ICES Journal of Marine Science, 62: 1463e1474 (2005)
doi:10.1016/j.icesjms.2005.08.003
The effect of abiotic and biotic factors on the importance
of macroplankton in the diet of Northeast Arctic cod
in recent years
E. L. Orlova, A. V. Dolgov, G. B. Rudneva,
and V. N. Nesterova
Orlova, E. L., Dolgov, A. V., Rudneva, G. B., and Nesterova, V. N. 2005. The effect of abiotic and biotic factors on the importance of macroplankton in the diet of Northeast Arctic
cod in recent years. e ICES Journal of Marine Science, 62: 1463e1474.
Using cod feeding data, this paper considers the distribution and abundance of macroplankton from different ecological groups (euphausiids and hyperiids) and the variability in their
consumption by cod over a period of years during which different water mass temperatures
were observed. These years were also characterized by variable abundance of capelin, cod’s
main food source. Differences in intensity and duration of cod consumption of euphausiids
and hyperiids species are shown, depending on their abundance, temperature conditions,
cod distribution, and the supply of capelin for cod. This paper discusses the energetics of
consuming different types of prey and the role euphausiids play in the energy balance of
cod. The low fat content of cod is sometimes associated with feeding on postspawning euphausiids in summer and autumn.
Ó 2005 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.
Keywords: Barents Sea, cod, euphausiids, feeding, hyperiids.
Received 1 July 2004; accepted 4 August 2005.
E. L. Orlova, A. V. Dolgov, G. B. Rudneva, and V. N. Nesterova: Polar Research Institute of
Marine Fisheries and Oceanography (PINRO), 6 Knipovich Street, 183763 Murmansk,
Russia. Correspondence to E. L. Orlova: tel: C7 8152 473424; fax: C7 1 78910518;
e-mail: [email protected].
Introduction
Common macroplankton (euphausiids and hyperiids) are
very important elements in the diet of the Barents Sea
cod (Gadus morhua L.). There are, however, significant differences in cod consumption depending on area, year, and
season (Zatsepin and Petrova, 1939; Berger, 1968; Ponomarenko and Yaragina, 1990; Dolgov, 1999; Orlova
et al., 2003). The main factors affecting cod consumption
of euphausiids and hyperiids are their abundance, distribution pattern, accessibility to cod, and the availability of capelin Mallotus villosus, the primary food of cod. Capelin as
well as other fish and animals have a similarly dramatic effect on macroplankton abundance. The most heavily consumed are euphausiids, but predation varies depending on
their availability, which is related to the season and size.
Postspawning euphausiids are eaten primarily by demersal
fish (cod and haddock) (Zatsepin and Petrova, 1939; Kovtsova et al., 1989), but euphausiid spawning stock and recruitment are overwhelmingly affected by capelin and
young individuals of various fish species (Drobysheva
1054-3139/$30.00
and Yaragina, 1990), herring (Manteifel, 1941), and polar
cod Boreogadus saida (Panasenko, 1978). Intense hyperiid
consumption (predominantly of the large Arctic species
Themisto libellula) was observed mostly in periods when
they fed on copepods in the water column, as well as during
the prewintering formation of concentrations in bottom
layers. The main consumers of this species are polar cod
(Panasenko, 1990), Sebastes marinus and Sebastes mentella
(Boldovsky, 1944; Antonov et al., 1989; Dolgov and Drevetnyak, 1993), and cod (Dolgov, 2000). Marine mammals
(harp seals and minke whales) feed mostly on prespawning
and spawning concentrations of euphausiids and hyperiids
at a depth down to 200 m (Folkow et al., 2000; Nilssen
et al., 2000). The other important factor determining fluctuations in euphausiid and hyperiid abundance is water
temperature, since their communities are formed from
species of different zoogeographical groups and ecology
(Drobysheva, 1979; Dalpadado, 2002).
Consumption of euphausiids has been studied intensively.
In warm years, cod mainly feed on the abundant boreal
species Thysanoessa inermis, whose largest concentrations
Ó 2005 International Council for the Exploration of the Sea. Published by Elsevier Ltd. All rights reserved.
1464
E. L. Orlova et al.
occur on shallow banks in the western, central, and northwestern parts of the Barents Sea. In cold years, when the
cold-water species T. raschii is predominant, euphausiid
concentrations grow in the eastern areas, where cod
consume them more intensively.
The switch to predation on euphausiids usually coincides
with the conclusion of winter and spring feeding on capelin.
Availability of euphausiid concentrations during this period
is an important factor in the annual cycle of cod foraging.
Migrating cod find high concentrations of euphausiids during their spawning and settlement to bottom layers. In the
southern Barents Sea, cod start feeding on euphausiids during MayeJune (western areas) and JulyeAugust (central
areas); during cold and warm years, feeding periods differ
by approximately one month (Zatsepin and Petrova,
1939). In the northwest Barents Sea (the Bear Island-Spitsbergen area), after the winter period, cod start to feed
actively on euphausiids that form prespawning concentrations (Berger, 1968): in years with normal temperature,
this occurs in MayeApril, and during cold years extends
to July. In this area, cod prey on postspawning and prewintering concentrations of euphausiids between JuneeAugust
and NovembereDecember (Orlova et al., 2003).
From 1950 to the 1980s, considerable variation in euphausiid abundance and changes to their role in the feeding
of cod were observed. During this time, the effect of biotic
and abiotic factors often overlapped. A sharp reduction in
euphausiid stocks in the early 1950s (warm period) caused
starvation of cod during three summer seasons in 1950,
1951, and 1952 (Grinkevich, 1957). The reduction was related to an increase in the abundance of capelin and cod, the
main consumers of euphausiids, as well as the birth of an
abundant herring year class in 1950 (Shutova-Korzh,
1960). During the 1960e1970s, a cold period that saw an
abrupt reduction in herring abundance and a concurrent increase in capelin abundance, year-to-year and seasonal occurrence of euphausiids in the diets of cod and capelin
showed opposite trends (Ponomarenko and Yaragina,
1990). At the end of the cold period, stabilization of the
T. raschii stock was observed in the eastern part of the
sea (Drobysheva, 1988). Euphausiids were consumed by
cod at low levels because of the westerly cod distribution
during 1979e1982 and active predation on capelin in those
areas (Yaragina, 1984). Since food supply to cod in the period of reduced euphausiid abundance was high, they did
not migrate for long distances.
This period gave way to one of even sharper fluctuations
in the abundance of euphausiids (1980e1990s), concurrent
with variability in Barents Sea water temperature (Bochkov
and Tereshchenko, 1992) and variability in the abundance
of the main consumers of plankton. For instance, the total
stock of capelin during 1980e1990 varied from 0.86 million tonnes (1986) to 7.0 million tonnes (1990) (Ushakov,
2000). The main reasons behind this fluctuation were periodic fishing for capelin and their intensive consumption by
predators of all trophic levels. For example, cod alone
consumed between 1.5e2.8 and 0.9e3.4 million tonnes in
1990e1992, according to different estimates (Bogstad and
Mehl, 1992; Dolgov, 2002), during a period when abundance grew steadily. During this period, the ratio of capelin
and cod abundance in the Barents Sea changed abruptly
(ICES, 2004a, b). For each cod (conventional index of supply with the main food), there were 1500e2700 capelin individuals during 1978e1983, no more than 200e300
capelin individuals during 1985e2000, and only 14 capelin
in 1995 (Orlova and Dolgov, 2004). During the study period, redistribution of cod stocks between the main feeding
areas, i.e. the southern part of the sea (usual feeding area)
and the Bear Island-Spitsbergen area (northwestern part
of the sea), was observed, associated to a large extent
with changes in the food supply.
Likewise, consumption of hyperiids by cod is worthy of
our attention. In mixed concentrations of hyperiids in the
Barents Sea, the abundant species Themisto abyssorum
and T. libellula are predominant, but it is recognized
(Vinogradov et al., 1982; Dalpadado et al., 2001) that the
first of the above species dwells mostly in the Atlantic
Waters, while the second inhabits Arctic Waters. Specifically, more dense concentrations of hyperiids, especially
of the large Arctic species T. libellula, are formed in areas
occupied by Arctic Waters in the north and northeast of the
Barents Sea. In this connection, concentrations of feeding
cod (boreal species) and hyperiid concentrations coincide
in the limited area (in the east to 45e47(E), thereby decreasing spatial accessibility of hyperiids to cod. Thus, in
contrast to euphausiids, the distribution pattern of hyperiids
from different origins affects their consumption by cod to
a greater extent. In addition, hyperiids spend much time
in the water column feeding on Calanus, which also influences their accessibility to cod. The frequency of hyperiids
in cod diet usually increases in autumn when they form prespawning concentrations in the near-bottom layers, which,
depending on temperature, can be extended in time. Likewise, in spring, depending on the time that hyperiids ascend
into the water column, the duration of hyperiid consumption is also variable, i.e. in warm years they are consumed
until April, while in cold years until MayeJuly (Orlova
et al., 2004).
Along with these factors, year-to-year fluctuations in the
consumption of hyperiids, similar to those of euphausiids,
are related to their abundance, as well as to the availability
to cod of its main food (capelin). So, in some cold periods
during the 1950e1960s with low capelin availability, cod
fed on hyperiids fairly regularly in the western and central
fishing areas (Berger, 1968), with the highest frequencies
occurring in the northwest area of the sea. Because of
high consumption of capelin by cod (Shleinik, 1996) during
the 1970s to early 1980s, the role of hyperiids was minor.
An increase in their consumption was observed in the
mid-1980s, and this grew with a reduction of capelin abundance (Bogstad and Mehl, 1992; Dolgov, 1995), reaching
its maximum during 1986e1987 for the period of the
Effect of abiotic and biotic factors on the importance of macroplankton in the diet of cod
dramatic decline in the capelin stock. Therefore, most researchers associate the increase in hyperiid abundance
with a decrease in capelin predation, although in our
view, a more likely reason behind the sharp rise in abundance of hyperiids is because they occupied a food niche
that became available when the capelin stock was reduced
(Kashkin and Kashkina, 1996).
Over a long period of time (1984e1999), consumption of
hyperiids by cod in the Barents Sea was mostly opposite to
that of capelin (Dolgov, 2000). When the percentage of
capelin in the annual diet of cod was less than 10e20%
by weight, the proportion of hyperiids increased greatly, attaining the maximum of 16.9e23.7% in the period
1986e1989. During 2000e2004, the level of capelin consumption by cod was quite high (22.8e45.5%), while hyperiids constituted just 0.4e3.9%. The interrelationship
between consumption of these two food items is most
prominent in the Bear Island-Spitsbergen area where cod
consumption of hyperiids is more stable.
The purpose of the present paper is to evaluate the importance of euphausiids and hyperiids in the cod diet during
the last 20 years (1984e2003), including year-to-year, seasonal, local, and age-related variation in their consumption
by cod in years with different water temperature.
Material and methods
In this paper, quantitative data on cod feeding, from the
joint RussianeNorwegian database of stomach contents of
marine organisms in the Barents Sea (more than 193 000
stomachs), were used. Details of sampling, analysis, and
storage are provided by Mehl and Yaragina (1992). In addition, quantitative data on cod feeding were used (more than
12 000 stomachs). These data included information on the
index of stomach fullness from 0 (empty stomach) to 4
(full stomach) and occurrence of each prey species.
Euphausiids and hyperiids were identified to species during analysis of quantitative data, but when analysing qualitative data, they were identified only to family. To show
the importance of hyperiids and euphausiids in the cod
diet, the percentage weight %w (stated as a percentage of
the food bolus weight) and frequency of occurrence %fo
(stated as a percentage of the number of feeding fish)
were applied. The intensity of cod feeding was evaluated,
based on total and partial fullness index (W).
Data from annual surveys of macroplankton organisms
conducted in the Barents Sea (Figure 1) during autumne
winter by the near-trawl net in the bottom layer (6e10 m
from the bottom) were also used. In the quantitative assessment, the index of abundance was calculated as the arithmetic mean of catches expressed in individuals 1000 mÿ3.
When analysing the role of Themisto spp. in the feeding
of cod, information for 1984e2000 was used (Orlova et al.,
1989; Dolgov, 2000; Orlova et al., 2003), supplemented
with data for 2001e2002.
1465
Results
As in previous periods, great fluctuations in the abundance
of macroplankton were observed in the period under study
(Figure 2). Fluctuations were largely related to the abundance of capelin, their main consumer. Variations in abundance of euphausiids, as a result of capelin predation,
reflected those reported for the southern part of the sea (Orlova et al., 2000). Abundance of these crustaceans at the
end of the year was 1.9 times higher than the long-term
mean when the capelin stock was low (1986e1988,
1994e1996); 1.4 times higher than the long-term mean at
a high level of the capelin stock (1985, 1989, 1993, 1997,
and 1998); and 3 times lower when the capelin stock was
at its maximum level (1990e1992). The above trend was
maintained in recent years under a new reduction in the
capelin stock (ICES, 2004b). In the northwest, the trend revealed itself to a lesser extent.
The dynamics of euphausiid and hyperiid consumption
by cod was the opposite of cod consumption of capelin, although the amount of euphausiids and hyperiids consumed
in most cases was not the same as that of capelin. Unusual
features of their consumption by cod are illustrated by using
examples of different years, distinguished by different temperature, the time of cod changing to high levels of feeding
on euphausiids and hyperiids, and the length of the feeding
season.
Euphausiids
Cold years
In the southern Barents Sea, 1987, 1997, and 1998 were
cold years. Cod on the wintering grounds fed on euphausiids to a limited extent, and their percentage in the cod
diet during the first quarter did not exceed 0.1e0.3% by
weight (Table 1). In 1987, there were high survival rates
of euphausiids due to low abundance of capelin, and the
mean density of their concentrations varied from 1900 individuals 1000 mÿ3 (central and eastern parts of the sea) to
3000 individuals 1000 mÿ3 (coastal areas of Murmansk).
Low cod predation on euphausiids was associated with prolonged feeding by cod on redfish during over-wintering in
the Bear Island-Spitsbergen area. The change to feeding
on euphausiids in summer occurred late. Only during the
shift of the main cod concentrations to the Murmansk
Bank (70e72(N 35e37.5(E) and coastal areas of Murmansk (JuneeAugust), where concentrations of euphausiids were high, were high levels of cod consumption
observed (with 60e90% frequency of occurrence). The
same level of cod predation on euphausiids was maintained
during the eastward cod migration. Maximum predation in
1987 fell in the third quarter when cod fed on euphausiids
(mostly on T. raschii) at the eastern margin of the feeding
area (Table 1). However, on the whole, the partial index
of cod stomach fullness by euphausiids was not high
(Figure 3).
1466
E. L. Orlova et al.
80°
44
79°
78°
43
37
29
41
77°
30
35
39
76°
31
75°
34
32
74°
38
36
33
40
17
73°
18
42
21
72°
19
16
15
4a
22
9
23
71°
8
24
26 25
11
70°
10
20a
4c
3B
10a 6B
12 13
69°
4B
5
20B
2B
6a
7
1B
1a
1
2a
27
14
14
28
68°
5°
10°
15°
20°
25°
30°
35°
40°
45°
50°
55°
60°
65°
70°
Figure 1. Chart of the Barents Sea fishing areas. 1-The Vaigach area; 1a-the Pechora area; 1b-the Kolguev area; 2a-the Kanin-Kolguev
Shallows; 2b-the Northern slope of the Kanin-Kolguev Shallows; 3a-the Kanin Bank; 3b-the North Kanin Bank; 20b-the Southern part of
the Novaya Zemlya Shallows; 4a-the Goose Bank Northern slope; 4b-the Goose Bank Western slope; 4c-the Goose Bank Southern slope;
5-the North-Central area; 6a-the West-Central area; 6b-the Murmansk Shallows Northern slope; 7-the Murmansk Shallows; 18-the Central
Deep; 19-the Northern part of the Novaya Zemlya Shallows; 20a-the Goose Land Shallows; 8-the Murmansk Bank North-Western slope;
9-the Finnmarken Bank; 10a-the Murmansk Bank North-Western slope; 10-the Murmansk Bank South-Western slope; 15-the Murmansk
Tongue; 16-the Central Plateau; 17-the Demidov Bank; 21-the Nordkin Bank; 22-the Norwegian Deep; 11-the Rybachya Bank; 12-the
Kildin Bank; 13-the West Coastal area; 14-the East Coastal area; 23-the Søre Bank; 24-the Fugløy Bank; 25-the Malangen Bank; 26the Andøy Bank; 27-the Vesterálen; 28-the Røst Bank; 29-the West Spitsbergen; 30-the South Cape Deep; 31-the Spitsbergen Bank;
32-the Bear Island Bank Western slope; 33-the Bear Island Bank Southern slope; 34-the Bear Island Bank Eastern slope; 35-the Hopen
Island area; 36-the Western Deep; 37-the Persey Elevation; 38-the Central Elevation; 42-the Kopytov area; 39-the Novaya Zemlya Shallows; 40-the Sukhoy Nos area; 41-the Admiralty Islands area.
In 1997, euphausiids were relatively scarce and evenly
distributed in different parts of the sea. Beginning in April,
they became highly important to the cod diet, primarily in
the coastal areas of Norway and Murmansk (frequency of
occurrence was 35e75% and 30e60%, respectively). Feeding on euphausiids was even more pronounced in JuneeAugust when cod reached the Murmansk Bank
slopes, where euphausiid concentrations were very high
(1e5 individuals mÿ3). Euphausiids served both as the
main prey for cod (frequency of occurrence 70e80%)
and as additional food for capelin. Euphausiids appeared
to keep the abundance of both predators stable. In JulyeAugust, the area of intensive cod feeding on euphausiids shifted to the central part of the sea. With
euphausiids dominating the cod diet, the index of stomach
fullness reached a magnitude of 2e3, and 75e100% of the
cod were observed to have fed. In August, intensive feeding
on euphausiids continued in the eastern part of the sea as
well, but in September their importance there decreased
sharply, and they occurred only as additional food. The partial index of stomach fullness attributable to euphausiids in
1997 was slightly higher than in 1987 (Figure 3); the main
consumption of euphausiids occurred in the second and
third quarters (Table 1).
In 1998, the level of euphausiid consumption by cod was
fairly close to that of 1997, but seasonal differences were
observed. As early as May, in the majority of the western
areas, there were almost no euphausiids in the cod diet. Exceptionally, the frequency of occurrence of euphausiids was
made up 43e73% to the north of the Norwegian coast
(Nordkyn Bank, Norwegian Deep), but in the coastal areas
of Norway, they were scarce in the cod diet. In coastal
Murmansk, region-intensive consumption of euphausiids
was observed to begin in June, but in the western areas including the Murmansk Bank, their role in this period was
less important (Figure 3). In these areas, despite a later
change to feeding on euphausiids, the frequency of occurrence in JulyeAugust was as high as in the central areas
of the sea where local feeding continued in September
(Figure 4). A small proportion of cod reaching some of
the eastern areas fed on euphausiids as late as October
and December.
Effect of abiotic and biotic factors on the importance of macroplankton in the diet of cod
1467
1400
Southern areas
Northwest areas
1000
800
1
Concentration, individuals 1000-3
1200
600
400
200
2
2003
2001
1999
1997
1995
1993
1991
1989
1987
1985
1983
0
Year
Figure 2. Mean indices of concentrations of euphausiids (1) and hyperiids (2) in the Barents Sea during the period 1983e2003.
In the northwestern Barents Sea, the periods 1986e1988
and 1996e1998 were cold. The specific characteristics of
euphausiid consumption were determined by water temperature and depended on the availability of capelin for cod. In
the first period (1986e1987), the higher abundance of euphausiids compared with the long-term mean notwithstanding, their importance in the cod diet was very low (Figure 2),
becoming significant in only a few seasons (Table 1). Since
the amount of material on feeding was not large, it was not
possible to characterize comprehensively any peculiarities
of their consumption by cod during these years. However,
it can be assumed that the reason behind the low consumption could be a departure from the usual cod migration pattern owing to a shortage of capelin, and under cold
conditions, the coincidence of cod and euphausiid concentrations was of short duration. It was most pronounced in
1987, when in the northernmost wintering areas of cod, cold
waters prevailed, favouring the retention of the cod there.
In the later period, consumption of euphausiids was more
intensive and consistent through time, although some distinctions by season were noted. In 1996, despite lowered
water temperature in the Barents Sea, heat advection to
the northwestern areas with the Norwegian Current was
higher than normal, contributing to active migration of
cod to this area in June. Migrating and wintering cod fed
on euphausiids from April through July (50e89% by frequency of occurrence), which by weight accounted for
24% and 7.4% in the second and third quarters, respectively
(Table 1). However, on the whole, their proportion in the
cod diet remained low (Figure 3). In 1997, against the background of lower temperatures in the northwest, steady
consumption of euphausiids began in the same period, but
occurred over a larger area and was more prolonged (until
November). At the same time, the frequency of euphausiid
occurrence in the cod stomachs varied greatly. In 1998, because of negative water temperature anomalies in the Murmansk and central branches of the North Cape Current, the
feeding migration of cod began approximately one month
later. The start of feeding on euphausiids in the west was
also protracted (AprileJune) and accompanied by wide variations in euphausiid proportion in the cod diet; on the whole
their importance as food for cod was not great (Figure 3).
Warm years
In the southern part of the sea during warm years
(1990e1992, 1995, 1999, and 2000), consumption of euphausiids was at a minimal level. The low level of consumption was mainly associated with a high capelin stock
and low abundance of euphausiids (Figure 2). A small exception occurred during 1995 and 1999 (Figure 2), when
a slight increase in the proportion of euphausiids in the
cod diet in the second or third quarter was observed (Table
1). In 1995, this was largely caused by steady consumption
of euphausiids during MayeJune in the coastal areas of
Murmansk (50e90% frequency of occurrence) where, by
this period, the majority of euphausiids had spawned, and
their availability was high. It is important to note that, in
contrast to previous months when up to 40e80% of cod
had empty stomachs owing to a low capelin stock, in the
period of increased feeding on euphausiids, such individuals made up no more than 15e25%, and the index of cod
1468
Table 1. Proportion of the main food items in cod diet by quarter in the Bear Island-Spitsbergen area in 1984e2002 expressed as % of the food bolus weight.
Percentage of food bolus weight
1984
1985
1986
1987
1988
1989
1990
1991
1992
1993
1994
1995
1996
1997
1998
1999
2000
2001
2002
Capelin
I
II
III
IV
d
d
6.1
d
d
0.6
20.8
11.1
1.5
0.0
8.3
11.8
6.7
5.1
2.7
2.4
1.2
15.8
14.7
0.0
24.3
50.8
9.1
42.4
5.8
20.9
45.6
92.6
36.6
68.8
62.4
72.1
42.5
7.8
36.7
17.3
12.9
0.0
6.1
0.2
7.6
d
4.0
5.1
9.4
1.5
0.6
2.1
7.1
0.1
8.5
16.5
14.4
1.5
38.0
10.9
13.3
17.3
32.1
7.9
3.5
59.7
81.1
24.1
9.1
39.0
22.4
3.2
6.8
20.6
25.7
14.2
5.6
2.7
47.5
20.6
Shrimp
I
II
III
IV
d
d
23.2
d
d
68.8
4.6
45.0
5.2
3.6
6.4
6.3
9.3
25.5
4.5
5.5
10.3
22.7
0.6
4.9
19.4
35.9
6.0
4.6
35.9
35.7
4.9
0.4
9.3
4.4
4.6
3.6
22.6
35.0
14.3
8.8
17.8
36.6
17.0
42.3
15.1
d
8.8
2.9
11.9
51.2
5.1
0.5
5.9
6.7
21.0
5.3
19.7
3.4
10.2
16.5
31.1
19.7
3.3
19.2
30.4
6.3
2.6
9.1
3.0
3.2
12.1
8.1
25.9
8.7
5.9
5.0
17.8
3.6
2.8
4.4
Euphausiids
I
II
III
IV
d
d
1.0
d
d
0.5
0.1
1.1
0.0
45.9
0.5
0.0
0.0
0.0
1.3
1.9
1.0
4.4
4.3
0.9
0.7
0.4
1.4
2.5
0.2
0.5
0.2
0.2
0.0
0.7
0.8
0.2
0.0
5.0
0.3
0.0
0.0
0.3
0.3
0.2
0.1
d
1.7
0.2
0.2
0.5
8.0
0.2
0.6
23.6
7.4
0.5
0.2
6.6
8.6
0.6
0.3
5.4
5.4
1.3
0.3
12.0
1.2
1.6
1.1
12.4
2.6
1.3
0.3
13.2
0.7
0.9
1.8
6.5
2.4
1.2
Hyperiids
I
II
III
IV
d
d
1.7
d
d
0.0
28.4
24.4
0.0
1.2
28.4
49.3
0.0
0.0
35.2
39.7
0.2
2.0
4.1
3.8
0.2
0.1
27.5
1.5
0.2
0.1
1.5
0.5
0.6
0.3
1.1
0.5
0.0
0.1
0.3
0.0
0.0
0.1
6.1
0.2
0.1
d
2.4
44.8
0.1
0.0
12.9
2.0
0.8
4.3
10.7
60.8
0.0
4.6
3.5
3.6
2.7
0.8
28.0
6.8
0.0
0.8
2.9
4.4
2.4
2.2
18.1
11.5
0.5
0.7
4.8
1.7
0.1
0.8
0.8
1.1
Cod
I
II
III
IV
d
d
1.6
d
d
0.0
2.1
0.0
0.0
0.0
2.6
0.0
18.5
0.4
0.1
4.2
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
0.0
2.4
0.1
0.0
9.1
0.0
0.1
3.8
0.0
14.7
1.0
0.0
25.8
0.0
1.7
0.0
1.3
d
6.5
8.2
7.3
3.1
9.5
42.3
51.6
24.7
20.6
3.9
8.4
42.6
22.2
30.2
17.3
33.2
1.1
17.9
30.4
6.3
3.4
7.2
22.6
12.8
2.8
3.2
15.2
13.9
6.3
18.6
17.1
8.8
1.4
5.8
E. L. Orlova et al.
Quarter
Effect of abiotic and biotic factors on the importance of macroplankton in the diet of cod
400
Southern Barents Sea
70
350
60
300
50
250
40
200
hyperiids
30
150
euphausiids
20
100
mean index of fullness
2004
2002
2000
1998
1996
1994
1992
0
1990
0
1988
50
1986
10
1984
Total index of fullness
Partial index of fullness
80
1469
350
70
300
60
0
2004
0
2002
50
2000
10
1998
100
1996
20
1994
150
1992
30
1990
200
1988
40
1986
250
1984
50
Total index of fullness
Partial index of fullness
Bear Island-Spitsbergen area
Figure 3. Proportion of hyperiids and euphausiids (partial index of stomach fullness, W) and total index of stomach fullness (W) of cod
in the southern Barents Sea and Bear Island-Spitsbergen area (northwestern area).
stomach fullness did not exceed 1.5e2. In 1999, euphausiids were predominantly consumed during June (western
areas), JulyeAugust (western and coastal areas), and September (central areas).
In the northwest of the sea, 1990e1995 and 1999e2000
were warm years. The level of cod predation on euphausiids
was fairly low and close to that in the southern part of the
sea. The partial index of stomach fullness by euphausiids
in 1999, even at a low total index of stomach fullness
(250.9W), constituted only 6.8W (Figure 3). Levels of euphausiid consumption in the south and north of the Barents
Sea were not concurrent and not always dependent on the
abundance of winter concentrations of euphausiids; instead,
they were sometimes dependent on the availability of other,
more preferred food. This was confirmed by the situation in
the three years that showed different abundances of
euphausiids (the highest abundances in 1995 and 2000, the
lowest in 1999). The most pronounced example was feeding
of cod in 1995, when the capelin supply was very low and
cod fed predominantly on shrimp. In April, shrimp constituted 65e90% by frequency of occurrence, while cod did not
consume euphausiids at all. The picture remained the
same in June and July, but in those cases when there were
few shrimp in the diet, cod changed to feeding on euphausiids. Only in August did euphausiids occupy a dominant
position (from 25% to 85%). On some occasions, consumption of euphausiids was high in September, as well as in October and November. In 2000, when there was an increased
proportion of capelin in the cod diet, and euphausiids (even
at high population abundance) quite often took second place
in terms of frequency of occurrence. In this case, cod exploited two peaks of euphausiid abundance, in AprileMay
1470
a
E. L. Orlova et al.
(prespawning concentrations) and in JulyeAugust (postspawning concentrations). The situation was repeated also
at lower abundance of euphausiids during 1999, and as
was the case during 2000, cod diet was dominated by four
species: capelin, shrimp, euphausiids, and hyperiids,
substituting for one another.
80
78
76
74
72
70
68
b
16
20
24
28
32
36
40
44
48
16
20
24
28
32
36
40
44
48
16
20
24
28
32
36
40
44
80
78
76
74
72
70
68
c
80
78
76
74
72
70
68
d
48
80
Normal years
During normal years (1984e1986, 1988, 1993e1994, and
1996 for the southern part of the sea and 1984e1985 for
the northwest) the nature of euphausiid consumption by
cod reflected the effects of factors observed in other years
and described above. Therefore, in 1984e1986, availability
of capelin had the largest effect on the level of euphausiid
consumption. Capelin were scarce mostly in the southern
part of the sea, which led to cod feeding more intensively
on euphausiids (Figure 3). In some cases, euphausiids
were the main food of small cod (20e40 cm) in summer
(Orlova et al., 1996). In 1988, the most important factors
were probably a lack of capelin and high abundance of euphausiids; mean density of euphausiids was almost three
times higher than the long-term mean (Figure 2), reaching
700e1000 individuals 1000 mÿ3 in local concentrations in
the west. That year, consumption of euphausiids began as
early as JanuaryeFebruary; the highest frequency of occurrence (30e35%) was in the coastal areas of Norway and adjacent waters. At the same time, feeding of cod was not
stable, and the proportion of feeding individuals ranged
widely (20e80%). The partial index of stomach fullness
by euphausiids accounted for more than 10% of the total index. However, it is worth noting that high rates of euphausiid consumption were probably one of the reasons for the
low intensity of cod feeding. The other prominent increase
in euphausiid consumption (Figure 3) was related to a new
reduction in capelin abundance in the second half of the
1990s and a corresponding rise in abundance of euphausiids
(Figure 2).
78
76
Hyperiids
74
72
70
68
16
20
24
28
32
36
40
44
48
1 to 10
11 to 20
21 to 40
41 to 60
61 to 100
Figure 4. Frequency of occurrence of euphausiids (% of number of
fish) in cod stomachs in June (a), July (b), August (c), and September (d) 1998.
An increase in hyperiid consumption by cod in the northwest was observed as early as 1985 (Figure 3). The most
intensive consumption was by relatively small cod
(20e40 cm and 40e60 cm) in August (Table 2), when
young cold-water Themisto libellula (13e15 mm) were
mainly consumed. In the other areas, a 10-mm warm-water
T. abyssorum also occurred from time to time.
In 1986e1987, both warm-water T. abyssorum and coldwater T. libellula played a significant role in cod feeding in
the southwestern and coastal areas (JulyeAugust), constituting 60e90% by frequency of occurrence. In addition,
the increased importance of T. libellula in the central, eastern, and northwestern areas of the sea in SeptembereOctober 1987 was noted (Orlova et al., 1989). In western areas,
T. abyssorum (immature individuals of 10 mm size) mostly
Effect of abiotic and biotic factors on the importance of macroplankton in the diet of cod
1471
Table 2. Percentage of Themisto in the diet of cod of different size in 1985e1988 (before slash e T. abyssorum, after slash e T. libellula).
20e40 cm
Month
1985
March
April
November
August
August
August
1986
January
February
August
August
1987
September
October
November
March
August
September
September
November
October
1988
January
August
August
41e60 cm
% Frequency
of occurrence
% by
weight
Mean
length
(mm)
% Frequency
of occurrence
0/10
d
d
0/29
0/64
0/100
0/2
d
d
0/6
0/8
0/47
d/10
d
d
d/15
d/10
d/20
33/33
18/3
70/14
0/24
0.1/0.4
0.1/0.1
49/2
0/5
Eastern areas
d
60/40
25/d
d
0/40
0/25
d
d
0/67
Western areas
Central areas
Murmansk coast
0/6
9/5
0/14
Area
Western areas
Northwest areas
Central areas
Murmansk coast
Western areas
Northwest areas
Western areas
Northwest areas
Central areas
61e80 cm
% by
weight
Mean
length
(mm)
% Frequency
of occurrence
% by
weight
Mean
length
(mm)
0/10
0/5
0/36
0/61
0/57
0/13
0/2
0/0.1
0/0.1
0/34
0/2
0/6
d/15
d/14
d/15
d/13
d/11
d/10
0/50
d
0/50
0/22
d
d
0/1
d
0/0.1
0/0.3
d
d
d/10
d
d/11
d/10
d
d
10/13
11/21
12/10
d/5
10/20
10/1
32/17
0/28
0/0.1
0/0.1
32/2
0/8
11/13
12/12
15/10
d/10
21/16
7/2
d
d
0/0
0/0
d
d
11/13
11/10
d
d
d
4/88
3/d
d
0/94
0/91
d
d
0/48
d
10/30
10/d
d
d/20
d/20
d
d
d/30
0/45
58/61
20/31
0/9
0/55
0/42
d
12/6
0/70
0/32
3/83
4/35
0/0.3
0/53
0/44
d
0.3/0.2
0/52
d/21
10/30
10/28
d10
d/19
d/21
d
10/16
d/28
0/13
33/56
29/29
0/23
0/71
d
0/25
0/3
0/50
0/38
1/74
0/33
0/0.1
0/22
d
0/13
0/0.1
0/39
d/24
10/28
10/30
d/14
d/17
d
d/25
d/15
d/30
0/19
6/1
0/1
d/35
10/20
d/18
0/5
25/24
23/d
0/1
3/10
4/d
d/31
10/17
11/d
d
6/33
50/d
d
0.1/10
2/d
d
10/20
10/d
Dash means no data.
occurred in the cod diet in OctobereNovember, while T. libellula (mature individuals of 21e24 mm to 28e30 mm)
were predominant in SeptembereNovember. In the northwestern and eastern areas, cod fed solely on T. libellula
(17e21 mm long in AugusteSeptember and 28e30 mm
in October), which dominated the diet of fish 20e40 cm
and 40e60 cm long (Table 2). Large-scale consumption
of T. libellula by cod in that year is also worth noting, given
the great importance of hyperiids in some areas in the
northeast and southeast of the sea (the highest was up to
65e80% by weight). In 1988, the main consumption of hyperiids by cod was observed in the western and central
areas of the southern sea. In the west during January, cod
fed on prespawning concentrations of T. libellula of
3.1e3.5 mm long, while in the central areas (during August) they preyed on mixed concentrations of T. libellula
of 10e20 mm long (Table 2). In years of the highest hyperiid abundance, total consumption by cod (Figure 2), when
the main food item was T. libellula, indicated the great
role hyperiids play in cod feeding during the third and
fourth quarters, both in the southern sea and Bear IslandSpitsbergen area, except for the recent warm years (Table
1). It should be noted that, in years of maximum consumption of hyperiids, the partial index of stomach fullness was
quite high (42e63W) and accounted for up to 29% of the
total index (Figure 3).
An increase in the level of hyperiid consumption in the
northwest of the sea was also observed in some other years,
when their abundance was not high, including normal
(1994), warm (1995), and cold (1996) years. A common feature of these years was low availability of capelin for cod.
In 1994, cod remained in the western part of the feeding
area until August, where they fed on various prey, although
at this time, up to 65% of individuals had empty stomachs.
Only in SeptembereNovember with the shift of the main
concentrations to the Hope Island area (75.5e77.5(N
1472
E. L. Orlova et al.
25e31(E), did cod change to feeding on hyperiids and, as
a result, stabilized their feeding. Almost all individuals
fed; their index of fullness reached 2e2.5. In this period,
the percentage of hyperiids by weight made up nearly
45% of the cod food in the fourth quarter (Table 1).
In 1995, concentrations of hyperiids were lower than in
1987 (Figure 2). Cod fed on hyperiids and euphausiids at
the same time. Hyperiid importance increased gradually
with the decrease in the proportion of euphausiids and the
cod feeding migration to areas where cold Arctic Waters
prevailed. Within the large concentrations of hyperiids in
the Hope Island area, hyperiids were of primary importance
in the cod diet (95% by frequency of occurrence in September, 45% in October, and 85% in November) as well as in
the sparse concentrations on the Great Perseus Bank
(76e79(N 30e47(E) in September (85%). During November, some cod remained in these areas continuing to
feed actively. The proportion of hyperiids in the cod diet
in the third and fourth quarters was estimated at about
15% by weight (Table 1).
In 1996, as in previous years, consumption of hyperiids
by cod was observed during their migration to the central
area of the feeding ground in AugusteSeptember. In these
months, hyperiids dominated cod diet (90e100%) on the
Central Bank (74e76(N 31e34(E), but the most intensive
feeding on hyperiids was recorded on the Great Perseus
Bank in OctobereNovember, during which up to 95% of
cod fed, and their index of fullness exceeded 2. In the
fourth quarter, hyperiids accounted for more than 60% of
cod prey by weight (Table 1).
Discussion
Analysis indicated that, as in the past, there were great differences in cod consumption of macroplankton crustaceans
(euphausiids and hyperiids) during the period 1984e2004,
giving rise to different perceptions of their role in the annual
rhythm of cod feeding. As before, the main factor influencing the total level of consumption of the crustaceans by cod
was availability of capelin, an observation supported by
many researchers (Bogstad and Mehl, 1997; Bogstad and
Gjosæter, 2001). Regarding euphausiids, the effect of this
factor showed itself in two ways: (i) the level of predation
by prespawning capelin, which reduced the remaining
abundance of euphausiids in the period of cod summer
feeding, and (ii) the availability of capelin, the main cod
food. For hyperiids, the relationship is more intricate, as
low abundance of capelin could be the cause of a sharp
increase in the abundance of predatory species (T. libellula)
as a result of their occupying an empty food niche
(Calanus), particularly in cold years. Under wide fluctuations in capelin abundance, there was a pronounced inverse
relationship between consumption of capelin and euphausiids by cod (Ponomarenko and Yaragina, 1990), and also
between consumption of capelin and hyperiids by cod
(Dolgov, 2000; Dalpadado, 2002). At the same time, our
data showing higher proportions of euphausiids and
hyperiids in the diet of younger, smaller cod conform quite
well with data from the other researchers, both in the
Barents Sea (Dalpadado and Bogstad, 2004) and in the
waters of Iceland, where euphausiids are an important component of the diet of 10e40-cm cod (Asthorsson and
Pálsson, 1987).
When evaluating the role of macroplankton organisms in
cod feeding, the season is of great importance. The dynamics of lipid production and mobilization during the process
of their reproduction is strongly related to season. As illustrated by the example of northern krill Meganyctiphanes
norvegica, the content of lipids in large prespawning individuals can be 1.5e2 times higher than that in postspawning ones (Albessard and Mayzaud, 2003). Thus, depending
on the level of euphausiid consumption in different seasons
(wintering, prespawning, and postspawning concentrations), cod consume different amounts of calories, which
in turn affect their fatness. The fatness index depends particularly on how much capelin, which has a particularly
high caloric index, is eaten (Makarova, 1968). In addition,
availability of capelin determines a certain type of cod
feeding (Orlova et al., 2000, 2003). In view of this, the lowest fatness of cod throughout the whole feeding season is
observed in years of low consumption of capelin and increased importance of euphausiids and hyperiids in their
diet. Yaragina et al. (2003) found that the energy potential
of cod (i.e. total energy content of lipids in the liver of mature females in spawning year), which represents an integrated index of feeding conditions in the current year, is
determined by weight percentage of capelin in the cod
diet. At the same time, a significant negative relationship
was revealed between energy potential of cod and weight
percentage of hyperiids and, to a lesser extent, of euphausiids. The latter observation is probably related to the fact
that cod not only consume high levels of postspawning euphausiids in summer, but also (in MarcheApril and OctobereDecember) feed on prespawning and prewintering
concentrations of the crustaceans in both warm and cold
years.
Acknowledgements
We thank two anonymous reviewers for their constructive
comments on the draft manuscript. We also acknowledge
the help of Nick Bailey (FRS, Aberdeen) and Andrew
Payne (Cefas, Lowestoft) in improving the English
language and for valuable suggestions on the draft paper.
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