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Reactionsofpennedherringand
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Fisheries Research 22 (1995) 243-254
Reactions of penned herring and cod to playback of
original, frequency-filtered and time-smoothed
vessel sound
Arill Engb*, Ole Arve Misund, Aud Vold Soldal, Berit Horvei’,
Ame Solstad2
Institul!eof Marine Research, Fish Capture Division, P.O. Box 1870, N-5024 Bergen, Norway
Accepted 21 June 1994
Abstract
The behavioural responses of penned cod (Gadus morhua L. ) and herring (&pea harengus L. ) to playback of original, frequency-filtered
and time-smoothed sound recordings
from a trawler were tested. Avoidance reactions of both cod and herring were observed
during playback of the original, 60-300Hz and 300-3000Hz spectra, but hardly to the
20-60Hz spectrum. The duration of responses of cod was longer to original than to timesmoothed sound. The conclusion is that the main determinant for triggering avoidance
reactions of cod and herring is vessel sound level within the most sensitive frequency region, although other sound characteristics, such as temporal structure, also seem to be of
importance.
Keywords: Gadus morhua; Clupea harengus; Behaviour
1. Introduction
The hearing ability of fish ranges from infrasound (Sand and Karlsen, 1986)
to above 1 kHz (Hawkins, 1993). Fish can discriminate between sounds of different amplitude and frequency, determine direction and distance to the sound
source (Popper et al., 1988), and distinguish between sounds with complex patterns in temporal structure (Fay, 1980).
The sound generated from a vessel and the gear during fishing operations may
have considerable effect on the catch success. Although it is clear that fish are
* Corresponding author.
’ Present address: SINTEF DELAB, N-7034 Trondheim, Norway.
’ Present address: IKU Petroleum Research, N-7034 Trondheim,
Norway.
0165-7836/95/$09.50
0 1995 Elsevier Science B.V. All rights reserved
sSDIO16!i-7836(94)00317-P
244
A. Eng&s et al. /Fisheries Research 22 (I 995) 243-254
able to detect the sound from a fishing vessel at great distances (Chapman and
Hawkins, 1969; Buerkle, 1977), it is not yet fully understood which specific characteristics of the sound are necessary to make the fish not only detect but also
react to the sound (Food and Agriculture Organization (FAO ), 1970; Schwarz,
1985). Sudden changes in revolutions or pitch during circling of a herring school
are in practice experienced to play an important role in scaring under certain
conditions (Olsen, 1976). Erickson ( 1979) and Bercy and Bordeau ( 1987)
showed that where major peaks existed in the low-frequency sound spectrum of
fishing vessels, catches of tuna were lower than where the spectrum was relatively
smooth.
To determine characteristics of the vessel sound that arouse avoidance reactions in cod ( Gadus morhua L. ) and herring ( &pea harengus L. ) , we have studied the reactions of penned fish to playback of original, filtered and time-smoothed
recordings from a trawler.
2. Materials and methods
2. I. Recordings of sound
Sound energy of a factory trawler (56.9 m length overall, 3000 HP) that claimed
to have low catch rates owing to fish avoidance was recorded during fishing with
a bottom trawl at about 300 m depth in a sheltered fiord in Western Norway.
Revolutions, pitch and vessel speed (about 3 m s- ’ ) were set as during ordinary
fishing. Two hydrophones were positioned 5 m apart at 5 m depth (Nisja et al.,
1989), and the vessel passed at a distance of 45 m. The sound recordings started
when the vessel was about 200 m in front of the hydrophones and stopped when
the vessel was about 200 m behind them. This gave sound recordings of about
130 s in duration (Fig. 1).
2.2. Editing of sound for playback
Four categories of sound from the vessel were edited and used for playback
experiments.
( 1) The original sound recordings of the vessel noise were used (Figs. 1 and
2).
(2) The original sound recordings was split up into three frequency bands,
according to the audiogram established for cod by Chapman and Hawkins
( 1973)-20-60 Hz (increasing sensitivity), 60-300 Hz (maximum sensitivity),
and 300-3000 Hz (decreasing sensitivity). The splitting was done by a Butterworth filter, which had an attenuation slope 24 dB per octave outside the - 3 dB
points.
( 3) The amplitude of the original recordings was time-smoothed by smoothing
the fluctuations of the r.m.s. effect of the original recordings with an automatic
gain-controlled amplifier, giving a constant sound level, and then employing tri-
A. Eng& et al. /Fisheries Research 22 (1995) 243-254
245
Fig. 1. Time lapse of the total sound level in the frequency band 20-400 Hz in the original recording
of the trawler compared with the same recording after time-smoothing.
Fig. 2. Variation in relative amplitude of the frequency distribution
in the original recording of the trawler.
( l/3 octave bandwidth)
vs. time
angle amplification to obtain the same maximum sound level as that of the original sound (Figs. 1 and 3). However, the maximum level was reached about 15 s
earlier in the time-smoothed sound sequence than in the original one.
246
A. Eng#s et al. /Fisheries Research 22 (199s) 243-254
Frequency
Fig. 3. Variation in relative amplitude of the frequency distribution ( l/3 octave bandwidth) vs. time
in the time-smoothed version of the trawler sound.
(4) The three bands as in Category 2 were used, but time-smoothed.
2.3. Playback experiments
The experiments were carried out in a sheltered coastal area outside Bergen,
Norway, during spring 1989, with cod and herring as test fish. The cod were caught
with traps at about 5 m depth, and the herring with purse seine close to the surface. Two groups of cod ( 18 and 16 fish of length 33-53 cm) and one group of
herring ( 18 fish of length 22-28 cm) were tested. Cod and herring were placed
in the experimental net pen (3 m x 3 m x 3 m) for 4 days and 7 days before testing, respectively. The fish were not fed during the experimental period.
An underwater loudspeaker was positioned at 2 m depth at a distance of 11 m
from the nearest net wall, i.e. outside the near field of the lowest frequency transmitted (20 Hz) (Hawkins, 1993 ). The ambient noise level and the playback of
the sound recordings were measured with a hydrophone placed inside the net pen
at 2 m depth.
The ambient noise level showed a mean value of approximately 90 dB re 1 PPa
in the 50-3000 Hz band (Fig. 4). The 50 Hz component of the spectrum is disregarded owing to electrical noise in measuring instruments. The measured sound
levels for the different playback sequences (average level measurements over 30
s before and after maximum level) are given in Fig. 5. It should be noted that the
three filtered frequency bands still contain sound components outside the specified bandwidth, owing to limitations inherent in the filtering method.
A. EngcEFet al. /Fisheries Research 22 (1995) 243-254
I
. noise
. ambient
from
241
trawler
noise
L/^i-..
Fig. 4. Maximum background noise level at the experimental site and the trawler sound level in the
pen when the total level of the original trawler sound playback reached maximum intensity ( l/3
octave bandwidth ) .
Fig. 5. Frequency-separated
level of the frequency-filtered
(l/3 octave bandwidth) sound level in the pen when the total sound
sound spectra reached maximum intensity.
During the playback of the sound sequences, the behaviour of the two species
was observed with an underwater TV camera, mounted in a comer of the net pen.
Every second day during daylight, both species were presented with 3-4 paired
(original and smoothed sequences of the same spectrum), randomly selected
playback sequences ( 130 s), separated by a rest of at least 20 min.
Video recordings of the fish behaviour in the pen were analysed in 10 s intervals from 1 min before until 1 min after playback. The behaviour was classified
according to the following criteria: group pattern ( 1, shoal; 2, school; see Pitcher,
1983); vertical swimming ( - 1, downwards; 0, horizontally; 1, upwards); tail
beat frequency (number of tail beats per 10 s interval).
The overall responses to the playbacks were categorized as follows: no response
248
A. Engds et al. /Fisheries Research 22 (I 995) 243-254
(no systematic change in behaviour during a playback sequence); avoidance response (change from loose schooling or random orientation in shoals to dense
schooling, slow diving, or diagonal swimming close to the bottom of the pen);
alarm response (rapid polarization and burst speed swimming to the bottom of
the pen). The start and duration of the overall responses to the playbacks were
measured.
3. Results
Penned cod and herring reacted to the vessel sound in 73% and 75% of the
playback experiments, respectively (Tables 1 and 2). The reactions were always
categorized as avoidance, and no alarm reactions were observed. When responding to a playback, the cod packed together, polarized, and swam slowly downwards to the bottom of the pen, up along the net wall, and down to the bottom
again (Figs. 6 and 7). The herring were shoaling or loosely schooling around, just
above the bottom of the pen during daytime, but when exposed to a playback, the
herring packed denser and were strictly schooling in a diagonal path along the
pen bottom (Fig. 6). Neither of the species increased the tailbeat frequency when
responding to playbacks.
Using the start and duration of the responses as reaction estimators reveals no
significant differences between cod and herring in their reactions to the playbacks
(Table 3). There were significant differences in the duration of the responses
between the various spectra, and between the original and smoothed sound. The
start of the responses was not significantly different between the spectra and between these two types of sound.
Table 1
Number of responses, duration of response, and start of response (in seconds from start of playback)
for the various playback categories for cod
Modification
Whole
spectrum
20-60 Hz
60-300
300-3000 Hz
Sum
NS: Pz 0.05.
Smoothed
Original
Smoothed
Original
Smoohted
Original
Smoothed
Original
Smoothed
Original
Response
(no.)
Duration of response (s)
Start of response (s)
No
Yes
Mean f SD
Paired
t-test
Mean f SD
Paired ttest
6
2
6
6
0
0
2
1
14
10
9
12
1
1
13
14
6
9
29
36
37.3 f 38.6
105.3 k 64.9
4.3f 11.3
2.8f 7.5
63.8 k29.3
92.8 + 35.8
46.2+ 36.6
98.Ok51.6
41.6k37.1
84.3 f 58.8
Pi 0.05
21.9f28.3
19.2f 16.1
1.0
40.0
18.2+ 17.8
20.8It: 19.2
19.2f22.2
20.1 f 19.1
19.0f21.6
20.6f17.8
NS
NS
P< 0.05
P< 0.05
‘<‘.05
NS
NS
NS
249
A. Engds et al. /Fisheries Research 22 (1995) 243-254
Table 2
Numbers of responses, duration of response, and start of response (in seconds from start of playback)
for the various playback categories for herring
Modification
Response
Start of response (s)
Duration of response (s)
(no.)
No
Yes
Original
Smoothed
01
11
7
Original
Smoothed
2
300-3000 Hz
Original
Smoothed
Sum
Original
Smoothed
Whole
spectrum
20-60 Hz
Paired ttest
Mean f SD
Paired
t-test
76.3k62.1
92.3
f 34.7
NS
11.3k7.5
7.7t 10.7
NS
42
48.3
23.7 + 38.2
50.0
NS
12.7? 12.2
16.5k22.6
NS
02
63
35.0* 39.4
103.3k82.2
NS
25.7
9.8fll.O
+ 22.0
NS
49
23
15
46.0+
75.7+ 50.8
52.0
P= 0.04
14.7+
14.8t 14.9
15.7
NS
Mean ? SD
2.0
1.5
6
3
a
z
1.0
”
0.5
0.0
0
30
60
90
120
150
i80
210
240
270
~‘~l”,“,.~,‘~,“,‘.,,~,.,,
t
0
30
60
90
TIME fs)
coo:
20-60
nz
HERRING:
20-60
120
150
TIME
Is)
1
180
210
240
HZ
Fig. 6. Group index distributions (average CLSD) of cod and herring during playback of the whole and
frequency-fihered original and time-smoothed trawler sound spectra. Upward arrow indicates start
and downward arrow indicates stop of vessel sound playback.
270
A. Engk et al. /Fisheries Research 22 (1995) 243-254
250
coo:
60-300
HERRINO:
HZ
2.0
3
z
3,
4 1.0s
:
1.0.
B
::
0
:
0.5
0.5-
I
I
0
30
60
120
90
TIME
con:
300-3000
1SO
180
210
240
270
0
30
90
60
120
150
TIME
Is1
300-3000
HERRING:
nr
180
240
210
270
Id
"7.
2.0s
Z.O-
z
HZ
1.5.
I.§B
60-300
2.0-
1.5-
l.SE.
z
:
z
4
1.0-
D1.0s
J
0,
0.5.
0.5-
i
t
0.0
0
30
60
I
I
I
I
I
I
90
120
150
100
2iO
2.0
TIME
(s)
c
t
0.0
I
0
270
30
60
-
smooth
90
120
”
I
150
,’
I
4
ieo
-
-
I
210
I’
1 ”
240
TIME Cd
SOUND
-
original
- --
Fig. 6 (continued).
As apparent from Figs. 6 and 7, the cod hardly reacted to the 20-60 Hz spectrum. The strength of the responses of cod to the other spectra seemed rather
similar (Table 1). The herring showed only a few and late reactions to the 20-60
Hz spectrum, and the duration of the responses was longest to the whole and
highest-frequency spectrum.
For cod, the duration of the responses to original spectra was generally longer
than to smoothed sound for three of the four frequency spectra, and also when
pooling all the experiments (Table 1) . Only when pooling all the experiments for
herring was there a significant difference in the duration of responses to the original and smoothed sound (Table 2). Although not significant, a tendency for
longer responses to original sound at the spectrum level was indicated also for
herring.
Substantial variation between trials was, however, found both in swimming
behaviour (Figs. 6 and 7 ) and in duration and start of responses to the two types
of sound and the various spectra (Tables 1 and 2). Both cod and herring behaved
differently from one playback experiment to another; other external stimuli
(strong tide-currents, sunlight, and presence of potential predators outside the
net wall) seemed to weaken the response strength.
r
270
A. Engds et al. /Fisheries Research 22 (I 995) 243-254
251
Fig. 7. Vertical swimming index distribution (average f SD) of cod during playback of the whole and
frequency-filtered original and time-smoothed trawler sound spectra. Upward arrow indicates start
and downward arrow indicates stop of vessel sound playback.
Table 3
Linear model for duration of response and start of response for cod and herring
Start of response
Duration of response
Species
Spectrum
Modificatia’n
F
Pr>F
F
Pr>F
0.1
14.4
23.0
0.80
CO.01
CO.01
2.0
1.8
0.1
0.16
0.16
0.78
F, Variance ratio; Pr, significance probability.
4. Discussion
As also observed in field situations (Olsen et al., 1983; Ona and God@, 1990 ),
the penned cod reacted to the playback of vessel noise by slowly diving. Both cod
and herring moved into dense, structured schools, and the herring swam diago-
252
A. Eng6s et al. /Fisheries Research 22 (1995) 243-254
nally along the bottom of the pen. Schwarz and Greer ( 1984) recorded similar
reactions of Pacific herring to playbacks of noise from large fishing vessels. Herring schools circled by purse seiners or approached by a survey vessel are known
to avoid horizontally at some distance from the vessel (Misund, 1990)) whereas
diving reactions have been recorded for schools passed over by a vessel (Misund
and Aglen, 1992). One assumed reason for schooling is to maximize the probability of survival if attacked by predators (Pitcher and Parrish, 1993). The
schooling response may therefore indicate that the cod and herring reacted to the
vessel noise as a potential but moderate threat, as there were no signs of alarm or
panic reactions.
In accordance with the equality in auditory thresholds for cod and herring (Enger, 1967; Chapman and Hawkins, 1973), there were no significant differences
between the two species in the start and duration of responses to the various playback sequences of vessel sound. Both species reacted to the 60-300 Hz, 300-3000
Hz, and the full spectrum, but hardly to the 20-60 Hz spectrum. This agrees with
the frequency bands of highest sensitivity for cod and herring.
As earlier stated, however, the three filtered sound sequences still contained
components outside the desired frequency band (Fig. 5 ). In the 20-60 Hz spectrum, the sound level in the frequency range of highest sensitivity for cod (603 10 Hz) reached about 118 dB re 1 PPa. When extrapolating from Chapman and
Hawkins (1973), this is about 10 dB above the auditory threshold at a background noise level of 90 dB re 1 PPa. Therefore the fish probably sensed the noise
in the 20-60 Hz spectrum also, but as no reaction was triggered, the amplitude
did not exceed the reaction threshold.
When responding, both cod and herring usually started long before the playback noise was at maximum level. As apparent when considering the noise field
from the vessel (Figs. 2 and 3), there were components in the 60-300 Hz band
that reached about the maximum level immediately after the beginning of the
playbacks. The maximum amplitude in the sensitive frequency band of the other
playback sequences were higher (about S- 10 dB ) than that of the 20-60 Hz spectrum. This difference in sound level seemed to determine whether the fish responded or not. Therefore, the sound level of the vessel noise in the most sensitive frequency region is probably the main determinant for eliciting avoidance
behaviour in cod and herring.
Cod and herring generally reacted for a longer time to the original noise than
to the time-smoothed version. However, the start of response to the original or
smoothed versions was not different. This indicates that the sound components
eliciting a response to the original spectra were also present in the time-smoothed
ones. Nevertheless, the cod and herring clearly can differentiate between the two
types of spectra, as the frequency of responses to the time-smoothed noise was
lower, and the reaction ceased earlier, than to the original vessel noise. The maximum level of the time-smoothed spectra was reached after about 65 s of playback, and for the original spectrum about 80 s. For herring, the difference in time
until maximum level may account for most of the difference in the duration of
the responses. On average, the herring ceased reacting about 15 s after the maxi-
A. Engcis et al. /Fisheries
Research 22 (1995) 243-254
253
mum level of both the time-smoothed
and original spectrum. However, this is
not true for cod, which on average ceased responding to the time-smoothed spectra before the maximum level, whereas the responses to the original spectra usually ceased after the maximum level.
The reactions of cod and herring varied slightly from one,playback to another.
Fluctuations in ambient noise level, which for low frequencies may be rapid
(Wenz, 1962), may explain behavioural variations between succeeding playbacks. Weak responses during days with heavy tide or strong sunlight show that
stimuli other than vessel noise influence the behaviour of the penned fish. Contrary to Olsen ( 1976 ), we did not record any habituation to the playbacks. As the
responses were unconditioned,
this was probably a result of our experimental
strategy, based on a semi-natural environment, series of only 3-4 playbacks per
day only, and a break of at least 1 day between each series of playbacks.
The sound level radiated during trawling is substantial (Chapman and Hawkins, 1969; Hawkins and MacLennan, 197 1 ), and Buerkle ( 1977) has calculated
that cod may detect trawling sound at a range of 3.2 km in summer and 2.5 km
in winter. Therefore, avoidance reactions may also be induced by other characteristics of the sound field than the amplitude alone. We have shown that slight
changes in spectral and temporal structures of the trawler sound field may modify
the avoidance reactions of cod and herring. Temporal characteristics of the sound
fields of vessels may also to some extent account for their different catch rates, as
shown by Erickson ( 1979) and Bercy and Bordeau ( 1987) for tuna fishing vessels. But whether avoidance behaviour to fishing vessels is as dependent on the
temporal structure of the sound fields as suggested by these workers remains to
be tested.
Acknowledgements
We thank John Dalen, Anders FernS and Svein Lokkeborg for helpful suggestions during manuscript preparation. This study was supported by grants from
the Norwegian Council for Fisheries Research. Anders Brettingen corrected the
English and Elen Hals kindly prepared the manuscript.
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