ICES Journal of Marine Science, 61: 1278e1290 (2004)
doi:10.1016/j.icesjms.2004.09.005
Vertical distribution and feeding patterns in fish foraging
on the krill Meganyctiphanes norvegica
M. S. R. Onsrud, S. Kaartvedt, A. Røstad, and T. A. Klevjer
Onsrud, M. S. R., Kaartvedt, S., Røstad, A., and Klevjer, T. A. 2004. Vertical distribution
and feeding patterns in fish foraging on the krill Meganyctiphanes norvegica. e ICES
Journal of Marine Science, 61: 1278e1290.
Fish and krill were studied at a 120 m deep site in the Oslofjord, Norway. Herring (Clupea
harengus), whiting (Merlangius merlangus), and Norway pout (Trisopterus esmarkii) were
foraging on krill (Euphausiacea, Meganyctiphanes norvegica) during both day and night.
During daytime, herring and whiting were foraging in the upper and middle part of the krill
assemblage, while the deep-living, and often benthopelagic Norway pout was approaching
the krill from below. Krill and fish ascended and fish schools dispersed at dusk. At night,
herring and whiting were feeding near the surface, with the shallowest distribution
suggested for herring. Norway pout foraged in midwater. Krill antipredator behaviour
comprised diel vertical migration and instantaneous escape reactions, and the krill also
appeared to actively seek out strata with low acoustic recordings of fish. Fish accumulated
beneath the research vessel when the ship was anchored at a fixed location during acoustic
studies, apparently resulting in artificially high local fish abundances. Since we suggest that
krill respond to the presence of fish, such high fish abundance may bias studies of
interactions between the fish predators and their krill prey.
Ó 2004 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.
Keywords: antipredator behaviour, fish accumulation, fish and krill distribution, fishekrill
interaction.
M. S. R. Onsrud, S. Kaartvedt, A. Røstad, and T. A. Klevjer: Department of Biology,
University of Oslo, PO Box 1066, 0316 Oslo, Norway. Correspondence to S. Kaartvedt: tel:
C47 22854739; fax: C47 22854438; e-mail: [email protected].
Introduction
The vertical distributions of plankton and fish often reflect
a trade-off between optimizing food intake and minimizing
risk of predation (Johnsen and Jakobsen, 1987; Lazzaro,
1987; Aksnes and Giske, 1990; Bollens and Frost, 1991;
Milinski, 1993; Loose and Dawidowicz, 1994), being
further mediated by temperature owing to its regulating
effect on metabolic rates (Wurtsbaugh and Neverman,
1988; Giske et al., 1990; Dawidowicz and Loose, 1992).
Fish are normally visual predators, and feeding is most
efficient in daylight and in shallow water. Small planktivorous fish are themselves subject to predation by piscivores.
They may reduce risk of daytime predation by schooling
(e.g. Gallego and Heath, 1994; Connell, 2000), or by diel
vertical migrations (e.g. Clark and Levy, 1988). Some small
planktivores live in close association with the bottom
during the day (Albert, 1994; Kaartvedt et al., 1996),
migrating upwards into the water column at night
(Beamish, 1966; Bailey, 1975; Albert, 1994, 1995).
Vertical gradients in visual encounter rates between
predators and prey will be species-specific, partly as
1054-3139/$30.00
a function of eye size (Aksnes and Giske, 1993), but will
be absent in darkness at great depths. Models of planktivore
foraging typically assume negligible foraging by particulate
feeders below their visual foraging thresholds (Giske and
Salvanes, 1995). However, many particulate feeders can
forage non-visually (Montgomery et al., 1988; Janssen,
1996; Ryer et al., 2002). Laboratory studies suggest that
some fish locate their prey by means of the mechanosensory
lateral-line system when low light renders vision ineffective
(Dijkgraaf, 1963; Janssen et al., 1995; Janssen, 1997; Ryer
et al., 2002). Some planktivorous fish species respond to
mechanical stimuli imitating prey (Janssen, 1996), and both
swimming behaviour (Barham, 1966; Janssen et al., 1992),
and lateral-line morphology (Janssen et al., 1995) suggest
that they may be partially tactile predators.
Euphausiids, and in the North Atlantic specifically the
krill Meganyctiphanes norvegica, are key organisms in
food webs, utilizing diverse food sources and being
prominent prey organisms for planktivores. Previous
studies in the Oslofjord have revealed that M. norvegica
is the main constituent of an acoustic scattering layer (SL)
that stays below ca. 70 m by day and migrates upwards at
Ó 2004 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.
Distribution and feeding of fish on krill
night (Onsrud and Kaartvedt, 1998; Kaartvedt et al., 2002).
The krill layer typically remains below schooling fish by
day (Onsrud and Kaartvedt, 1998; Bagøien et al., 2000),
although records of fish schools in the upper fringe of the
krill layer have been made (Klevjer, 2001; Kaartvedt et al.,
2002). Their vertical distributions overlap at night. Another
group of fish seems to be associated with the krill during
both day and night, and a third group leaves the benthic
boundary zone near sunset, migrating into midwater
(Onsrud and Kaartvedt, 1998; Kaartvedt et al., 2002). The
identities and the feeding patterns of these fish have not
been established.
Knowledge of distribution and behaviour of planktivorous fish is essential for understanding plankton ecology.
Likewise, plankton distribution and behaviour are essential
driving forces for the distribution and behaviour of fish.
Therefore, in a series of studies, we aimed to address both
the fish and plankton components of the ecosystem in the
Oslofjord, Norway (e.g. Onsrud and Kaartvedt, 1998;
Bagøien et al., 2000; Kaartvedt et al., 2002; Klevjer and
Kaartvedt, 2003). In the present study, we investigate the
distribution and feeding of the fish co-occurring with
the krill during the diel cycle. Our aims were to identify the
main component of the fish assemblage, establish their
vertical distributions, and assess their diel feeding patterns.
Material and methods
The study was conducted at a 120 m deep site in the
Oslofjord, Norway, March 1998, March 2000, November
2000, March and June 2001. Additionally, trawl catches
from March 1997 were included. Descriptions of the study
site are given by Onsrud and Kaartvedt (1998) and Bagøien
et al. (2000). The RV ‘‘Trygve Braarud’’ was anchored at
a fixed position (59(48#N 10(34#E) during diel acoustic
studies. Trawling was conducted in transects adjacent to the
anchor station.
Sampling procedures for temperature, salinity, oxygen
and light measurements were the same as detailed in
Onsrud and Kaartvedt (1998). Chlorophyll a concentrations
were analysed in water samples from discrete depths
1279
according to the procedures of Strickland and Parsons
(1972). Subsurface light extinction was measured in the
upper 25 m using a 2P LiCor 190SA quantum sensor.
Mesozooplankton was collected by a WP2 plankton net
(Tranter, 1968). The net was hauled vertically at 50 cm sÿ1,
and filtered volumes were estimated by multiplying towing
distance with net aperture. Duplicate daytime-series (five
depth intervals covering the whole water column) were
taken in November 2000, March and June 2001. Previous
studies have shown little variation between replicated net
tows (Vedal, 1997), and identification and enumeration was
therefore made for only one of the series for each survey.
Acoustic studies
SIMRAD EK500 echosounders (software version 5.3) with
38- and 120-kHz split-beam transducers were used for
studies of fish and krill. Fish are recorded on both
frequencies, while krill are mainly detected at 120 kHz,
where they appear as recognizable blue scattering layers
(Onsrud and Kaartvedt, 1998; Kaartvedt et al., 2002;
Klevjer and Kaartvedt, 2003).
We applied hull-mounted transducers in various combinations with submerged transducers (Table 1). The submerged transducers were used to obtain better resolution of
deep-living targets (partly for use in other studies), but also
to observe if the abundance of acoustic targets deviated
immediately beneath and at some distance away from the
ship. For each frequency, only one transducer could be used
at a given time. The submerged 120-kHz transducer was
used in a downward-looking mode immediately beneath the
ship, while the 38 kHz was placed on the sea bottom, facing
upwards (at various distances from the ship; Table 1), and
was coupled to the EK500 on board ‘‘Trygve Braarud’’ by
a 300-m cable. This transducer was mounted to a steel
frame with gimbal couplings to ensure horizontal orientation of the transducer surface. Total weight of the
transducer with frame was ca. 100 kg.
Data were stored by the software program Echo
Receiver (Mork, 2000) and later processed by the EP500
postprocessing software, version 5.4 (Lindem and Al
Houari, 1993) and by the Sonar 5 postprocessing software,
Table 1. Transducers and location of transducers for the various sampling periods. The submerged 120 kHz transducer was downwardlooking, 38 kHz transducer located on the sea floor was directed towards the surface.
38 kHz
Hull-mounted (12()
March 1998
March 2000
November 2000
March 2001
June 2001
120 kHz
Submerged (7.1()
X
X
Hull-mounted (7.1()
Submerged (7.1()
X
66 m, vessel side
sea floor, vessel side
sea floor, 80 m distance
sea floor, 80 m distance
X
50 m, vessel side
50 m, vessel side
1280
M. S. R. Onsrud et al.
version 5.8.7 (Balk and Lindem, 2002). The EK500 was
operating at maximum pulse repetition frequency, i.e. ca.
2 sÿ1 for the 120-m depth range. The vertical resolutions
were 10 cm and 3 cm for the 38 and 120 kHz, respectively.
Pulse durations were 1 ms (38 kHz) and 0.3 ms (120 kHz).
The main engine of the vessel was turned off, and only
navigation lights were lit during acoustic studies.
Trawling
Pelagic and bottom trawling were used to identify acoustic
targets, establish their size distribution, and provide
stomachs for diet investigation. A total of 66 pelagic and
24 bottom hauls were taken.
We used a pelagic trawl with an aperture of about
100 m2, towed at 2 knots. The mesh size was 20 cm near
the opening, declining to 1 cm at the rear end. The pelagic
trawling depths were selected so as to target the acoustic
recordings. Fishing depth was measured by an autonomous
mini-STD (SAIV model 202), attached to the trawl. Since
the exact depth could first be established after the tow,
fishing depth during trawling was estimated as 1/3 of the
wire length, a relationship derived empirically from earlier
trawling surveys. Effective trawling time (from the time the
trawl was at the desired trawling depth until haulback) was
generally between 20 and 30 min.
The bottom-trawl aperture was 57 m2, with a mesh size
of 2 cm at the rear end. Bottom trawling was performed
with a vessel speed of 1.5 knots. Bottom trawling was only
performed during daytime.
All fish were identified to species, counted, measured for
total length (TL) according to Fotland et al. (2000),
weighed, and thereafter frozen at ÿ18(C. For fish with
a total length larger than 25 cm, stomachs were removed,
weighed, and frozen separately. Stomach fullness was
categorized in groups on a scale from 1 to 5 (1 denotes
empty, 5 full/distended) according to Fotland et al. (2000).
The volume of krill captured in each tow was noted.
Frozen fish/stomachs from the November 2000, March
and June 2001 cruises were later thawed and analysed in the
laboratory. Prey organisms in the stomachs were identified
to the lowest possible taxon. Prey organisms were counted
and the wet weight of the stomach content and krill fraction
was determined. State of digestion was categorized to
groups on a scale from 1 to 5 (1 denotes undigested, 5 fully
digested/unrecognizable; Fotland et al., 2000).
Results
Environmental data
Below ~30 m for all surveys, the vertical temperature and
salinity profiles were practically homogenous with depth
(Figure 1A). Temperature at the surface varied between
surveys, with a minimum temperature of 2.2(C in March
1997 and a maximum of 20(C in June 2001. Salinity
declined markedly above the sill depth of 19 m, except for
March 2001 when there was virtually no salinity gradient.
The water was generally well oxygenated, apart for low
oxygen content at midwater depth in November (min.
1.5 ml lÿ1, oxygen saturation 22.8% at 62 m; Figure 1A).
The maximum chlorophyll a concentration in the upper
10 m varied between 1.2 and 3 mg lÿ1 (Figure 1B). The 1%
light depth was particularly shallow in November (4 m), and
occurred between 12e15 m for the other study periods.
Copepod distribution
Copepods were usually most abundant in the uppermost
25 m (Figure 1C). Pseudocalanus sp. dominated the upper
layer in November, while over-wintering Calanus spp.
were the most abundant species at depth at that time. In
March and June, juvenile Calanus spp. and Temora spp.
dominated the upper stratum. The most abundant
cyclopoid species at all depths were Oithona spp. and
Oncaea spp.
Distribution of krill and fish
The krill layer was restricted to waters deeper than ca. 70 m
during the day, mainly concentrated in a 20e40-m thick
layer (Figure 2A, B). The krill ascended at dusk, followed
by a subsequent descent shortly after reaching the surface.
However, in March 1998 strong recordings of krill were
made close to the surface also later at night. These
recordings followed a break for trawling, and represent
a period when recordings of fish were low in the upper
30 m (cf. upper left, right-hand part of Figure 2A).
By day, fish schools occurred above the krill layer,
particularly evident the second day of the studies (Figure
2AeC). Some schooling fish were also occasionally seen
entering the krill layer (e.g. Figure 3). Non-schooling fish
(appearing as a scattering layer (SL) in the compressed
plots) were distributed together with the krill. Additionally,
fish occurred below the krill layer, apparently associated
with the bottom in March and living pelagically below
about 90 m in November (Figure 2AeC).
Fish ascended and schools dispersed at dusk (Figure 2).
Fish from the pelagic schools and those associated with the
krill layer concentrated in the upper ~30e40 m. The
benthopelagic fish ascending from near the bottom established a scattering layer in midwater, below ~40 m. The
upper fringe of this midwater layer maintained its vertical
distribution throughout the night, before performing a coherent downward migration in the morning (starting approximately 1 h before sunrise). In contrast, on two of three
occasions the lower edge of the layer started sinking long
before the approach of daylight. This is most conspicuous in
the March 1998 echogram (Figure 2A), when the SL
descended at a velocity of about 1.5 cm sÿ1. An apparent
dawn rise of the lower edge was recorded in November.
Distribution and feeding of fish on krill
1281
March 98
March 97
March 00
Temperature (°C) , salinity (psu) and oxygen (ml l-1)
0
20
40 °C
20
40 °C
0
20
40 °C
psu
psu
psu
ml l-1
ml l-1
A)
0
0
20
40
60
80
100
120
November 00
March 01
Temperature (°C) , salinity (psu) and oxygen (ml l-1)
0
20
40 °C
0
0
20
40 °C
0
psu
psu
ml l-1
ml l -1
June 01
40 °C
20
psu
ml l -1
20
40
60
80
B)
Depth (m)
100
120
Chl. a (µg l-1)
0
1
2
3
0
1
2
3
0
1
2
3
0
20
40
60
80
100
120
Copepods m-3
C)
0
1000 2000 3000
0
1000 2000 3000
0
2000 4000 6000
0
20
40
60
80
100
120
Figure 1. Vertical distributions of A) temperature (solid line), salinity (broken line), oxygen (broken, dotted line); B) chlorophyll a; and C)
copepods (black cyclopoid, grey calanoid) for the various sampling periods.
In March 2001, a loosely aggregated and dielly migrating
~15-m thick SL was the prevailing acoustic structure, as
seen from the bottom-mounted transducer. However, in the
morning of the 28 March, when switching from bottom- to
hull-mounted transducer, a distinct difference in backscattering from the two ensonified volumes was observed, with
much stronger fish records obtained from the hull-mounted
transducer (Figure 4). The 38-kHz volume backscattering
M. S. R. Onsrud et al.
1282
16:45
A)
Sunset Krill
Ship passage
03:30
21:10
Fish
Sunrise Krill 07:50
5
35
Break
for
trawling
65
95
120
13:10
B)
Sunset
Sunrise
0
30
45
48
51
54
57
10:30 60
63
66
69
72
75
78
60
Depth (m)
90
120
C)
15:00
09:30
Sunrise
Sunset
5
35
65
95
120
D)
14:20
0
30
Sunset
Sunrise
08:15
42
45
48
51
54
57
60
63
66
69
72
75
60
90
110
Figure 2. Acoustic recordings: A) 4e5 March 1998, 120-kHz (7.1() hull-mounted transducer. B) 13e14 November 2000, 120-kHz (7.1()
hull-mounted transducer. Sv threshold for A) and B) ÿ78 dB. C) 15e16 March 2000, 38-kHz (12() hull-mounted transducer. D) 27e28
March 2001, 38-kHz (7.1() bottom-located transducer. Sv threshold for C) and D) ÿ75 dB.
A)
0
Depth (m)
Distribution and feeding of fish on krill
76
1283
86
125
Time (h)
76
Depth (m)
B)
86
Figure 3. 120-kHz recordings 16 March 2000. A) Echogram from hull-mounted transducer, 11:54 to 12:14 hours, Sv threshold ÿ78 dB.
The area bounded by horizontal red lines show the depth range covered by the printout from the submersible transducer. B) Echogram
printout from submersible transducer with 10-m depth range, showing the scattering layer with greater resolution, 08:09 to 08:16 hours.
(Sv) from the layer below 75 m differed by ca. 9 dB,
indicating an about eight times higher biomass directly
beneath the vessel compared to 80 m away from the vessel.
Volume backscattering increased with time beneath the
ship throughout the diel studies, as evidenced from the
records by the hull-mounted transducers. This phenomenon
could not be observed in March (or June), when the
upward-looking, bottom-mounted transducer was located
away from the vessel.
Repeatedly, virtually all fish targets disappeared from the
acoustic beam, resulting in ‘‘voids’’ in the recordings
(Figure 2). This coincided with ships passing at a distance
of 200e400 m.
Trawling
Krill (Meganyctiphanes norvegica), whiting (Merlangius
merlangus), Norway pout (Trisopterus esmarkii), herring
M. S. R. Onsrud et al.
1284
Depth (m)
A)
0
B) 0
30
30
60
60
90
90
110
120
Time (h)
Figure 4. 38-kHz recordings 28 March 2001, Sv threshold ÿ75 dB; A) bottom-located transducer (7.1() 07:35 to 08:15; B) hull-mounted
transducer (12() 09:01 to 09:44.
(Clupea harengus), and sprat (Sprattus sprattus) were the
prevailing species in the pelagic trawl catches. Moreover,
catches in June were totally dominated by jellyfish (Cyanea
capillata and Aurelia aurita), mainly in the size range
5e35 cm.
Daytime catches increased with depth, apart for sprat,
which gave the largest daytime catches in midwater (Figure
5; all hauls pooled). At night, herring, whiting, and sprat
were most abundant in the upper 50 m, with the shallowest
distribution suggested for herring. Norway pout had the
deepest nocturnal distribution, with maximum abundance in
midwater and no catches in the upper 25 m.
Sprat, whiting, and Norway pout were also present in the
bottom trawls, but the prevailing species in these catches
were rockling (Rhinonemus cimbrius) and American plaice
(Hippoglossoides platessoides) (Table 2). Shrimps were
numerous in March and June 2001. Catches of krill were
insignificant in the bottom trawl.
found by day in March, but neither stomach fullness nor
state of digestion revealed clear diel patterns in food uptake
(Table 3). Copepod remains in November were dominated
by Centropages spp., and cladocerans were also identified.
These groups were only represented in the WP2-hauls in
the upper 25 m. Herring additionally preyed upon polychaetes, isopods, and small decapods, indicating feeding at
depth during the day.
Sprat stomachs did not contain krill prey. The stomach
contents comprised large numbers of newly eaten (state of
digestion 1e3) copepods and zooplankton larvae by night
in March, while no stomachs had newly eaten food items
during day. In November, stomach fullness was generally
low and state of digestion high at all times. However, a few
sprat caught in upper layers during the day had newly eaten
Temora spp., Calanus spp., and Centropages spp.
Discussion
Fish distribution and feeding
Feeding
For whiting, krill constituted up to 99% of the stomach
content by weight, on average ~82% during both day and
night (maximum number of krill found in one stomach was
40 krill; fish length 21 cm). Small sprat, a few decapods,
amphipods, and polychaetes were also found in the whiting
stomachs. No systematic trends were apparent comparing
proportion of stomachs containing krill or state of digestion
during the day and night (Table 3).
The diet of Norway pout was dominated by M. norvegica
and calanoid copepods, particularly Calanus spp. Also a few
decapods and amphipods were found in the Norway pout
stomachs. No significant differences in stomach fullness, or
normalized stomach wet weight could be found between
day/night (chi-square and KruskaleWallis tests, p O 0.05).
Herring stomachs contained krill prey during both day
and night. The highest number of krill per stomach was
Schooling fish occurred above and in the upper part of the
krill layer by day, while schools dispersed at night, in
accordance with previous studies at the station (Onsrud and
Kaartvedt, 1998; Bagøien et al., 2000; Røstad, 2000;
Kaartvedt et al., 2002). The relative contribution of sprat
and herring in these acoustic signatures is hard to assess, as
it is inherently difficult to capture schooling fish by small
pelagic trawls. However, the catches suggested that
a majority of herring belonged to the deepest schools (cf.
Figure 5), the acoustic recordings demonstrated spatial
interaction between krill and the deep schooling fish by day
(cf. Figure 3), and the stomach contents of herring did
suggest feeding by day in deep water.
Herring stomachs contained krill during both day and
night, but stomach contents were always well digested. Any
nocturnal predation on krill would be restricted to the
shallowest fringe of the krill population, as indicated from
Distribution and feeding of fish on krill
1285
Numbers per litre per nautical mile (+s.e.)
0
10
20
30
40
50
0
10
20
30
40
50
2
4
6
8
10
0
2
4
6
8
10
10
20
30
40
50
0
10
20
30
40
50
200
0
75
0
Whiting
Depth (m)
0 - 25
25 - 50
50 - 75
75 - 100
0
Norway pout
Depth (m)
0 - 25
25 - 50
50 - 75
75 - 100
0
Herring
Depth (m)
0 - 25
25 - 50
50 - 75
75 - 100
0
50
100
150
50
100
150
200
Sprat
Depth (m)
0 - 25
25 - 50
50 - 75
75 - 100
0
25
50
25
50
75
Krill
Depth (m)
0 - 25
25 - 50
50 - 75
75 - 100
Day
Night
Figure 5. Vertical distribution for whiting, Norway pout, herring, sprat, and krill from trawl catches, all hauls pooled (nday Z 37;
nnight Z 29).
the shallow distribution of herring. During our investigations, nocturnal light levels at the surface would range from
about 10ÿ4 to 10ÿ6 mmol mÿ2 sÿ1 (full moon to clear nights
with no moon). The lower visual threshold for herring
feeding by biting (as apposed to filter-feeding) is ranging
from 3.6 ! 10ÿ2 to 7 ! 10ÿ3 lux (Blaxter, 1964), equalling
1.4 ! 10ÿ4 to 7 ! 10ÿ4 mmol mÿ2 sÿ1. This would suggest
the possibility of visual feeding close to the surface (cf.
Batty et al., 1986; Blaxter, 1988).
The trawl catches showed that whiting were associated
with the krill during both day and night, and the single fish
targets in the krill SL would largely represent this species.
Although the visual threshold for whiting feeding on
M. norvegica is not established, whiting is expected to have
a lower visual threshold than herring, due to their larger eye
size (cf. Aksnes and Giske, 1993; Torgersen, 2001a).
Whiting foraging in deep SLs of krill during daytime have
been observed in previous studies from Lurefjorden, western
Norway, which is characterized by low light penetration in
the basin water (Bagøien, 1999; Torgersen, 2001a).
We suggest that whiting was foraging on krill during
both day and night in the Oslofjord. The proportion of
1286
Table 2. Bottom trawl catches by day. Numbers in parenthesis are figures normalized to catch per nautical mile. Others include the species haddock (M. aeglefinus), blue whiting
(M. poutassou), herring (C. harengus), poor cod (T. minutus), silvery pout (G. argenteus thori), eelpout (Z. viviparous), Mueller’s pearlside (M. müelleri), goby (A. minuta), and thorny skate
(R. radiata) (total number !10 for all trawls pooled).
Norway pout
Whiting
Cod
Rockling
Sprat
American plaice
Plaice
Flounder
G. morhua
R. cimbrius
S. sprattus
H. platessoides
P. platessa
G. cynoglossus
4(5.33)
15(20)
5(20)
2(2.7)
9(8.6)
12(12)
2(3.2)
15(20)
2(8)
2(2.7)
4(3.8)
10(10)
17(27.2)
1(1.3)
6(6.9)
5(13.3)
4(4.6)
5(3.6)
6(5)
13(11.1)
19(16.2)
24(21.3)
24(19.2)
4(5.3)
4(5.3)
1(1.1)
7(9.3)
Time
T. esmarkii
M. merlangius
12 Mar 1997
11:15
12:40
10:45
11:35
13:15
12.20
13.45
09.35
10:40
11:30
14:00
15:15
09:37
11:20
12:50
14:40
11:45
12:45
13:35
11:25
12:15
14:20
15:15
16:20
3(4)
1(1.3)
19 Mar 1997
2 Mar 1998
16 Nov 2000
27 Nov 2000
28 Mar 2001
18 Jun 2001
n.d., no data.
6(8)
1(4)
1(1.3)
1(1)
1(1.1)
2(5.3)
1(0.7)
1(1.1)
2(2.3)
4(10.7)
1(1.1)
1(0.7)
1(0.9)
1(0.9)
1(1.3)
1(0.9)
1(0.8)
9(12)
11(14.7)
4(4.6)
5(6.7)
1(1.1)
3(3.4)
1(1)
2(2)
5(6.7)
1(1.3)
1(1.3)
1(1)
2(2)
1(1.6)
1(0.9)
3(2.6)
2(1.8)
3(4)
9(12)
4(4.6)
11(14.7)
2(2.7)
3(3.4)
12(10.7)
18(18)
4(6.4)
1(1.3)
1(1.1)
1(2.7)
1(1.1)
2(1.5)
2(1.7)
3(2.6)
6(5.1)
11(9.8)
3(2.4)
3(4)
6(6.9)
2(2.7)
1(1.3)
2(2.3)
2(2)
1(0.9)
6(5.1)
1(0.9)
4(3.2)
1(1.3)
5(5.7)
7(7)
Others
Krill (l)
5(6.7)
4(3.8)
4(4)
!0.5(0.7)
!0.5(0.5)
Shrimps (l)
3(4)
3(3)
3(4.8)
1(1)
2(3.2)
!0.5(0.8)
1(1.1)
1(1.1)
2(1.7)
1(1.1)
3(3.4)
2(1.5)
2(1.7)
1(0.9)
1(0.9)
1(1.3)
1(1.3)
1(1.1)
2(2.3)
1(0.8)
1(1.3)
1(1.3)
3(3.4)
2(2.3)
!0.5(0.4)
!1
n.d.
n.d.
n.d.
n.d.
!1(1.3)
!1(1.3)
!1(1.1)
3(2.9)
10(16)
0.5(0.7)
3(3.4)
!0.5(1.3)
1(1.1)
!0.5(0.4)
!0.5(0.4)
n.d.
n.d.
n.d.
n.d.
24.5(32.7)
31(41.3)
13(14.9)
33(44)
34.5(46)
36(41.1)
36(32)
28(28)
M. S. R. Onsrud et al.
Survey
0.00
0.00
d
0.00
6.25
d
25.00
20.00
d
51.72
12.50
d
0.00
0.00
d
0.00
0.00
d
4.08(0.79)
2.79(1.40)
d
4.00(0.69)
5.00(0.00)
d
2.20(0.83)
1.50(0.70)
d
1.90(1.10)
5.13(4.64)
d
17.24
20.00
d
31.03
50.00
d
2.91(0.84)
3.43(0.89)
d
Herring
Nov 2000
March 2001
June 2001
2.29(0.46)
2.70(0.47)
d
15.25
0.00
d
22.73
0.00
d
32.20
47.61
d
31.82
25.00
d
0.00
0.00
d
0.00
0.00
d
3.72(0.84)
3.41(1.26)
d
3.45(1.00)
3.69(0.85)
d
1.54(0.71)
2.10(1.20)
d
1.54(0.78)
2.17(1.33)
d
44.07
47.62
d
59.09
75.00
d
3.27(1.42)
4.00(1.31)
d
Norway pout
Nov 2000
March 2001
June 2001
2.93(1.08)
3.62(0.86)
d
14.81
6.25
26.92
25.00
8.16
7.14
7.41
0.00
7.69
9.62
2.04
0.00
0.04
0.03
0.08
0.13
0.02
0.04
1.88(0.91)
2.77(1.09)
2.92(1.75)
2.89(0.91)
3.03(1.17)
3.32(1.25)
3.47(3.47)
5.92(11.39)
1.44(1.01)
1.82(0.98)
3.95(4.28)
2.17(2.33)
35.19
79.69
34.62
42.31
75.51
42.86
3.00(1.20)
3.25(0.97)
2.23(1.03)
2.67(1.37)
3.28(1.03)
3.08(1.21)
Whiting
Nov 2000
March 2001
June 2001
Night
Day
Night
Day
Night
Day
Night
Day
Night
Day
Night
Day
Night
Day
Empty
stomachs (%)
Stomachs with
copepod structures (%)
Stomachs with
fish structures (%)
State of digestion
of krill (s.d.)
Number of krill
stomachÿ1 (s.d.)
Stomach with
krill structures (%)
Stomach
fullness (s.d.)
Table 3. Stomach fullness, percentage stomachs with krill structures, number of krill per stomach and digestion status, percentage stomachs with fish structures, copepod remains and
percentage empty stomachs for whiting, Norway pout, and hearing in November 2002, March and June 2001.
Distribution and feeding of fish on krill
1287
stomachs with krill structures were similar, or higher by
day than by night, while the state of digestion for whiting
captured at night suggested that food had been eaten
recently.
While both herring and whiting apparently would be
most efficient predators in the upper part of the krill layer,
Norway pout were distributed deeper than the krill and thus
attacking from below. Norway pout has been established as
a benthopelagic species from many previous studies. It is
a common, and often dominant constituent in bottom trawls
from the Skagerrak and the North Sea (Hjort and Ruud,
1938; Raitt and Adams, 1965; Poulsen, 1968; Bergstad,
1990; Daan et al., 1990; Albert, 1994), and Larsen (1998)
obtained large catches of Norway pout in the bottom trawl
at the study site. However, the degree of bottom association
varies, and Kaartvedt et al. (1996) showed how Norway
pout left the benthic boundary zone when turbidity caused
the light attenuation to increase. Kaartvedt et al. (1996)
interpreted this situation as equivalent to ‘‘antipredator
windows’’ which may occur at dawn and dusk, when light
levels are sufficiently high to detect abundant plankton
prey, while being sufficiently low to give relative safety
with respect to visually foraging piscivores (Clark and
Levy, 1988). Also in their study, the pout was foraging in
the lower part of a krill layer.
Norway pout were part of the bottom-associated, dielly
migrating acoustic layer. Fish ascending from the bottom at
night, establishing a SL in midwater has been a recurrent
phenomenon through years of study at this site (Onsrud and
Kaartvedt, 1998; Kaartvedt et al., 2002). In November
2000, the source for the nocturnal layer lived pelagically
during day. We ascribe this to the particularly high light
extinction on this occasion (i.e. a similar phenomenon as
outlined by Kaartvedt et al., 1996). The 1% light depth was
then found as shallow as ca. 4 m, compared with 12e15 m
during the other sampling occasions. The high light
extinction was associated with record high run-off from
land, caused by extensive rainfall prior to the sampling
period.
We conclude that Norway pout were foraging on krill
during both day and night. No clear diel feeding pattern was
established from the stomach contents in our study. Albert
(1994) found predation of Norway pout on M. norvegica at
night, while Kaartvedt et al. (1996) documented foraging
on krill during daytime. However, the prey-detection
mechanism may have varied between day and night.
Whether visual or non-visual perception, or a combination
of both, is most important in locating the prey will depend
on both visual acuity and the sensitivity of the lateral-line
system of the species in question (Ryer et al., 2002).
Norway pout have particularly large eyes, presumably
enabling them to feed visually in relatively deep water
during day. Nevertheless, their deep night-time distribution
renders visual predation unlikely. The lateral-line morphology of Norway pout suggests that it may be a partially
tactile predator (John Janssen pers. comm.). The slowly
1288
M. S. R. Onsrud et al.
sinking SL would correspond to the description of nonvisual, ambush-feeding fish detecting their prey by using
the lateral-line system (Janssen et al., 1995; Janssen, 1997),
although cessation of feeding represents an alternative
explanation for this pattern. Several reports on midnight
sinking in other species have documented a subsequent
dawn rise during the morning ‘‘antipredation window’’
(Clark and Levy, 1988; Bagøien et al., 2001). Such a switch
to visual predation would represent one possible explanation of the rise of the lower edge of the midwater acoustic
layer in November 2000.
Aggregation behaviour
Fish aggregated beneath the research vessel in the course of
each acoustic study period, evidenced by a conspicuous
build-up in acoustic backscattering as recorded by the hullmounted transducers (Figure 2). A corresponding increase
was also observed from the bottom-mounted transducer in
November, when the upward-looking transducer was
located on the seabed in close proximity to the ship (Onsrud
et al., in preperation), but was not recorded in March and
June (the latter not shown), when the bottom-mounted
transducer was located ~80 m away from the ship. In March
we were able to compare the level of acoustic backscattering
just beneath and away from the ship, revealing a much
higher fish abundance under the ship (Figure 4).
On several occasions, all fish targets disappeared from the
ensonified volume, and then reappeared 10e20 min later.
This occurred simultaneously with the passing of commercial vessels 200e400 m away. Corresponding patterns have
been recorded during previous studies (Onsrud and
Kaartvedt, 1998; Kaartvedt et al., 2002). Ship-avoidance
behaviour by diving or horizontal swimming in response to
the pressure wave ahead of ships and the low frequent noise
generated from propellers have been repeatedly reported
(Olsen et al., 1983; Diner and Masse, 1987; Fréon and
Misund, 1998). There is concern how this may lead to
underestimation of fish abundance from a moving vessel.
This study, on the contrary, demonstrates how fish
abundance may be overestimated in ecological studies at
a fixed site. The particular mechanisms that account for this
aggregation is beyond the scope of this paper. The
aggregation behaviour is, however, of potential importance
in evaluating the interactions between the fish predators and
their krill prey. In our study, backscattering ascribed to krill
became more prominent at low fish abundance.
Krill distribution and antipredator behaviour
Krill was a main food item for whiting, Norway pout and
herring. The distribution of fish and krill seemed to be
governed by predatoreprey relationships, and not by
physical properties of the habitat, apart from the light
conditions which have a direct impact on predatoreprey
interactions involving visual predators. Temperature and
salinity below sill depth were fairly homogeneous, and
could not explain the variation in distribution by day, or
nocturnal distributions in the basin water. In the period with
lowest oxygen content of the basin water (November 2000;
oxygen saturation of 22.8%), both fish and krill were
abundant.
Krill were preyed on by planktivorous fish with different
vertical distribution and foraging tactics, and were exposed
to predators throughout the water column during both day
and night. Their diel vertical migration would provide
relative safety in the darkness of deep water, but their
pelagic predators were still active. Further descent might
have been unrewarding, bringing them into the realm of
large-eyed, deep-living predators (Norway pout). Furthermore, M. norvegica are themselves visual predators
(Torgersen, 2001b), using visual senses in locating deepliving prey (Kaartvedt et al., 2002) so their daytime
distribution may be a trade-off between predator avoidance
and searching for food.
Most focus on plankton antipredator behaviour has been
on diel vertical migration. The current study suggests
additional mechanisms. The ‘‘voids’’ in the krill recordings
in the proximity of deep fish assemblages (cf. Figure 3)
suggest that the krill performed instantaneous escape
reactions during day. It appeared that M. norvegica would
seek out water with reduced fish abundance at night (cf.
Figure 2). Earlier investigations have displayed avoidance
of the surface layer by the krill SL at the anchor station,
where fish recordings normally are abundant (Onsrud and
Kaartvedt, 1998; Kaartvedt et al., 2002). Artificial accumulation of fish under the ship at the anchor station could
enhance the surface avoidance behaviour.
Acknowledgements
This study was funded by the Research Council of Norway
(Project no. 133355/122). We greatly appreciate the
assistance given by Rita Amundsen and the RV ‘‘Trygve
Braarud’’ crew, and thank Espen Bagøien and two
anonymous referees for valuable comments on the draft
manuscript.
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