ICES Journal of Marine Science, 61: 1062e1070 (2004)
doi:10.1016/j.icesjms.2004.07.003
Use of data storage tags to quantify vertical movements
of cod: effects on acoustic measures
O. Heffernan, D. Righton, and K. Michalsen
Heffernan, O., Righton, D., and Michalsen, K. 2004. Use of data storage tags to quantify
vertical movements of cod: effects on acoustic measures. e ICES Journal of Marine
Science, 61: 1062e1070.
Depth data from archival tagging studies of cod (Gadus morhua) were used in three
different analyses with the aim of testing basic assumptions of cod behaviour. Examination
of post-release depth profiles from cod tagged in the Barents, North, and Irish Seas revealed
that some cod underwent a post-release period of adaptation to increasing depth as they
readjusted their buoyancy to its pre-tagging level. This depth adaptation behaviour was
characterized by gradually increasing mean depth, and enabled the calculation of neutralbuoyancy compliant descent rates, which were less than 1 m h1. Estimated rates of vertical
movement were shown to be highly dependent upon the frequency at which depth was
sampled. Maximum estimated rates of ascent and descent from sampling intervals of 10 or
15 min were inconsistent with the maintenance of neutral buoyancy, but estimates from
sampling intervals greater than 1 h were not. Calculation of tilt angles using depth data
sampled at 10-s intervals showed that cod were often tilted more than 5( relative to the
horizontal, and that this effect was more pronounced at night. These findings suggest that
basic assumptions regarding cod physiology and behaviour require revision if the accuracy
and precision of acoustic methods are to be improved.
Crown Copyright Ó 2004 Published by Elsevier Ltd on behalf of International Council for the
Exploration of the Sea. All rights reserved.
Keywords: acoustic survey methodologies, cod, data storage tags, tilt angle, target strength,
vertical movement.
Received 18 March 2003; accepted 30 April 2004.
O. Heffernan and D. Righton: Centre for Environment, Fisheries and Aquaculture Science,
Lowestoft Laboratory, Pakefield Road, Lowestoft, Suffolk NR33 0HT, England, UK.
K. Michalsen: Institute of Marine Research, PO Box 1870 Nordnes, NO-5817 Bergen,
Norway. Correspondence to O. Heffernan: e-mail: olheff[email protected].
Introduction
Acoustic methodologies have gained widespread use in
fishing practices since their development in the mid-1960s,
owing to their distinct advantage of being able to detect
objects throughout the entire water column with the
exception of thin ‘‘dead zones’’ at the surface and seabed.
Acoustic methods are now applied to a number of fisheriesrelated problems, including sizing fish, monitoring of fish
movements, studying fish behaviour (MacLennan and
Simmonds, 1992; Aglen, 1994), and particularly assessment
of biomass of commercially important stocks (Michalsen
et al., 1996; Aglen et al., 1999). Given their socio-economic
importance, the accuracy of stock assessments is essential
(Aglen et al., 1999), but acoustic-based biomass estimates
are subject to both systematic and sampling error (Aglen
et al., 1999; Rose et al., 2000).
The greatest source of bias in acoustic-based biomass
estimates is target strength (MacLennan and Simmonds,
1054-3139/$30.00
1992; Simmonds et al., 1992), a measure of the acoustic
backscatter received from objects in the water column.
Target strength varies considerably between species and is
greatest in fish with a swimbladder (Foote, 1985), which
alone can be responsible for 90e95% of the reflected
acoustic energy (Foote, 1980). Target strength is assumed to
be relatively constant for fish of a given size and species at
a given acoustic frequency (MacLennan and Simmonds,
1992). Species-specific estimates of target strength are based
on two key assumptions: (i) the volume and shape of the
swimbladder are independent of depth changes (i.e.
individuals are always neutrally buoyant) and (ii) the
swimbladder is oriented horizontally relative to the acoustic
pulse. Aglen (1994) suggested that violation of these
assumptions could affect the estimate of fish biomass by
a factor of 10. In consequence, efforts have been made over
the past 20 years to increase knowledge regarding the
compliance of fish behaviour and physiology with these
assumptions, particularly in relation to cod.
Crown Copyright Ó 2004 Published by Elsevier Ltd on behalf of
International Council for the Exploration of the Sea. All rights reserved.
Quantifying vertical movements of cod
The traditional view of cod swimbladder physiology is
that neutral buoyancy is maintained at all times. Laboratory
experiments on 25e50 cm cod by Harden Jones and
Scholes (1985) showed that gas secretion into the
swimbladder is slow and that cod can descend at a rate of
approximately 0.7 m h1 while remaining neutrally buoyant. In contrast, gas resorption from the swimbladder is
more rapid than gas secretion and dependent upon
residence depth, but is still limited in most cases to several
metres per hour (Arnold and Greer-Walker, 1992).
Studies of cod tagged and released in the wild have shown
that rates of descent over hours or days can be consistent with
laboratory-derived estimates of neutrally buoyant descent
(Arnold and Greer-Walker, 1992; Thorsteinsson, 1995) and,
in some cases, with laboratory-derived estimates of neutrally
buoyant ascent (Thorsteinsson, 1995; Godø and Michalsen,
2000). Over short time periods (minutes to hours) however,
laboratory studies have shown that cod can tolerate rapid
changes in pressure without exhibiting erratic behaviour or
showing difficulty with swimming (Harden Jones and
Scholes, 1985), provided the pressure reduction after an
ascent is not greater than 25% and the pressure increase not
greater than 50%. Cod are able to make rapid ascents and
descents between these pressure limits, known as the free
vertical range (FVR, after Arnold and Greer-Walker, 1992),
without the need for buoyancy adjustment. This is
corroborated by observations of rapid vertical movements
observed in field studies of cod (Zilanov, 1963; Arnold,
1992; Arnold and Greer-Walker, 1992; Rose, 1993; Lawson
and Rose, 1999; Godø and Michalsen, 2000; Righton et al.,
2001; Righton and Metcalfe, 2002). Due to inconsistency in
the frequency at which depth data have been recorded in
these studies, exact estimates of the rates of vertical
movement of cod, and whether these are compliant with
the maintenance of neutral buoyancy, vary considerably.
Regardless of the rate at which cod can ascend or
descend in the water column and remain neutrally buoyant,
the assumption that the swimbladder remains oriented
horizontally relative to the acoustic pulse is questionable.
Cod can adjust their vertical position in the water column
by use of their pectoral fins and minimize their tilt angles,
but individuals commonly ascend or descend by altering the
tilt angle of the body and using the caudal fin for propulsion
(Harden Jones and Scholes, 1985). Systematic changes in
vertical movement associated with time of day or season
would produce a corresponding change in tilt angle, with
potentially serious implications for acoustic biomass
estimates (Foote, 1980; Michalsen et al., 1996; Aglen
et al., 1999; Orlowski, 2001). Measurement of tilt angles of
wild fish over long periods remains a challenge, however.
In this paper, high-resolution depth data from data
storage tags were used to calculate rates of depth change
and tilt angle distributions of cod in the North, Irish and
Barents Seas. The post-release rates of descent over several
days have been calculated to estimate the natural rates of
neutrally buoyant descent. The rates of vertical movements
1063
undertaken by cod have been compared at several sampling
frequencies, from 10 min to 4 h, to determine the effect of
sampling rate on the estimation of vertical movement rates.
Theoretical tilt angles calculated from extremely rapid
depth recordings (10-s intervals) have been used to assess
whether cod are likely to be tilted away from the horizontal
and whether the distributions of these tilt angles show any
systematic bias. The results challenge some of the key
assumptions regarding cod behaviour that are currently
used in fisheries biomass estimation.
Material and methods
Data storage tags
Two different types of tag were used in this study: the
LTD_1200 (LOTEK Wireless Ltd) and the DST_300 (Star
Oddi Corporation). The LTD_1200 is a small (18 57 mm;
16 g in air, 3 g in water) electronic archival tag that can store
as many as 750 000 records. It is capable of recording depth
(0e100 m G 0.02 m, but depth rated to 150 m) and water
temperature (4(C to 23(C G 0.03(C) at pre-programmed
intervals. LTD_1200s were deployed on cod in the North and
Irish Seas and, depending on the aims of the experiment,
programmed to record depth and temperature at intervals
between 10 s and 10 min (Table 1).
The Star Oddi DST_300 is small (46 13 mm; 8 g in air;
1 g in water) with a storage capacity of 32 000 records. It is
capable of recording depth (780 G 2.0 m) and water
temperature (1(C to 40(C G 0.03(C). DST_300s were
deployed on cod in the Barents Sea and were programmed to
record depth and temperature at 15-min intervals.
Fish capture and experimental design
In the southern North Sea, cod were caught in shallow
water (!25 m) by rod or longline. In the northern North
Sea, cod were caught in deep water (O60 m) using a BT
158 Jackson Rock-hopper trawl modified to include a PVC
liner in the codend that retained approximately 1 m3 of
seawater upon hauling. Cod in the Irish Sea were caught
using rod and line in water of 75e90 m depth. In the
Barents Sea, cod were caught at 200 m using ground trawl
and purse seine. In all cases, captured fish were brought
slowly to the surface to optimize post-tagging survival.
Details of the number of tagged fish released and recaptured
are presented in Table 1.
Fish tagging
Cod of approximately 50 cm or greater in length and in
good condition were considered suitable for tagging. Fish
were tagged either externally or internally (Table 1).
External tags were attached by threading monofilament
line from the attachment points of the DST through the
muscles anterior to the first dorsal fin and fastening the ends
securely on the other side by metal crimps. In the case of
O. Heffernan et al.
1064
Table 1. Details of DST-tagged cod from the North, Irish and Barents Seas analysed in the present paper. The figures in the final three
columns represent the number of individuals per release included in each analysis.
Area of capture
and release
Coordinates latitude
and longitude
Date of
release
Tagging
method
Number
released
(recaptured)
Depth
adaptation
analysis
Resampling
analysis
Tilt
angle
analysis
Southern North Sea
52(220 N 1(450 00E;
53(370 N 02(110 E
53(390 N 05(370 W;
53(300 N 5(500 W
52(220 N 1(450 00E;
53(370 N 02(110 E
57(420 N 6(20 W;
60(80 N 1(570 E
67(300 N, 12(E
MareMay 1999
External
67 (32)
3
32
e
Apr 1999
External
19 (4)
4
e
e
MareJun 2001
External
68 (22)
1
e
e
FebeMar 2002
Internal
50 (6)
e
e
10
Apr 1999
External
41 (10)
2
10
e
Central Irish Sea
Southern North Sea
Northern North Sea
Barents Sea
internal tagging, individuals were first placed in a shallow
(20 cm) bath containing anaesthetic until light anaesthesia
was achieved. Subsequently, a small (1.5 cm) incision was
made in the skin of the belly, just behind the ventral fins,
and a DST was inserted. The incision was then stitched
twice with EthiconÒ coated absorbable sutures (4/0 vicryl)
and the wound smeared with antibiotic powder mixed with
orahesive. All surgical instruments were sterilized before
use on each individual.
Fish release and recapture
In order to detect any adverse effects of the tagging
procedure, fish were placed in a shallow recovery tank
(60 cm deep) prior to being released into the sea. Fish that
did not make a sufficient recovery from the surgery and
anaesthetic were not released. Fish recaptures were made
through the commercial fishery, with a financial incentive
offered for their return.
0
Data analysis
Estimation of the rate of neutrally buoyant descent (Rt)
Analysis of the behaviour of cod immediately after tagging is
often avoided because of potential damage to or rupture of
the swimbladder caused by the capture procedure (Godø and
Michalsen, 2000) or because of potentially abnormal
behaviour resulting from tagging (e.g. Robichaud and Rose,
2001). In cases where the swimbladder of the individual
remains intact or where damage to the swimbladder has
healed rapidly, post-release behaviour is characterized by the
individual gradually increasing its mean depth to a relatively
stable ‘residence depth’ (usually the capture depth, pers.
obs.) over a period of days (Figure 1). During this time,
individuals make rapid vertical movements over very short
time periods. These movements are characterized by a large
vertical movement in one direction balanced by a movement
of equal magnitude in the opposite direction (Figure 1). Over
time, the upper limit of these vertical movements becomes
20
40
60
0
tadapt
Change in depth
Depth (m)
10
20
Dres
30
Adaptation
period
40
Time since release (h)
Figure 1. Depth profile for cod 1412, showing characteristic post-release behaviour. Values of the time taken for the cod to adapt (tadapt) to
a stable depth (Dres) are shown, and were used to calculate the rate of neutrally buoyant descent (Dt).
Quantifying vertical movements of cod
progressively deeper and post-tagging behaviour can
therefore be used to generate estimates of the rate of
neutrally-buoyant descent (Arnold and Greer-Walker,
1992), termed hereafter Rt, if it is assumed that the upper
limit of these ascents represents neutral buoyancy. The depth
records of 75 individuals were inspected and 10 records were
selected (Table 1) that represented particularly clear
examples of post-release depth adaptation.
Simple regression analyses between time during adaptation, depth, and temperature were often strongly influenced
by outlying values of depth and so were unsuitable for
accurate estimations of Rt. Instead we plotted a line of best
fit that extended through the uppermost portion of the depth
range (Figure 2) of each adaptation period, based on the
assumption that cod were neutrally buoyant only at the
upper limit of their depth range, and excluded points
outside of the FVR of the individual. A linear regression
was then performed between depth and time during
adaptation to find the value of Rt compatible with the
FVR (Rt FVR). We are confident that this method objectively eliminates outlying values to provide the best
possible estimate of Rt. Values of Rt estimated in this
way were compared to the theoretical maximum rate (Rt
potential) derived from the formula Rt potential Z 0.066T C
0.25, where T was mean temperature during the adaptation
period (after Harden Jones and Scholes, 1985).
Estimation of maximum rate of vertical movement
DST records of all individuals released between March and
May 1999 in the southern North Sea and for all individuals
released in the Barents Sea in April 1999 (Table 1) were
used in this analysis. The first two weeks of data after
release were excluded, so that the rates of movement were
those at mean residence depth and were representative of
cod detected on acoustic surveys and not of post-tagging
adaptation behaviour. Tag records were between three and
266 days in length. The depth change between each
sampling interval was calculated for the original sampling
1065
interval (10 min for cod tagged in the North Sea and 15 min
for cod in the Barents Sea), in addition to the depth change
between 30, 60, 120 and 240-min sampling intervals for
each tag record. Standardized maximum rates of ascent and
descent (m h1) were then extracted by day for each DST
record at each sampling interval. Mean maximum rates of
vertical movement were calculated by taking the mean of
the greatest vertical movement per day for all tag records.
Linear regression was used to calculate the relationship
between the values computed from the original sampling
rate and the resampled rates for each individual.
Estimation of tilt angle
Tilt angle in wild fish can only be measured with customized
sensors (Michalsen, unpubl. data). However, if the horizontal
distance travelled (D) by an individual is assumed to be
constant, i.e. speed over the ground is constant, tilt angle can
be inferred from the depth change (Dd) between very high
frequency recordings by calculating the arctangent of the
depth change divided by the distance travelled, i.e. arctan
(Dd/D).
Data from 10 cod (LTD-1200s, programmed to record at
10-s intervals for a period of 10 days; Table 1) were used to
calculate estimates of tilt angle, assuming swimming speeds
of 0.3, 0.5, 0.7, and 0.9 BL s1 (based on speeds estimated in
Arnold et al., 1994). Values of Dd less than 20 cm in
magnitude (approximately two-thirds of the raw data) were
excluded from the analysis to eliminate the effect of tidal
swell on estimates of depth.
Results
Rate of neutrally buoyant descent
Estimates of Rt FVR over the period of adaptation were
highly variable between individuals, ranging from
0.20 m h1 to 0.69 m h1. Some fish increased their depth
Time since release (h)
0
10
20
30
40
0
Depth (m)
10
20
30
40
Figure 2. Depth profiles of cod 1412 showing Dt FVR: linear regression using only the depth records within the limits of the free vertical
range (records shown by filled symbols, dashed black lines show the upper and lower depth limits of the FVR).
O. Heffernan et al.
1066
Table 2. Summary of results of depth adaptation analysis. Records were chosen after visual inspection of depth profiles of tagged cod
released in the North Sea (NS), Irish Sea (IS), and the Barents Sea (BS). The method of calculation for Dt is given in the text. FVR denotes
the free vertical range, as described in the text.
Tag number
780
791
1362
1412
1430
1433
1604
1635
1661
1657
Mean
Gs.d.
Location
Average temperature ((C)
Mean residence
depth (Dres) (m)
Time to reach
mean depth (tadapt) (days)
Number of observations (n)
Dt FVR
Dt potential
Proportion of n within FVR
Proportion of n O FVR
Proportion of n ! FVR
BS
6.1
78.6
BS
6.6
111.8
IS
8.2
105.0
NS
7.8
26.9
IS
8.1
62.5
IS
8.3
85.3
NS
6.6
67.1
NS
8.4
28.0
IS
8.3
57.3
NS
7.9
27.6
7.6
65.0
31.1
6.5
5.9
9.3
1.8
6.1
4.9
6.6
3.8
7.1
2.8
5.5
2.22
940
0.25
0.66
0.05
0.95
0.00
471
0.62
0.68
0.52
0.47
0.00
1343
0.26
0.79
1.0
0.0
0.0
257
0.69
0.77
0.81
0.12
0.07
874
0.52
0.79
0.91
0.06
0.03
708
0.67
0.80
0.89
0.10
0.01
948
0.30
0.68
0.19
0.81
0.00
543
0.24
0.80
0.91
0.08
0.01
1014
0.39
0.80
0.37
0.31
0.32
397
0.42
0.77
0.42
0.58
0.00
749
0.45
0.75
0.53
0.37
0.10
0.18
0.06
0.33
0.32
0.18
relatively slowly and steadily, whereas others descended
more rapidly and reached their residence depth in a shorter
time period (Table 2) and at a shallower depth, depending
on the area of release and recapture. The mean residence
depth ranged from 28 m in the North Sea to 112 m in the
Barents Sea. On average, individuals took 5.5 days to reach
a stable depth. All estimated values of Rt FVR were less than
1 m h1 (Table 2). None of the observed values reached the
maximum physiological rate (Rt potential), as defined by
Harden Jones and Scholes (1985) (Table 2).
Maximum rate of vertical movement
Post-adaptation, cod exhibited rapid vertical movements that
greatly exceeded the highest estimates of neutrally buoyant
descent and ascent. Overall, the rates of vertical movement
estimated for cod in the Barents Sea were much higher than
rates estimated for North Sea cod. At the highest sampling
frequency, maximum ascent rates were estimated as
approximately 32 m h1 in the North Sea and 174 m h1 in
the Barents Sea (Table 3). The estimated maximum rates of
descent were similar in magnitude. The estimates of mean
maximum ascent rate and descent rate declined as sampling
frequency decreased (Figure 3). At the lowest sampling
frequency, estimates of maximum ascent rates fell to
1.14 m h1 for the North Sea, a 30-fold difference, and
7.9 m h1 for the Barents Sea, a 25-fold difference. As
sampling frequency decreased, so too did the proportion of
variability explained by a linear regression between the
estimate of maximum rate of movement derived from the
original sampling rate for ascent and descent rates (Tables 3,
4). All mean maximum rates of short-term vertical descents
exceeded the maximum physiological rates of neutrally
buoyant movement. The highest rate of movement observed
for cod in the North Sea was 374 m h1 at the highest
sampling frequency and decreased to 15 m h1 at the lowest
sampling frequency. In the Barents Sea, the maximum
observed ascent rate was 719 m h1 and maximum descent
rate 902 m h1, decreasing to 88 m h1 and 65 m h1,
respectively, at the lowest sampling frequency.
Tilt angle
The mean distance moved between successive 10-s sampling
intervals was 0.48 m G 0.4 m, but rose above 20 m in
exceptional cases. Calculated tilt angle ranged between
Table 3. Mean (Gs.d.) maximum rates of vertical movement (m h1) estimated at various sampling intervals (minutes) for North Sea and
Barents Sea cod in the period post-adaptation. The original sampling interval was 10 min for the North Sea and 15 min for the Barents Sea.
North Sea cod
Sampling interval
10 or 15
30
60
120
240
Mean maximum
ascent rate
31.65
9.58
4.57
2.24
1.14
(31.74)
(10.31)
(5.16)
(3.51)
(5.27)
Barents Sea cod
Mean maximum
descent rate
30.99
9.30
4.43
2.16
1.07
(30.03)
(9.65)
(4.76)
(3.40)
(5.26)
Mean maximum
ascent rate
Mean maximum
descent rate
174.37
90.35
41.21
18.95
7.9
193.39
94.03
40.54
20.73
7.99
(154.31)
(93.74)
(41.06)
(24.03)
(27.03)
(175.11)
(103.74)
(43.85)
(26.28)
(26.58)
Quantifying vertical movements of cod
85( and 85(, with the distribution of tilt angle becoming
more kurtose as assumed swimming speed increased (Figure
4a). Deviations from the horizontal of 5( or greater were
common at all assumed swimming speeds (100% at
0.3 BL s1 decreasing to 31% at 0.9 BL s1). Values above
15( were relatively rare (47% decreasing to 4%). Tilt angles
were significantly lower during hours of daylight, regardless
of assumed swimming speed (Figure 4b; Student’s t-test,
values of t1,23 between 4.35 and 5.55, p ! 0.001 in all cases).
Mean maximum ascent rate (m h-1)
(a)
70
60
50
40
30
20
10
Discussion
0
0
100
200
300
Sampling interval (min)
(b)
Mean maximum ascent rate (m h-1)
1067
350
300
250
200
150
100
50
0
0
50
100
150
200
250
300
Sampling interval (min)
Figure 3. Mean (Gs.d.) daily maximum ascent movement rate
estimated at various sampling intervals for (a) tagged cod released
in the North Sea (n Z 32 individuals, 2557 days of data) and (b)
tagged cod released in the Barents Sea (n Z 9 individuals, 210
days of data).
Table 4. Mean regression coefficient (b) and R2 values (Gs.d.) for
the regression of the rate of movement estimated at original
sampling frequencies against the rate estimated at less frequent
intervals for cod in the North Sea (2224 observations).
Sampling intervals
(min)
Ascents
10 vs.
10 vs.
10 vs.
10 vs.
Mean
b (Gs.d.)
Mean R2
(Gs.d.)
30
60
120
240
0.29
0.16
0.07
0.03
(0.07)
(0.10)
(0.02)
(0.02)
0.71 (0.25)
0.68 (0.21)
0.6 (0.23)
0.47(0.28)
Descents
10 vs. 30
10 vs. 60
10 vs. 120
10 vs. 240
0.24
0.11
0.05
0.02
(0.08)
(0.04)
(0.02)
(0.01)
0.61
0.48
0.37
0.33
(0.26)
(0.26)
(0.22)
(0.24)
Although behaviour accounts for only one potential source
of bias in reference target strength for acoustic estimates
(MacLennan and Simmonds, 1992; Rose et al., 2000), the
ICES Working Group on Fisheries Acoustic Science and
Technology recently concluded that fish behaviour is one of
the greatest potential sources of bias in fisheries acoustics
(ICES, 2000). Lack of high-resolution observational data
remains a barrier to assessing the real implications of cod
behaviour for acoustic survey estimates (MacLennan and
Simmonds, 1992). Although the data and analyses presented
here are by no means exhaustive, it is clear that highresolution data obtained from archival tags provide a means
to explore the systematic variation in vertical movement
exhibited by cod. Overall, the present study suggests several
reasons why acoustic returns from cod are unlikely to meet
the requirements of reference target strength assumptions.
Gas secretion into the swimbladder is slow. Depth adaptation
was an obvious and stereotypical behaviour that permitted
the estimation of rates of neutrally buoyant descent. The Rt
values of between 0.24 and 0.69 m h1 were comparable to
those reported by Arnold and Greer-Walker (1992) of
0.3e0.8 m h1 for cod in the North Sea and to rates of
0.3e0.6 m h1 calculated for DST-tagged cod in Icelandic
waters (Thorsteinsson, 1995). The variation of Rt between
individuals indicates that the rate of gas secretion to the
swimbladder was variable under natural conditions, although
never rapid enough to allow individuals to make rapid
descents and remain neutrally buoyant. Maximum rates of
vertical movement can be very high. Large, sporadic vertical
movements of wild cod have been reported previously
(Zilanov, 1963; Beamish, 1966; Rose, 1993; Lawson and
Rose, 1999; Godø and Michalsen, 2000; Stensholt et al.,
2002). The high-frequency depth data described in the
present study provide clear evidence that cod routinely and
frequently make vertical movements at a rapid rate in both
the North and Barents Seas. Our results show that lowfrequency sampling (O10-min intervals) underestimated the
real maximum rate of vertical movement of cod (e.g.
Thorsteinsson, 1995; Godø and Michalsen, 2000), and that
the maximum rates of vertical movement recorded by highfrequency sampling in both regions were inconsistent with
the maintenance of neutral buoyancy.
O. Heffernan et al.
1068
(a)
0.25
0.3 BL
0.5 BL
0.7 BL
0.2
Frequency
0.9 BL
0.15
0.1
0.05
0
-23 -21 -19 -17 -15 -13 -11 -9 -7 -5 -3 -1
1
3
5
7
9 11 13 15 17 19 21
Tilt (°)
(b)
20
Deviation from horizontal (°)
18
16
14
12
10
8
6
0.3 BL
4
0.5 BL
0.7 BL
2
0.9 BL
0
0
2
4
6
8
10
12
14
16
18
20
22
24
Time of day (h)
Figure 4. Estimated tilt angle of 10 individual cod tagged and released in the northern North Sea. Tilt angles were calculated from all
vertical movements O20 cm (n Z 218 074). (a) Distribution of tilt angles at a range of assumed swimming speeds, where positive angles
denote a ‘head-up’ orientation and negative angles a ‘head-down’ orientation. (b) Mean deviation from the horizontal ( positive or negative
tilt) at different times of the day. Solid symbols show night-time values, while hollow symbols show daytime values.
To avoid underestimation of real vertical movement rates,
depth data should be collected at as high a frequency as
possible. Our analyses show that rates of vertical movement
should be sampled at a frequency of 10-min intervals, and
perhaps even more frequently. Where data storage in the tag
is limited, short periods of high frequency depth recordings
could be used to ‘fingerprint’ vertical movement behaviour in
order to extend the inferential power of the lower-frequency
data and maximize the efficiency of memory usage.
Extremely high-frequency depth data revealed that cod
were often tilted at an angle to the horizontal. The
distribution of tilt angle was fairly broad (as for Harden
Jones and Scholes, 1981) and cod deviated more than 5(
from the horizontal for a considerable proportion of the
time. This was more pronounced at night (as for Foote,
1985). Changes in tilt angle caused by swimming motion,
such as those described here, could cause systematic
changes in target strength in the region of 3e4 dB (Nakken
Quantifying vertical movements of cod
and Olsen, 1977; Rose and Porter, 1996). McQuinn and
Winger (2003) reported a 6 dB decrease in target strength
of cod in situ between a tilt angle of 0( and 10( head-up,
which showed a systematic bias with time of day. Ideally,
tilt angle in cod would be measured directly (Godø and
Michalsen, 2000), and given that DST compatible sensors
already exist (Mitson and Holliday, 1990), this is clearly an
important and achievable goal. In the absence of direct
measurements, however, and given the extreme paucity
of data on tilt angle distributions in free-living fish
(McClatchie et al., 1996a, b), the qualitative agreement of
the computational analysis with published results suggests
that the intentionally simple method of calculating tilt angle
has merit in providing insights into behaviour. An evolution
of the analysis would be the calculation of the tilt angle of
the swimbladder, as opposed to the fish, which may be
tilted as much as 7( upward, relative to the snoutetail axis
of the fish (Blaxter and Batty, 1990). The effect of tilt angle
on target strength could then be the subject of some simple
modelling.
Conclusions
Overall, the present study suggests that acoustic returns
from cod are unlikely to meet the requirements of reference
target strength assumptions. First, cod may often be positively or negatively buoyant, rather than neutrally buoyant,
as assumed in target-strength calculations, because they can
ascend and descend faster than neutral buoyancy can be
maintained. Second, cod undertake frequent ascents and
descents that require individuals to continually adjust their
tilt angle in the water column, especially at night.
Combined, these results suggest that the average strength
of echo-returns from individual cod is likely to be lower
than the reference target strength (see also Nakken and
Olsen, 1977). The implication is that cod biomass
calculated from acoustic-based surveys may be consistently
and systematically underestimated unless corrective factors
are applied to reference target-strength values. We suggest,
like Nakken and Olsen (1977) and Ona (1990) before us,
that the species-specific target strength for wild fish should
be adjusted to account for changes in target strength that
occur naturally. Integrating this knowledge of cod behaviour and applying it to the design of survey methods and the
interpretation of survey results would therefore be of
obvious benefit.
Acknowledgements
We thank Julian Metcalfe for valuable discussions, Bob
Turner and the crew of RV ‘‘Clupea’’ for assistance with fish
tagging, and two anonymous referees whose comments
considerably improved this study. Funding for this work was
provided by the UK Government (Defra project MF0317)
and by the Fisheries Directorate of the EU through projects
1069
EU-FAIR-CT98-4122/STEREO and EU-FP5-Q5RS-200200813/CODYSSEY).
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