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doi:10.1006/jfbi.2001.1649, available online at http://www.idealibrary.com on
Seasonal variations in the energy density of ﬁshes in the
J. Prnr×srN*‡ :Nn J. R. G. Hisioi†
*Danish Institute for Fisheries Research, North Sea Centre, P.O. Box 101, DK-9850
Hirtshals, Denmark and †Fisheries Research Service, Marine Laboratory, Victoria Road,
Aberdeen, AB11 9DB, Scotland
(Received 30 September 2000, Accepted 2 May 2001)
The energy density (E
, kJ g
wet mass) of saithe Pollachius virens, haddock Melanogrammus
aegleﬁnus, whiting Merlangius merlangus, Norway pout Trisopterus esmarki, herring Clupea
harengus, sprat Sprattus sprattus, sandeel Ammodytes marinus and pearlsides Maurolicus
Muelleri, from the North Sea, increased with total length, L
. However, there was not always
a signiﬁcant (P>0·05) linear relationship between L
. Seasonal diﬀerences in E
obvious in mature ﬁsh, while geographical diﬀerences were insigniﬁcant. For all species there
was a highly signiﬁcant correlation (P<0·0001) between the percent dry mass of the ﬁsh (D
. A general relationship was established for gadoids and sandeel E
and herring E
. Thus seasonal and size-speciﬁc data on E
for bioenergetics and gastric evacuation models can be determined simply from D
, which is
considerably less costly and time consuming than calorimetry or proximate analysis.
2001 The Fisheries Society of the British Isles
Key words: ash content; energy density; dry mass; season; ﬁsh length.
The use of bioenergetics models in ﬁsheries science and ecology has increased
rapidly during the last 10–15 years (Brandt & Hartman, 1993) and there is
increasing interest in the use of models to study interactions between seabirds,
other top predators and ﬁshes (Hislop et al., 1991a). Often these models are
based on energy transfer between predator and prey. In such models seasonal
changes in energy density of predators and their prey are important variables.
Energy transfer is not used in methods such as multispecies virtual population
analysis (MSVPA), which has been used to assess some North Sea ﬁsh stocks
(Sparholt, 1990). Instead, food consumption is estimated by combining ﬁeld
data on a predator’s stomach content mass with experimental data on the
relationship between gastric evacuation rate and stomach content (Bajkov, 1935;
Elliott & Persson, 1978; Pennington, 1985). There is uncertainty which is the
best model to describe gastric evacuation (Hislop et al., 1991b) although
exponential models are generally used. However, Andersen (1998, 1999) has
shown that gastric evacuation of gadoids can be described independently of meal
size by a square root model and that in whiting Merlangius merlangus (L.) prey
size has no eﬀect on the rate of gastric evacuation. The gastric evacuation rate
‡Author to whom correspondence should be addressed. Tel.: +45 33 96 32 00; fax: +45 33 96 32 60;
0022–1112/01/080380+10 $35.00/0 2001 The Fisheries Society of the British Isles
in whiting fed natural prey is, however, aﬀected by the energy density of the prey
items (Andersen, 1999). Using Andersen’s (1999) model, Pedersen (2000) found
that the speciﬁc daily rations of whiting were signiﬁcantly diﬀerent between years
and groups of whiting, depending on the energy density of their stomach
contents. Thus seasonal energy density data are also required for the application
of the gastric evacuation model. However, information on the energy density of
predator and their prey suitable for use in bioenergetics models is sparse.
Although many data are available (Cummins & Wuycheck, 1971; Harris &
Hislop, 1978; Hartman & Brandt, 1995) they can be misleading, because they do
not take into account that there are changes in energy density of ﬁshes both with
ontogeny (Craig, 1977) and season (Kelso, 1973; Foltz & Norden, 1977; Hislop
et al., 1991a). Therefore, if results obtained from models using energy data are
to be accurate, determinations of energy density of predator and prey are
required for seasons and ﬁsh size or age.
The present study is an attempt to expand former studies and to determine by
seasons and ﬁsh size the energy density of eight species for which there are
quantiﬁed predator-prey interactions in the North Sea.
MATERIALS AND METHODS
For determination of energy density, ungutted specimens of the piscivorous species
saithe Pollachius virens (L.), whiting, haddock Melanogrammus aegleﬁnus (L.), and their
main ﬁsh prey, herring Clupea harengus L., sprat Sprattus sprattus (L.), Norway pout
Trisopterus esmarki (Nilsson), sandeel Ammodytes marinus (Raitt) and pearlsides
Maurolicus muelleri (Gmelin), were collected by research and commercial vessels in the
northern and central North Sea during the period 1996–1998. The ﬁshes were collected
quarterly, Q1=January, February or March; Q2=April, May or June; Q3=July, August
or September; Q4=October, November or December. At sea, the ﬁshes were sorted into
length classes (total length, L
), whose boundaries varied with species and L
Each ﬁsh or batch of ﬁsh in the case of small individuals was wrapped in a polythene bag,
to minimize water loss, and stored in a domestic freezer at 20 C. To minimize
desiccation the ﬁshes were processed within 6 months after capture. However, ﬁshes
showing evidence of desiccation were not used.
All the saithe, whiting, herring, sprat, Norway pout and pearlsides were processed at
the Danish Institute for Fisheries Research (DIFRES), North Sea Centre, Hirtshals,
Denmark. Prior to determination of energy density the samples were warmed at room
temperature to a partially thawed state, which prevented loss of water and blood from the
ﬁshes. The ﬁshes were roughly chopped and homogenized. Fishes >20 cm L
homogenized in a Tecator Mill 1094 homogenizer for 4 min and subsequently in a Bu¨ chi
Mixer B-400 for 15 s, while smaller specimens were processed ﬁrst in a domestic food
blender and then in the Bu¨ chi mixer. Loss of water during processing was insigniﬁcant
for all size classs. Maximum loss (0·5% wet mass) was observed when ﬁshes >20 cm L
were chopped. For all size classes masses derived in this manner were therefore assumed
to be reliable and not inﬂuence by loss of water.
Two samples of the homogenate weighing c. 20 g each were oven-dried to constant
mass at 60 C (48 h) for the determination of dry mass (W
) content and afterwards
heated for 48 h at 600 C for determination of the ash mass. Two other samples were
oven-dried and two 1·0–1·3 g W
subsamples were combusted to measure energy density
with an IKA-Calorimeter C 7000. If the subsamples diﬀered by >1·5%, the variation was
above the precision of the calorimeter and a third subsample was combusted. The
average of the two to three subsamples was used for estimates of energy density for
The haddock and sandeel samples were processed at the Marine Laboratory,
Aberdeen, Scotland. Homogenates were prepared using procedures similar to those
rNr×cx nrNsi1x or risnrs 381
T:nir I. Energy density (kJ g
) of the common ﬁsh species in the North Sea by size
and quarter (sample size in parentheses). Bold and underlined ﬁgures are from Hislop
et al. (1991a) and Harris & Hislop (1978). Medio and ultimo refer to ﬁsh caught between
1–5 February and after 21 March, respectively
1 (medio) 1 (ultimo) 2 3 4
Saithe 200–249 4·1 (4)
Saithe 250–299 4·7 (6)
Saithe 300–349 4·7 (10)
Saithe 350–399 4·2 (20) 4·5 (20) 4·8 (20) 4·9 (20)
Saithe 400–449 4·6 (20) 4·4 (18) 5·1 (20) 4·8 (20)
Saithe 450–499 5·0 (19) 4·0 (20) 5·3 (20) 4·8 (20)
Saithe 500–599 5·5 (9) 4·0 (9) 5·6 (10) 5·2 (10)
Saithe 600–699 5·3 (10) 3·5 (9) 6·8 (10) 6·2 (5)
Saithe 700–799 5·0 (7) 4·8 (8) 6·0 (10)
Saithe 800–999 5·3 (10) 6·3 (10) 6·2 (2)
Saithe 1000–11 999 5·3 (2) 6·0 (4)
Haddock 100–119 3·9 (20)
Haddock 120–149 3·6 (21) 3·3 (10) 4·2 (10) 3·6 (10)
Haddock 150–199 3·7 (22) 3·9 (10) 4·1 (10) 4·1 (30)
Haddock 200–249 4·3 (14) 4·3 (10) 4·2 (10) 4·9 (14)
Haddock 250–299 4·7 (11) 4·0 (10) 4·6 (18) 4·9 (12)
Haddock 300–349 4·7 (14) 4·5 (25) 5·0 (10) 5·2 (23)
Haddock 350–399 4·7 (14) 3·6 (5) 5·5 (11) 5·5 (18)
Haddock 400–449 4·5 (11) 3·8 (7) 4·9 (11) 5·1 (11)
Haddock 450–499 4·4 (5) 5·3 (2) 5·3 (2)
Haddock 500–549 4·7 (1) 5·6 (5) 5·3 (1)
Haddock 550–599 3·6 (1)
Herring 40–49 4·1 (14)
Herring 50–59 4·2 (35)
Herring 60–79 3·9 (39)
Herring 80–99 4·6 4·5 (20) 4·6
Herring 100–119 4·7 (20) 4·6 (2) 4·4 (5) 4·6
Herring 120–149 4·4 (21) 4·5 (50) 5·2 (20) 6·3 (23)
Herring 150–199 4·4 (20) 4·4 (50) 10·1 (20) 7·1 (20)
Herring 200–249 6·5 (20) 5·7 (41) 11·0 (20) 8·5 (12)
Herring 250–299 8·5 4·9 (20) 11·9 (20) 8·8 (20)
Sprat 43–93 6·7 (2)
Sprat 104–137 10·9 (3)
Sprat 115–125 11·5 (20)
Sprat 110–119 6·4 (6)
Sprat 120–129 5·8 (10)
Sprat 130–139 5·9 (10)
Sprat 140–149 5·6 (6)
Pearlsides 45–72 7·3 (50)
Norway pout 40–49 3·8 (50) 3·9 (20)
Norway pout 50–59 3·8 (50) 3·9 (20)
Norway pout 60–79 3·9 (20)
Norway pout 80–99 4·5 (1) 4·8 (50)
Norway pout 100–119 6·2 (43) 4·0 (20) 4·2 (20) 5·7 (18) 5·2 (20)
Norway pout 120–149 6·4 (14) 4·1 (20) 4·4 (20) 6·3 (20) 7·0 (20)
Norway pout 150–199 4·7 (35) 4·0 (20) 5·7 (20) 7·0 (20)
382 ¡. irnr×srN :Nn ¡. ×. c. nisioi
employed at DIFRES. However, although most ﬁshes >20 cm were processed individ-
ually smaller specimens had to be processed in batches (pooled samples) because the
blender was unable to homogenize small quantities of tissue. One or more samples of the
homogenate, most weighing exactly 40 g, were taken for the determination of W
energy density E
. Dry mass was determined by weighing the homogenate before and
after freeze-drying for 72 h in a HETO CD8 freeze dryer. Because the W
of the other
species had been determined by oven-drying, the two drying techniques were compared
using replicate samples of homogenate from 20 haddock. No signiﬁcant or consistent
diﬀerence was observed between the W
of the freeze-dried and oven-dried samples.
After their W
had been determined, the freeze-dried samples were stored at 20 C for
periods ranging from weeks to months before their E
were determined by bomb
calorimetry. To eliminate any water that may have been absorbed during storage the
samples were oven-dried for several hours at 60 C before calorimetry was undertaken.
Spot checks indicated that W
were consistent and corresponded to those measured
immediately after freeze-drying.
The calorimetry of haddock and sandeel was carried out at DIFRES and Rowett
Research Institute (RRI), Aberdeen, Scotland, using an IKA C700 calorimeter and a
Gallenkamp adiabatic bomb calorimeter, respectively. Under normal circumstances two
samples per ﬁsh or per batch were used. However, if the E
, of the two samples diﬀered
by >5%, which is the precision of the Gallenkamp calorimeter, an additional samples was
processed. Also, replicate samples were used to determine (a) whether freeze dried
samples had the same E
, irrespective of where they were analysed (i.e. DIFRES or RRI)
and (b) whether freeze dried and oven-dried samples of the same ﬁsh returned similar E
In neither case were signiﬁcant diﬀerences detected.
For all eight species E
were initially expressed as kJ g
and were subsequently
converted to wet mass (W
) by multiplying by (1((W
In general, the energy density (E
, kJ g
) increased with increasing L
and varied between quarters (Table I). These seasonal diﬀerences were obvious
after the ﬁsh had attained maturity. Norway pout and herring showed particu-
larly pronounced diﬀerences in E
before and after spawning (note the E
T:nir I. Continued
1 (medio) 1 (ultimo) 2 3 4
Whiting 50–59 4·0 (40) 3·8 (4)
Whiting 60–79 4·0 (40) 3·7 (80)
Whiting 80–99 4·0 (2) 3·6 (40) 3·9 (50)
Whiting 100–119 4·1 (20) 3·8 (11) 3·8 (23) 3·8 (20)
Whiting 120–149 4·0 (20) 3·8 (46) 3·9 (21) 3·9 (20)
Whiting 150–199 4·3 (20) 3·9 (50) 4·7 (20) 4·2 (12)
Whiting 200–249 4·8 (20) 4·0 (35) 5·3 (10) 5·4 (3)
Whiting 250–299 5·0 (20) 4·3 (13) 5·4 (20) 5·1 (3)
Sandeel 60–69 4·0 3·7 (300)
Sandeel 70–79 4·6
Sandeel 80–99 4·4 4·2 (240)
Sandeel 100–119 5·4 5·6 (80)
Sandeel 120–149 5·8 6·2 (80)
Sandeel 150–199 6·1
rNr×cx nrNsi1x or risnrs 383
Norway pout sampled early and late in Q1, i.e. pre-spawning and post-
spawning). The E
of haddock did not diﬀer signiﬁcantly between geographical
areas, although in nearly every case the western values were higher than the
eastern ones (Table II).
Least-squared regression models were calculated by quarter (Q) with E
dependent variable and L
(mid-point of each sampled length class) as the
independent variable. The relationships for saithe were: Q1, E
=0·59, P>0·05); Q2, E
=0·23, P>0·05); Q3,
=0·70, P<0·05); Q4, E
=0·65, P=0·05). For haddock they were: Q1, E
=0·24, P>0·05); Q2, E
=0·03, P>0·05); Q3,
=0·84, P<0·05); Q4, E
=0·64, P>0·05). For saithe, signiﬁcant relationships were found in Q3 and Q4,
whereas haddock show signiﬁcant relationships in Q3 only. For whiting,
Norway pout, herring and sandeel none of the quarterly linear relationships was
For all species, least-squared regression models were generated for each
quarter with E
as the dependent variable and the percent dry mass proportion
)] as the independent variable. For saithe (Fig. 1) and the
other species the relationships were similar in all quarters. Therefore, for each
species the quarterly data were pooled and highly signiﬁcantly correlations
and energy density were established (Table III). Slopes of the
regression lines were not signiﬁcantly diﬀerent between gadoids and sandeel
(Table III). However, there were signiﬁcant diﬀerences between gadoids and
herring. Furthermore, the ash content did not change with ﬁsh size although the
average ash content was signiﬁcantly higher for gadoids than for herring, sprat
and pearlsides (Fig. 2). Therefore, the gadoid and sandeel data were combined
and a general relationship calculated between D
for gadoids and
=0·908, P<0·0001). For herring:
=0·999, P<0·0001) (Fig. 3). Slopes of the
two relationships were signiﬁcantly diﬀerent (t=9·0475, d.f.=19, P<0·001). This
was also the case using data within the common range of dry mass fractions only
(t=3·2722, d.f.=17, P<0·001). The corresponding relationships between percent
water content (C
) and E
P<0·0001) for gadoids and sandeel and E
=0·998, P<0·0001) for herring (Fig. 4).
T:nir II. Energy density (kJ g
) of haddock caught in east and west North Sea by
size and quarter (sample size in parentheses)
East West East West
120–149 3·5 (20) 3·6 (10)
150–199 3·9 (20) 3·9 (10) 3·7 (20) 4·1 (30)
200–249 3·9 (20) 3·4 (10) 3·9 (11) 4·9 (14)
250–299 3·8 (20) 4·0 (10) 4·4 (20) 4·9 (12)
384 ¡. irnr×srN :Nn ¡. ×. c. nisioi
The energy density of all species varied considerably with size and season.
Norway pout and herring showed particularly pronounced diﬀerences in energy
density between size and quarter (Table I). This is in accordance with Hislop
et al. (1991a) who found that the energy density of a ﬁsh depends not only on its
size but also on season. The seasonal variations in energy density are generally
associated with the reproductive and feeding cycles of the ﬁsh and tend to be
greater amongst the larger, mature members of the population (Hislop et al.,
1991a). Pronounced seasonal cycles are shown for cod Gadus morhua L.
(Schwalme & Chouinard, 1999) and strong seasonal cycles in energy density are
typical for clupeoids (Hunter & Leong, 1981; Flath & Diana, 1985; F. Arrhenius
& S. Hansson, pers. comm.). Large changes in energy density of Norway pout
can occur over a relatively short time period, i.e. a few months (Table I), and in
14 16 18 20 22 24 26 28
Fic. 1. Relationship between percent dry mass (D
) and energy density. (E
) for saithe in Q1 (),
Q2 (), Q3 () and Q4 ().
T:nir III. Least-squared regression models for estimating energy density (kJ g
from percent dry mass proportion (D
n Slope 95% CL Intercept 95% CL P
Saithe 0·939 33 0·305 0·028 2·205 0·666 <0·0001
Haddock 0·926 197 0·352 0·014 3·363 0·325 <0·0001
Whiting 0·955 18 0·375 0·041 3·666 0·850 <0·0001
Norway pout 0·982 17 0·401 0·028 4·355 0·665 <0·0001
Herring 0·999 20 0·417 0·007 4·640 0·189 <0·0001
Sprat 0·974 3 0·354 0·129 2·996 3·253 <0·02
Sandeel 0·957 19 0·351 0·036 2·897 0·840 <0·0001
rNr×cx nrNsi1x or risnrs 385
sandeels (Hislop et al., 1991a). Further, energy density of European perch Perca
ﬂuviatilis L. and yellow perch Perca ﬂavescens Mitchill diﬀers signiﬁcantly
among months (Craig, 1977; Henderson et al., 2000).
Fic. 2. Mean ash content (%) (95% CL) of eight North Sea ﬁsh species. (Sandeel data from N. G.
15 20 25 30 35 40
Fic. 3. Relationships between percent dry mass (D
) and energy density (E
) for gadoids and sandeel ()
and herring (). Regression lines (——) and 95% CL (– – –) are indicated.
386 ¡. irnr×srN :Nn ¡. ×. c. nisioi
Seasonal changes in energy density are not related only to the reproduction
cycle; they can also be related to seasonal changes in food consumption and diet.
Foltz & Norden (1977) found that smelt Osmerus mordax (L.) undergo a period
of energy storage prior to overwintering and spawning. Smelt apparently utilize
stored energy during the winter as evidenced by low feeding levels and losses
from the gut and carcass, which parallel gonad growth. In yellow perch decline
in energy density could be explained by the reduction in food consumption and
allocation of energy to gonad development (Henderson et al., 2000). During
both overwintering and spawning food consumption may be reduced or cease,
and ﬁshes must rely in part on stored energy reserves to survive both events.
Immediately after spawning energy reserves are commonly at a minimum and the
ﬁrst priority is to replenish energy reserves (Winkle et al., 1997). Knowledge of
the seasonal dynamics in energy density is therefore important when energy
transfer is quantiﬁed in predator-prey interactions.
Energy densities >10 kJ g
were measured for sprat and herring
>15 cm, whereas relatively low valeus (<6 kJ g
) were measured for
gadoids and sandeel. As bone has a relatively low energy content, species with
more bony parts would have a lower energy density per gram dry mass (Hartman
& Brandt, 1995). This is in accordance with the low ash content of herring
compared to gadoids (Fig. 3). As sprat rarely grow >15 cm they reach sexual
maturity, and hence have high levels of energy density, at a much smaller length
than herring (Hislop et al., 1991a). However, in the North Sea there are three
main stocks of herring that spawn at diﬀerent times and locations (Hulme, 1995).
Further, the North Sea Skagerrak area comprises both immature autumn
Water content (%)
55 60 65 70 75 80
Fic. 4. Relationships between water content (%) and energy density (E
) for gadoids and sandeel () and
herring (). Regression lines (——) and 95% CL (– – –) are indicated.
rNr×cx nrNsi1x or risnrs 387
spawners from the North Sea and mature spring spawners from the Baltic and
Skagerrak-Kattegat (Moksness & Fossum, 1991). Therefore, seasonal and
geographical ﬂuctuations in energy density are likely to be complex even though
the geographical diﬀerences in energy density of haddock were insigniﬁcant.
Fluctuations in energy density due to for instance spawning and migration,
imply that good geographical coverage and seasonal and size-speciﬁc energy
densities are needed to quantify predator-prey interactions because the precision
of not only the bioenergetics models but also the gastric evacuation method for
estimating food consumption relies on appropriate data on prey energy density.
Fish size was not a good predictor of energy density due to the overwhelming
inﬂuence of season. However, species-speciﬁc relationships between the percent
dry mass proportion of the ﬁsh and energy density appear adequate for
prediction of energy density of ﬁsh (Table III). Nevertheless, the present study
shows that there were insigniﬁcant diﬀerences between seasons (Fig. 1). The
insigniﬁcant diﬀerences between species in the intercepts and slopes of these
relationships indicate generalized models can be established for genus or family.
This is inconsistent with Hartman & Brandt (1995) who found that there are
species-speciﬁc diﬀerences in the energy density relationship. However, despite
these apparent species-speciﬁc diﬀerences, they used a general model for describ-
ing seasonal changes in energy content of ﬁshes. This model is very similar to the
general relationship established for gadoids and sandeel in the present study.
However, the present herring model diﬀers signiﬁcantly from the clupeidae
model established by Hartman & Brandt (1995). This could be due to the fact
that their work is mainly based on freshwater species. Nevertheless, both the
general model and the herring model are adequate for prediction of energy
density of ﬁshes. Therefore, data on energy density required for bioenergetics
and gastric evacuation models, can be obtained simply from the percent dry mass
proportion of ﬁsh sampled on appropriate time scales for all species and sizes
considered. This is a time saving procedure in comparison with calorimetry or
proximate analysis of each species and size class.
We thank D. Frandsen, M. Bell and W. MacDonald for help with bomb calorimetry.
We also thank N. G. Andersen and J. Riis-Vestergaard for rewarding discussions, and
two anonynous referees for valuable comments on the manuscript. B. Bøhle
co-ordinated collecting some of the saithe from Norwegian research vessels. The study
was supported ﬁnancially by EU FAIR project CT-95-0604 (CORMA).
Andersen, N. G. (1998). The eﬀect of meal size on gastric evacuation in whiting. Journal
of Fish Biology 52, 743–755. doi:10.1006/jfbi.1997.0617.
Andersen, N. G. (1999). The eﬀects of predator size, temperature, and prey character-
istics on gastric evacuation in whiting. Journal of Fish Biology 54, 287–301.
Bajkov, A. D. (1935). How to estimate the daily food consumption of ﬁsh under natural
conditions. Transactions of the American Fisheries Society 65, 288–289.
Brandt, S. B. & Hartman, K. J. (1993). Innovative approaches with bioenergetics
models: further applications to ﬁsh ecology and management. Transactions of the
American Fisheries Society 122, 731–735.
388 ¡. irnr×srN :Nn ¡. ×. c. nisioi
Craig, J. F. (1977). The body composition of adult perch, Perca ﬂuviatilis in Winder-
mere, with reference to seasonal changes and reproduction. Journal of Animal
Ecology 46, 617–632.
Cummins, K. W. & Wuycheck, J. C. (1971). Caloric equivalents for investigations in
ecological energetics. Miteilungen International Vereinigung fur Theoretische und
Angewandte Limnologie 18, 1–158.
Elliott, J. M. & Persson, L. (1978). The estimation of daily rates of food consumption for
ﬁsh. Journal of Animal Ecology 47, 977–991.
Flath, L. E. & Diana, J. S. (1985). Seasonal energy dynamics of the alewife in
southeastern Lake Michigan. Transactions of the American Fisheries Society 114,
Foltz, J. W. & Norden, C. R. (1977). Seasonal changes in food consumption and energy
content of smelt (Osmerus mordax) in Lake Michigan. Transactions of the
American Fisheries Society 106, 230–234.
Harris, M. P. & Hislop, J. R. G. (1978). The food of young Puﬃns Fratercula arctica.
Journal of Zoology, London 185, 213–236.
Hartman, K. J. & Brandt, S. B. (1995). Estimating energy density of ﬁsh. Transactions
of the American Fisheries Society 124, 347–355.
Henderson, B. A., Trivedi, T. & Collins, N. (2000). Annual cycle of energy allocation to
growth and reproduction of yellow perch. Journal of Fish Biology 57, 122–133.
Hislop, J. R. G., Harris, M. P. & Smith, J. G. M. (1991a). Variations in the caloriﬁc
value and total energy content of the lesser sandeel (Ammodytes marinus) and
other ﬁsh preyed on by seabirds. Journal of Zoology, London 224, 501–517.
Hislop, J. R. G., Robb, A. P., Bell, M. A. & Armstrong, D. W. (1991b). The diet and
food consumption of whiting (Merlangius merlangus) in the North Sea. ICES
Journal of Marine Science 48, 139–156.
Hulme, T. J. (1995). The use of vertebral counts to discriminate between North Sea
herring stocks. ICES Journal of Marine Science 52, 775–779.
Hunter, J. R. & Leong, R. (1981). The spawning energetics of female northern anchovy,
Engraulis mordax. Fishery Bulletin 79, 215–230.
Kelso, J. R. M. (1973). Seasonal energy changes in walleye and their diet in West Blue
Lake, Manitoba. Transactions of the American Fisheries Society 102, 363–368.
Moksness, E. & Fossum, P. (1991). Distinguishing spring- and autumn-spawned herring
larvae (Clupea harengus L.) by otolith microstructure. ICES Journal of Marine
Science 48, 61–66.
Pedersen, J. (2000). Food consumption and daily feeding periodicity: comparison
between pelagic and demersal whiting in the North Sea. Journal of Fish Biology
57, 402–416. doi:10.1006/jfbi.2000.1316.
Pennington, M. (1985). Estimating the average food consumption by ﬁsh in the ﬁeld
from stomach contents data. Dana 5, 81–86.
Schwalme, K. & Chouinard, G. A. (1999). Seasonal dynamics in feeding, organ weights,
and reproductive maturation of Atlantic cod (Gadus morhua) in the southern Gulf
of St Lawrence. ICES Journal of Marine Science 56, 303–319. doi:10.1006/
Sparholt, H. (1990). An estimate of the total biomass of ﬁsh in the North Sea. Journal
du Conseil International pour L’Exploration de la Mer 46, 200–210.
Winkle, W. V., Shuter, B. J., Holcomb, B. D., Jager, H. I., Tyler, J. A. & Whitaker, S. Y.
(1997). Regulation of energy acquisition and allocation to respiration, growth and
reproduction: simulation model and example using rainbow trout. In Early Life
History and Recruitment in Fish Populations (Chambers, R. C. & Trippel, E. A.,
eds), pp. 103–137. London: Chapman & Hall.
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