). The experimental session ended by
removing the fish from the restrainer and euthanizing it with a blow to the
head.
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To have control of the sound field in terms of both pressure and particle
acceleration, the sound exposure experiments were carried out in the acoustic
(Frauenhofer) and in the flow far-fields of the sound source. In this
experiment, another five fish were exposed using a second set-up, where the
test restrainer was only 30 cm from the transducer, which mimics the set-up of
Astrup and Møhl (Astrup and
Møhl, 1993). This range to the transducer placed the fish
in the pressure (Fresnel) near-field of the transducer, but outside the flow
near-field. The flow near-field is defined as the distance from the transducer
at which the particle motion cannot be predicted from the pressure component
of the sound field (Urick,
1983). If the product of kr, where k is the wave
number and r is the distance between the sound source and the
receiver, is much greater than 1, the restrainer could be assumed to be
outside the flow near-field. The kr product for a range of 30 cm was
calculated to be 63, at which the restrainer is considered to be well outside
the flow near-field of the transducer. The second type of near-field is the
Fresnel pressure near-field. This is the distance from a composite sound
source within which the sound source can no longer be regarded as being an
acoustic point source. The distance is calculated as:
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is the wavelength
(Urick, 1983). At distances
shorter than this, cancellations can occur, making nodes and notches, and
yielding an uneven sound-pressure field. The Fresnel near-field was in this
instance calculated to be 85 cm, so a distance of 30 cm puts the fish well
within the Fresnel near-field, which is likely to generate significant
pressure differences along the fish body for pure-tone pulses. For the 30 cm set-up, the received sound-pressure level at the head of the fish was measured to be 216±1 dB re. 1 µPa (pp) using a B&K 8103 hydrophone. The exposure period was again 30 s, giving an SEL of 187 dB re. 1 µPa2 s for a single pulse and 212 dB re. 1 µPa2 s for the entire exposure. Fifteen minutes after experimental exposure, the fish was exposed to the control, consisting of either a visual stimulus or a knock on the mount holding the restrainer. The fish was then euthanized with a blow to the head. Acoustic and heart rate data were processed using Matlab v. 6.5 (Mathworks, Inc., Natick, MA, USA) and the statistical analysis was carried out with the statistical toolbox in Matlab v. 6.5.
Behavioural experiment
The experiment was conducted in an aquarium containing six Atlantic cod.
Exposures consisted of 50 kHz pulses with duration of 10 ms and a repetition
rate of 10 pulses s–1. The exposure period was 1 s, and
consisted of 10 pulses. The stimulus was generated using an Agilent 22330A
arbitrary waveform generator connected to a custom-built amplifier and a Reson
2116 broadband transducer.
The exposure zone was monitored using two Profiline underwater cameras connected to laptops through Grabster AV400 A/D cards. One of the cameras was mounted on top of the transducer, thereby enabling the monitoring of fish passing in front of the transducer. A square measuring 1x1 m was placed at the far wall opposite the transducer. This was used to indicate the area viewed by the camera within which the fish was ensonified by the calibrated acoustic beam. The other camera was placed so as to give an aerial view of the area in front of the transducer where the fish would be exposed to between 208 dB re. 1 µPa (pp) and 220 dB re. 1 µPa (pp). The sound field was measured using a calibrated Reson TC 4034 hydrophone with a flat (±2 dB) frequency response from 1 to 150 kHz.
The cod was stimulated when in view of both cameras. A change in swimming behaviour was quantified by comparing the maximum tail-beat amplitude before and after the onset of exposure. This was carried out by analysing the video recordings of the swimming fish frame by frame. For each tail beat, the frame where the tail of the fish was displaced maximally from the longitudinal axis of the body was saved as an isolated picture. On each of these frames, a line was drawn through the two points that were given by the most anterior point of the head and by the beginning of the dorsal fin. This line indicated the main axis of the body from which the degree of tail displacement was measured. The distance from the tail to the main axis was measured using a ruler, and the distance was normalized by dividing it by the distance measured from the head to the beginning of the dorsal fin. Three tail beats before and three tail beats after the onset of the exposure were analysed in this way using Ulead VideoStudio 7 and Pinnacle Studio Version 9 video editing software. Statistical analysis was carried out using the statistical toolbox in Matlab v. 6.5.
Debilitation experiment
For this experiment, ten Atlantic cod with an average length of 38±4
cm (mean ± s.e.m.) were used.
An acoustically transparent flow chamber was built using a Plexiglas cylinder with an inner diameter of 20 cm. The cylinder was capped at both ends with honeycombs to ensure an approximately even velocity profile across the diameter of the flow chamber. One end of the flow chamber was mounted with a conical section 30 cm in length that was connected to a submersible pump with a capacity of 26 m3 h–1. The output of the water pump was set to create a water flow speed of approx. 0.4 m s–1 [measured with a flow probe (Höntzsch Instruments, Germany) in side the chamber] corresponding roughly to one body length. Each fish was introduced to the flow chamber 2 hours prior to the exposures. The water flow was started 30 min prior to sound exposure, after which the fish was assumed to have reached steady state.
Each fish was exposed to two treatments. Treatment one consisted of five
cycle 50 kHz clicks with a duration of 100 µs, a repetition rate of 200
clicks s–1 to mimic the buzz phase of an approaching toothed
whale (Madsen et al., 2005). A
mean received sound pressure of 212±3 dB re. 1 µPa (pp) was measured
inside the test tube in the volume occupied by the fish
(Fig. 4). This yields an SEL of
161 dB re. 1 µPa2 s click–1 (0.01 J
m–2). The second treatment consisted of a 50 kHz pulse with
duration of 10 ms, a repetition rate of 10 pulses s–1 with a
mean sound pressure level of 214±3 dB re. 1 µPa (pp) yielding an SEL
of 185 dB re. 1 µPa2 s pulse–1 (2.0 J
m–2).
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After a swimming period of 30 min in the flow chamber, the fish was exposed to both treatments in random order 11 min apart to allow the fish a chance to recuperate after the first treatment.
The fish was tracked from the time swimming commenced and until 2 min after the last exposure using a vertically mounted LoliTrack 2D video tracking system (Loligo Systems ApS, Tjete, Denmark) sampling at 15 frames s–1. To ensure good contrast between the fish and its background, a white acrylic board was placed underneath the flow chamber. The set-up was calibrated at the end of each session by placing a cross with known dimensions at the position of the fish. The tracking data consisting of x and y positions in the horizontal plane of the flow chamber was processed using Mathematica 5.2 (Wolfram Research, Champaign, IL, USA) and the statistical analysis was carried out in Matlab v. 6.5.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Anti-predator
behaviour is expected to yield a significant difference in the maximum
tail-beat amplitude before and after the stimulation, in that a strong
avoidance response would cause an increase in tail-beat amplitude. In the case
of debilitation, the cod is kept swimming at a constant speed and if
debilitation occurs, it is hypothesized that it will no longer be able to keep
its position in the strong water flow.
Heart rate experiment
Ten Atlantic cod were exposed to ultrasound in either a pressure near- or
far-field set-up. For both the near- and far-field treatments, the maximum HRI
from the 30 s pre-exposure and the 30 s exposure periods are compared for all
five fish in each treatment. For both the near- and far-field exposures, there
is no significant difference in max HRI between pre- and exposure periods
(near field, T=5; far field, P=0.6250; T=3,
P=0.3125, Wilcoxon's test for matched pairs). As the heart rate
pre-exposure periods for the two different treatments show both normal
distribution (P=0.6172, Bera-Jarque parametric hypothesis) and have
an equal variance (P>0.05), we pooled the data from the two
treatments (Sokal and Rohlf,
1998). After pooling of data there was no significant difference
between pre- and exposure periods (T=27, P=1, Wilcoxon's
test for matched pairs). Fig. 5
shows the HRI of all ten fish during a 70 s. window around the exposure
period, showing that no changes in HRI occur during the exposure period. For
the control treatments, in which the fish 6, 8 and 10 have been exposed to the
acoustic stimulation and the remaining fish have been exposed to the visual
stimulation (Fig. 6) the
maximum HRI before stimulation is significantly different from the maximum HRI
afterwards (T=0, P=0.002, Wilcoxon's test for matched
pairs).
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Debilitation experiment
Debilitation experiments were carried out on 10 Atlantic cod.
Fig. 8A,B show the mean
swimming speed of the 10 cod for click and pulse exposures, respectively. Data
are presented in a 40 s. window around the exposure. The fish was forced to
swim at a constant speed of 0.4 m s–1 to keep position, and
the deviation in swimming speed from this value as seen in
Fig. 8 is the second derivative
of the positional data of the fish. If the fish was swept back in the flow
chamber, it reflects an impaired swimming capability, thereby indicating
debilitation. The maximum swim speed before exposure is not significantly
different from the maximum swim speed during the experiment for either of the
two treatments (click, T=23, P=0.6953; pulse, T=18,
P=0.3750, Wilcoxon's test for matched pairs).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Plachta and Popper,
2003; Wilson et al.,
2008). Astrup and Møhl
(Astrup and Møhl, 1993)
also reported that Atlantic cod could be conditioned to detect ultrasound. In
light of these studies, we wanted to test whether high intensity ultrasound
evokes a response in unconditioned Atlantic cod in the form of bradycardia and
avoidance responses, as would be expected if cod, like shad, were able to
detect intense ultrasound as a part of an anti-predator measure.
In the heart rate experiment, we tested for any near-field effects of the
sound exposure that could enable the fish to detect ultrasound. There are
several mechanisms by which fish may detect such near-field effects. First, a
fish can be regarded as a rigid body when placed parallel to the direction of
the sound. Close to the sound source, at distances shorter than the length of
the fish, the sound pressure will diminish significantly, so that the front
and rear of the fish would experience different displacement. The head and
tail should thus ideally move with different velocities, but as the fish moves
as a rigid body it will move with an intermediate velocity, thus creating a
difference in movement between the fish and the water at either end of the
fish. This difference may be detected by the lateral line system
(Sand, 1984). In addition, in
the Fresnel near-field, because of the very high sound pressures used in this
experiment, differences between nodes and internodes in the near-field could
be very large and the mechanism mentioned above could thus be greatly
enhanced. The tuning curve for the lateral line shows no sensitivity at
frequencies as high as the ones used here, but, again, because of the very
high sound intensities used, it is possible that the system might still be
stimulated. We therefore tested the effects of ultrasound on the heart rate in
both a pressure near- and a far-field set-up. There were, however, no changes
in heart rate in either of the two set-ups.
Knudsen (Knudsen, 1994)
showed that bradycardia is induced in Atlantic cod immediately after exposure
to an acoustic stimulation consisting of a knock on the side of a holding
tank, and heart rate is therefore a short-term measure of the fish being
stressed or frightened by a given stimuli. We observed similar responses in
our control experiments (Fig.
6). However, we never observed such a response in the heart rate
data from the ultrasound exposure. If ultrasound was detected and perceived as
a potential threat from an approaching predator, we hypothesize that
bradycardia would have been the first indication, as it is a documented marker
of the orienting response in fish, and thus the first reaction in a row
leading to the flight or fight response
(Sokolov, 1963). If
bradycardia had been observed in our unconditioned fish, it would have implied
that cod will probably be affected more or less every time intense ultrasound
is detected from an odontocete or an echosounder. However, data from 10 cod
clearly demonstrate (Fig. 5)
that intense ultrasound at received levels of 213±1 dB re. 1 µPa
(pp), which is well above the conditioned detection thresholds of 204 dB re. 1
µPa (pp) reported by Astrup and Møhl
(Astrup and Møhl, 1993),
does not elicit any orienting response. The lack of orienting response shows
that these cod do not associate ultrasound with predation attempts or other
negative measures, despite the indication of normal hearing from the response
to the low frequency knock. The fish were allowed to recover for a month after
being caught. Complete regeneration of lost hair cells has been demonstrated
to occur within a few weeks of them being damaged
(Lombarte et al., 1993), so
the hearing of the fish was therefore assumed to be normal.
To further test the assertion that cod do not respond to intense
ultrasound, we conducted a series of playback experiments on free-swimming cod
to test the hypothesis that cod would show an avoidance or C-start response if
they, as inferred for shad (Plachta and
Popper, 2003; Wilson et al.,
2008), use ultrasound as a sensory cue to detect and evade
ultrasound emitting odontocetes. If intense ultrasound elicits an avoidance
response, significantly greater tail-beat amplitude would be expected after
the onset of the stimulus. Analysis of video sequences shows that received
levels between 208 and 220 dB re. µ1Pa (pp) did not elicit avoidance
responses in Atlantic cod (Fig.
7). However, in some cases the fish did seem to respond by
spreading out their pectoral fins, and momentarily increasing their swimming
speed slightly at the onset of the stimulation, though it was not enough to
significantly affect the tail-beat amplitude. This was, however, observed in
only a few fish swimming very close to the transducer, and was thus not a
consistent strong response, as is observed in shad at much lower received
levels (between 140 and 180 dB re. 1 µPa)
(Plachta and Popper, 2003).
This inconsistency in reaction was also observed by Astrup
(Astrup, 1997). The apparent
response in the present study was seen not only in cod but also in pollack,
pouting, saithe and sea bass in the same tank, and some members of all species
showed the same type of response. In one instance, the mild response was
elicited in two fish that were completely outside the ultrasonic beam but were
right next to the transducer where the received levels from the ultrasonic
pulse are more than an order of magnitude lower than in the beam. This
suggests that the mild response seen in a few cases is not a response to the
ultrasonic stimulation.
This then poses the question of what stimulus have these fish responded to? The Reson 2116 is a broadband transducer that also transmits low-frequency by-products, though at much lower outputs. The low-frequency components associated with the fast onset of a sound may therefore have been transmitted with a low directionality, possibly explaining why fish were observed to react outside the ultrasonic beam. Second, the peak–peak stimulus voltage of 140 V sent to the transducer would probably also create an electric field around it. In combination or separately, these two properties of stimulus could have caused the few observed responses rather than the ultrasonic exposure.
Given the lack of control in this behavioural experiment on the
free-swimming fish, the possibility cannot be excluded that these five cod did
not respond to ultrasonic exposure because of impaired hearing. However, in
light of the consistent lack of responses in the heart rate experiment and in
the behavioural experiment, we find it parsimonious to infer that the fish of
the behavioural experiment did indeed have normal hearing, but did not respond
to the ultrasonic exposure. In future experiments, control stimuli should
consist of infrasonic sound pulses to which cod in opposition to mid-frequency
stimuli (Kastelein et al.,
2008) respond strongly
(Knudsen, 1994).
Astrup and Møhl (Astrup and
Møhl, 1993) reported a detection threshold for ultrasound
in Atlantic cod of 204 dB re. 1 µPa (pp). The minimum exposure in the
behavioural experiment conducted in this study is 3 dB above that threshold
and in some cases more than 10 dB above it. This means that the intensity in
the exposure is at least twice that of the threshold intensity found by Astrup
and Møhl (Astrup and Møhl,
1993). Assuming that the cod in our study in fact had the
detection threshold for ultrasound reported by Astrup and Møhl
(Astrup and Møhl, 1993),
we would thus expect a consistent anti-predator response if the ability of
Atlantic cod to detect ultrasound indeed serves the same purpose as inferred
for the ultrasound/predator detector found among the members of the Alosinae
subfamily (Mann et al., 1998;
Plachta and Popper, 2003). As
neither bradycardia nor anti-predator responses are observed in Atlantic cod
when exposed to ultrasound, the biological relevance of potential ultrasound
detection is equivocal. We therefore, in contrast to Astrup and Møhl
(Astrup and Møhl, 1993)
and Astrup (Astrup, 1999),
conclude that cod probably have not developed ultrasound detection
capabilities to avoid predation from toothed whales, as suggested for shad
(Plachta and Popper, 2003).
The discrepancy between the findings from conditioned cod of Astrup and
Møhl (Astrup and Møhl,
1993) and the present results from unconditioned cod remain
unresolved, but it is possible that the cod used in the Astrup and Møhl
(Astrup and Møhl, 1993)
study, despite careful methodology, in fact were conditioned to artefacts
rather than to the ultrasonic component of the exposure.
Ultrasound might, however, still play a role in the acoustic
predator–prey interaction despite the lack of detection and behavioural
responses in cod. The prey debilitation hypothesis advanced by Norris and
Møhl (Norris and Møhl,
1983) proposes that very high intensities of ultrasound produced
by toothed whales could have a debilitating effect on their prey. Toothed
whales that capture prey increase their repetition rate, but lower their
source level by about 10–20 dB when they are within a few meters of
their prey (Madsen et al.,
2005; Madsen et al.,
2002), initiating what is termed the buzz phase
(Miller et al., 1995). Source
levels for most toothed whales do not exceed 230 dB re. 1 µPa (pp)
(Au, 1993), so the maximum
received levels at the prey would therefore not be expected to be higher than
some 210 to 215 dB re. 1 µPa (pp) during any given point of ensonification
from an approaching toothed whale predator.
Zagaeski (Zagaeski, 1987)
showed that a broadband impulse of very high peak pressure of more than 230 dB
re. 1 µPa (pp) generated by a spark generator had a debilitating effect on
guppies. But although the sound pulse did contain ultrasonic components, it is
very hard to discern whether ultrasound had any part in the debilitation, as
the signal also contained very intense low-frequency components with very
large particle motion component. Benoit-Bird et al.
(Benoit-Bird et al., 2006)
found no debilitating effects of ultrasound on Atlantic cod, Atlantic herring
and sea bass. They used lower received levels than in the present experiment,
and the parameters for testing debilitation could not quantify the escape and
swimming capabilities of the fish, as the fish were restrained to a very small
tank and did not have to swim to maintain position. Here, we tested whether
swimming cod could maintain their position in a strong water current, thereby
mimicking a situation in which a fish is chased by a predator. The
experimental setup in the debilitation experiment forced the fish to swim at a
constant speed. If debilitation occurred, we hypothesized that the ability of
the fish to maintain its position and thereby its swimming speed would be
impaired and that the fish would be flushed from its position by the water
current. Such a change in position and thereby swimming speed would be clearly
detectable in the tracking data, and thus provide an unequivocal test of
whether the received levels had any debilitating effects on the escape
capabilities of the cod. We found no debilitating effect of very high
intensity ultrasound on Atlantic cod, as all 10 fish successfully maintained
their position in the flow chamber at swimming speeds of more than 1 body
length s–1 (Fig.
8). Thus, the present findings are not consistent with the
debilitation hypothesis and it can be concluded that ultrasound exposures from
odontocetes or echosounders do not debilitate Atlantic cod at received levels
between 213 and 215 dB re. 1 µPa (pp).
Ultrasound is used for a variety of purposes in fishing and fisheries
management, and if cod indeed were able to detect ultrasound, it could be a
source of stress and behavioural disruption for areas heavily ensonified with
ultrasound. Second, echosounders are used to estimate stock sizes
(Michalsen et al., 1996), and
behavioural effects of ultrasound exposure would therefore introduce a bias in
the stock assessment. From the present data and under the assumption that the
cod used here are representative of cod in the wild, we conclude that such a
concern is unsupported and that evasion of ultrasound sources is unlikely to
occur.
In addition to echosounders, another anthropogenic ultrasound source is
becoming increasingly important in fisheries. Many cetaceans drown by being
caught in fishing nets, and such incidents are avoided by equipping the nets
with acoustic alarms to deter odontocetes. The pingers used for this emit
sounds between 10 and 160 kHz with source levels below 160 dB re. 1 µPa
(pp) (Kastelein et al., 2007).
Sound sources on fishing nets may, however, also make them detectable to the
fish targeted by the nets and in turn lead to reduced catch rates. Although
the ultrasonic frequencies are different for these pingers, the lack of
behavioural responses at much higher received levels than the source levels of
pingers supports the finding by Kastelein et al.
(Kastelein et al., 2007) that
ultrasonic pingers do not have any effect on Atlantic cod. Finally radio
telemetry using high frequency transmitters have been used to measure heart
rate on free-swimming Atlantic cod
(Claireaux et al., 1995). If
ultrasound had an effect on the heart rate and behaviour, results from such
experiments would have been compromised by the experimental animals showing
abnormal behaviour and heart rates. Present findings do not support concern
for such a bias.
Despite the strong negative evidence for ultrasound detection in cod,
acoustic stress is nonetheless an important issue to consider in fisheries
management and conservation. Atlantic cod has been documented to have acute
infrasonic hearing (Sand and Karlsen,
1986) and noise from a research vessel may produce avoidance
reactions in Atlantic herring (Ona et al.,
2007) and in Atlantic cod
(Olsen et al., 1983). Ship
noise is, thus, a potential stressor of fish populations and it may introduce
a bias in stock assessment and should be investigated further.
If the experimental results on captive cod presented here reflect the behaviour and sensory physiology of wild cod populations, it is concluded that ultrasound exposures mimicking those of echosounders and odontocetes will not induce acute stress responses, such as bradycardia or anti-predator responses in Atlantic cod. Frequent encounters with ultrasound sources will therefore most probably not induce a more chronic state of stress, and thus cause maladies such as increased susceptibility to parasites, abnormal development of larvae and in the end reduced recruitment to the adult population. As the cod used here did not respond to ultrasound, and are not debilitated by very high intensities, the question is which modalities can a cod use to detect an oncoming predator? We consider the low-frequency particle motion created by ships and swimming predators to be likely sensory cues and they should be subjects for further research.
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Acknowledgments |
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Footnotes |
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For a plane wave in an unbounded medium, the energy flux density in dB re.
1 µPa2s can be converted to J m–2 by dividing
the summed squared pressure on a linear scale by the specific impedance Z
(sound speed x density) of the medium. To exemplify, 182 dB re. 1
µPa2s=(1580 Pa2 sm–2)/(1500 m
s–1 x 1040 kg m–3)=1 J
m–2. 
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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