Additive budgeting of metabolic

costs in larval coregonids

Juha Karjalainen 1, Olli Ylönen 1 and Hannu Huuskonen 2

1 University of Jyväskylä, Department of Biological and Environmental Sciences, P.O.Box 35,

FIN-40351 Jyväskylä, Finland
E-mail: juhakar@cc.jyu.fi, olliylo@cc.jyu.fi
2 University of Joensuu, Karelian Institute, Department of Ecology, P.O.Box 111, FIN-80101 Joensuu, Finland
E-mail: hannu.huuskonen@joensuu.fi

Key words: energy allocation, larval whitefish, additive budgeting, costs of digestion, costs of activity

Abstract
Commonly used bioenergetics models of fish assume that the energy budget is additive, that is,
each component of the budget has its own allocation and at least the basal level of this specific ca-
pacity cannot be used for other purposes. However, it has been proposed that rapidly growing fish
larvae with a narrow metabolic scope may have to reduce the energy allocated to activity or main-
tenance in order to maintain high growth rates. This has been called previously compensatory
budgeting. In the present study, we addressed this important issue by conducting swimming
respirometer experiments and reanalysing previous feeding respirometer data using larval white-
fish. In the swimming respirometer, the total metabolic rate of unfed larvae was lower than the
total rate of fed larvae, in which the total rate increased with increasing ration. The swimming
respirometer experiments suggested that the costs of digestion and activity have their own basal
requirements and are at least to some extent independent. The reanalysis of the feeding respirom-
eter data showed that up to a specific growth rate of about 16% day-1 no suppression of mainte-
nance functions is needed to achieve high growth rates. These results together suggest that the
energy budget of larval whitefish is indeed additive, and that this assumption is therefore justified
as a theoretical base in modelling larval coregonid energetics.

Introduction
In fish energetics, interaction between activity and digestion is important because both compo-
nents influence greatly the growth rate and survival of fish (Blaikie and Kerr 1996). Traditionally,
the energy budgeting of fish is assumed to be additive (Winberg 1956) and this assumption un-
derpins commonly applied bioenergetics models (e.g. Kitchell et al. 1977; Karjalainen et al. 1997).

The Big Fish Bang. Proceedings of the 26th Annual Larval Fish Conference. 2003. Edited by Howard I. Browman and Anne Berit Skiftesvik
Published by the Institute of Marine Research, Postboks 1870 Nordnes, N-5817, Bergen, Norway. ISBN 82-7461-059-8
14 THE BIG FISH BANG

Additive budgeting assumes that each component has its own scope and that at least the basal level
of this specific capacity cannot be used for other purposes. This means also that to some extent
costs of digestion and activity must be independent. Blaikie and Kerr (1996) observed that differ-
ent organ systems (muscle vs. gastrointestine) of adult cod (Gadus morhua) may have independent
maximum metabolic capacities which can operate without interference. They argued that the
digestive system has its own blood circulation and capacity to transport gases, and that muscles for
swimming are a similarly independent system, and that the respiratory system can deliver enough
gas even when both systems work at their highest rate. Although this may not be true in juvenile and
adult fish of many species under variable feeding conditions (Farrell et al. 2001; Hunt von Herbing
and White 2002), the oxygen supply to tissues of larval fish is suggested to be limited by the mito-
chondrial capacity of each tissue rather than by the capacity of the respiratory system (Wieser 1995).
An alternative allocation model, the compensatory (Rombough 1994) budgeting, assumes that
the total aerobic capacity is divided between different functions by priority rules and that mainte-
nance is usually found to have a higher priority than growth and reproduction (Wieser 1994).
Priede (1985) proposed that the costs of digestion and swimming activity are mutually exclusive;
so that if a fish is swimming at its maximum speed, it cannot digest food simultaneously. This may
be especially inevitable under unfavourable conditions where the metabolic scope is not sufficient
to cover all metabolic activities running simultaneously. Thus, the metabolic budgeting may be ad-
ditive under favourable conditions, but compensatory under adverse conditions. Another implica-
tion of compensatory budgeting could be in the energy allocation of larval fish (Wieser and
Medgyesy 1990a, b; Rombough 1994; Wieser 1994, 1995): if fish larvae consume food and grow at
a very high rate (as they can) they must reduce the energy allocated to activity or maintenance
since growth has the highest priority. Positively phototactic larvae of many fish species, however,
perform continuous swimming behaviour and the priority of activity must also be high.
This critical allocation issue was examined in this study by carrying out a series of swimming
respirometer experiments and reanalysing the feeding respirometry data of Wieser and Medgyesy
(1990b) and Huuskonen et al. (1998). In the swimming experiments, the effect of meal size on
energy allocation of larval whitefish (Coregonus lavaretus L.) at near-maximum expenditures was
studied. The feeding respirometry experiments allowed us to estimate the magnitude of digestion
costs in whitefish larvae in relation to their growth rate.

Materials and Methods

Swimming respirometry. The eggs of whitefish were obtained from the hatchery of the Finnish
Game and Fisheries Institute in Laukaa where they were incubated over winter in glass jars. Three
weeks before hatching the eggs were transported to the hatchery of University of Jyväskylä and
water temperature was slowly increased from 2°C to 6-8°C which induced the start of the hatching.
Newly-hatched whitefish larvae were reared at 12°C in 45 dm3 glass aquaria and fed Artemia
nauplii. The larvae were given nauplii by an automatic feeding system once every hour during the
light period (from 0730 to 2330). The flow-through aquaria were cleaned twice a day by siphoning
faeces and food particles from the bottom.
 ADDITIVE A L L O C AT I O N O F M E TA B O L I C C O S T S 15

Figure 1. The maximum sustained swimming time

(mean±se) of unfed larval whitefish (total length
19-20 mm) swimming against a current at variable
speed (cm s-1 and body length s-1) in the swimming
respirometer at 12°C. The dotted line indicates the
swimming speed used in the 7 min swimming
respirometer experiments.

Oxygen consumption was measured in two

intermittent-flow respirometers (Forstner 1983;
Forstner et al. 1983) equipped with polaro-
graphic oxygen sensors (POS, YSI 5750). Each respirometer system included three parallel acrylic
swimming chambers (length 20 cm, diameter 1 cm). The oxygen consumption of each chamber
was recorded for 7 minutes and the average rate during this period extrapolated to an hourly value.
The oxygen electrode chamber and the fish chambers were flushed after each measurement with
fully aerated water. Bacterial oxygen consumption in the respirometers was measured at the begin-
ning and at the end of each experiment and was subtracted from the total decline of oxygen. Water
temperature and changes in air pressure during the measuring period were also taken into account
for the calculations (according to Forstner and Gnaiger 1983).
The allocation of energy costs of active larval whitefish was examined in three separate swim-
ming respirometer experiments. In the swimming respirometer, fish were forced to swim against a
current at 12 or 14°C for 7 minutes in order to reach their maximum aerobic performance and,
thus, metabolic rates. The duration of the exercise and the water current were adjusted according
to preliminary swimming tests with unfed larvae (Fig. 1).
In all experiments, half of the fish were fed for 2-3 hours on Artemia nauplii before the
respirometry while the rest of the larvae remained without food for 18-20 hours before the oxygen
consumption measurements. During the feeding period, both treatments were replicated (four
aquaria per treatment) and the oxygen consumption of 6-24 schools (5 larvae per school) ran-
domly sampled from the aquaria was measured in the respirometer. In experiments 1 and 2, fish
were fed in excess and in experiment 3, high (100% of fresh mass of fish) and low ±10% of FM)
rations were offered. High ration corresponded to the ad libitum feeding in experiments 1 and 2.
The fresh mass and total length of the larvae varied from 25-55 mg and 19-25 mm, respectively.
During the measurement period, each school of 5 fish swam against a current (4-6 cm s-1) and
the peak rates (total metabolic rate, RT) of the fed and unfed fish were recorded. In experiments 1
and 2, the same school of fish was placed into the chamber and measured three times, but because
there was no difference between three sequential measurements, in experiment 3 only one mea-
surement was carried out with each school. Experiment 1 was carried out in 2001 and experiment
2 in 2002. The costs of digestion (RSDA = the post-prandial rise in the metabolic rate, SDA as in
Jobling 1983) was calculated by subtracting the mean RT of unfed fish from the mean RT of fed fish.
In the swimming experiments, the standard metabolic rates (RM) of whitefish larvae were calculated
according to the mass- and temperature-dependent oxygen consumption functions of Karjalainen
et al. (1995). RM was measured from unfed fish and thus was lower than the RM of fed fish.
16 THE BIG FISH BANG

Feeding respirometry. The feeding respirometry data of Wieser and Medgyesy (1990b) and of
Huuskonen et al. (1998) were reanalysed to try to identify which cost budgeting model is appro-
priate for larval coregonids. Detailed descriptions of the feeding respirometer (Wieser and
Medgyesy 1990a) and experimental protocols (Huuskonen et al. 1998) are given elsewhere. The
experiments at 10°C (n=9) and 15°C (n=13) were carried out in Innsbruck in 1991, and those at
12°C (n=2) in Joensuu in 1996 (Huuskonen 1997; Huuskonen et al. 1998).
In the feeding respirometer, three components of the energy budget could be determined
directly: food consumption (C), total metabolism (RT) and growth (PG). Further, it was possible to
separate total metabolic rate (RT) into standard metabolic rate (RM) and feeding-induced thermo-
genesis (RF); i.e. the energy used for maintenance was distinguished from costs related to activity
and digestion, absorption and processing of food (Wieser and Medgyesy 1990b). RF and RSDA have
thus slightly different meanings: RSDA includes no feeding costs, and RF is practically synonymous
with the apparent heat increment (AHI, Beamish and Trippel 1990). Metabolic rates were calculat-
ed as in Wieser and Medgyesy (1990b): 1) RT = sum of all oxygen consumption measurements
recorded hourly; 2) RM = the average of the three lowest values during the dark period multiplied
by the number of hours during an experiment; and 3) RF = RT - RM. The RF could be further
divided into RSDA and RACT (the costs of activity). The following calculations were used to convert
oxygen consumption and somatic growth into energy units: 1 µmol O2 = 0.45 J and 1 mg DM =
22.7 J (Wieser and Medgyesy 1990b).
RT, RM, RF and PG were inversely correlated with fish body mass (Wieser and Medgyesy 1990b)
and, due to the high size differences (fresh body mass 12.5-210 mg) of the fish in the separate ex-
periments, RT, RM, RF and PG were mass-corrected. The mass-dependent power functions used for
the conversion were calculated according to the original feeding respirometry data: RT = 34.7 FM-
0.132, R = 57.09 FM-0.160 and P = 62.2 FM-0.576. Furthermore, the true R was calculated in order
M G F
to correct the observed overestimation of the RM in the feeding respirometer experiments. The
overestimation of RM was feeding induced and this part of the costs was added to RF in order to
obtain true RF. These calculations are explained in detail in the next section.

Results
Like many other positively phototactic fish larvae, after hatching, whitefish larvae have very vigor-
ous swimming behaviour, high metabolic costs and extremely narrow scope for the physiological
performance. In our four feeding respirometry experiments, the costs of the maintenance (RM),
digestion (RSDA) and activity (RACT) were on average 68%, 22% and 10% of the total metabolic
costs, respectively. Note, however, that RM here evidently included some level of activity due to the
continuous swimming of larval fish.
In the swimming respirometer experiments, the total metabolic rate (RT) of unfed larvae was
lower than the total rate of fed larvae, and both total costs and digestion costs (RSDA) of the larvae
fed on a high ration were higher than the rates of larvae fed on a low ration. Food ration signifi-
cantly affected the total costs and digestion costs (Table 1, Fig. 2). The constant swimming speed in
the swimming chambers kept the activity and maintenance costs at a constant level.
 ADDITIVE A L L O C AT I O N O F M E TA B O L I C C O S T S 17

Table 1. Fresh mass (mg, mean ± standard deviation) and oxygen consumption rates (mean ± standard deviation,
n = number of cases in parentheses) of the fed (low or high ration) and unfed (no food) larval whitefish in the
swimming respirometer experiments at 12 and 14°C. Asterisks and dashes indicate the significant (*, p<0.05)
and insignificant (-, p>0.05) difference between the food rations, respectively.
Fresh mass Temperature Total metabolic rate RT
Experiment
mg ± SD °C µmol g–1 h–1 ± SD (n)
No food Low Ration High Ration
1 33.7±4.1 14 21.0±3.0 (18) * no data 26.3±5.6 (18)
2 57.6±4.0 14 19.4±2.0 (6) * no data 26.5±2.3 (6)
3 25.6±4.8 12 17.5±4.1 (8) ns 20.9±4.9 (11) * 25.0±1.6 (4)

Wieser and Medgyesy (1990b) observed that when whitefish larvae grew at a very high rate the
costs of feeding and digestion (RF) remained nearly constant or were independent of the growth
rate (PG) (Fig. 3A, dotted regression lines were originally based on data at 15°C). In the original
form of the data, RF indeed increased more slowly among the fast-growing larvae. However,
because the costs of maintenance (mass-corrected RM in Fig. 3B) correlated positively with PG at
15°C, the RM was obviously overestimated and RF underestimated in the high ration experiments.
Thus, the “true” RF was calculated as follows: firstly, the intercept constant (17.22 and 14.20 µmol
g-1 h-1 at 15°C and at 10-12°C, respectively) was subtracted from the each RM and then, the differ-
ence was added to the RF. The maximum difference at 15°C was 9.4 µmol g-1 h-1. The relationships
between the mass-corrected “true” RF and PG were linear and significant at all temperatures (Fig. 3C).
The RF correction was also made for low temperature experiments, although the regression
between RM and PG was not significant at 10 and 12°C. After the correction, the RF differed
between the temperatures, which was not observed in the original data.
RF and food consumption (C) also had a linear relationship: higher C produced higher RF. (Fig. 3D).
The high variation in this relationship was mainly due to inaccurate estimation of the number of
Artemia during each feeding period.

The summary of the results from all experiments are repre-

Figure 2. The oxygen consumption

(µmol g-1 h-1, based on fresh body
mass) of fed (ration 1 = low and
ration 3 = ad libitum) and unfed
(ration=0) larval whitefish in the
swimming respirometer experiments 1
and 2 at 14°C and experiment 3 at
12°C. The costs of digestion (RSDA),
activity and maintenance (RM+ACT)
are given separately and the vertical
lines represent the standard errors of
the mean of total oxygen consumption
rates (RT).
18 THE BIG FISH BANG

Figure 3. The oxygen consumption (µmol g-1h-1, based on fresh body mass) of larval whitefish in the feeding
respirometer experiments. The relationship A. between the costs of digestion (feeding induced thermogenesis
RF) and the specific growth rate (PG, % d-1), B. between the mass-corrected maintenance costs (standard meta-
bolic rate RM) and PG, C. between the true RF and PG and D. between the true RF and food consumption rate
(C, J g-1 h-1) at 15°C (black circle, solid line) and at 10 and 12°C (blank symbol, dashed line). The dotted lines
(linear regressions) in section A were fitted according to Wieser and Medgyesy (1990b, see text). All mass-
corrected rates correspond the rates of a larva at the size of 30 mg fresh body mass.

sented in Fig. 4. In the swimming experiments, although the fish swam at high speed, it was the higher
ration that produced the higher total costs. The predicted maintenance costs were fairly constant, as
was the proportion of energy allocated to the forced activity. The RM (on average 17.6 µmol g-1 h-1 at
14°C) calculated for the swimming respirometer experiments corresponded well to the “true” RM
(17.22 at 15°C) extrapolated from the measurements of the feeding experiments. The proportion of
the activity costs was smaller than in the feeding respirometer experiments which may be due to the
oxygen debt after swimming.
In the feeding experiments, the activity costs (RACT) increased in relation to the ration (more
food, more time and energy in feeding) and likewise the RSDA and the total costs were higher in the
 ADDITIVE A L L O C AT I O N O F M E TA B O L I C C O S T S 19

Figure 4. The oxygen consumption (µmol g-1h-1,

based on fresh body mass) of fed and unfed larval
whitefish in the swimming and feeding respirome-
ters. The costs of digestion (RSDA), activity (RACT)
and maintenance (RM) are given separately. The
rates were converted to correspond with the rates at
14°C. The temperature conversions (12°C to 14°C
and 15°C to 14°C) were made according to tempera-
ture-dependent function in Karjalainen et al.
(1995). The numbers above bars indicate ration
levels (0=unfed, 1=low ration, 2= medium ration,
3= fed ad libitum).

high ration experiments. Unfortunately, in only four of the 20 feeding experiments were RACT data
available for this analysis. The RM was again fairly constant except in the last experiment, when it
seemed too high and probably included either digestion or activity costs. In the high ration exper-
iments, the specific growth rates were from 14 to 16%.

Discussion
Our reanalysis of the feeding respirometer data of larval whitefish suggested that up to a growth
rate of 16% d-1 there was a positive linear correlation between the costs of growth and the growth
rate. Hence, the aerobic capacity available for digestion is sufficient and there is no need for com-
pensatory budgeting. The higher ration produced higher costs of feeding and digestion as well as
higher growth rate, and thus, the energy budget of the larval whitefish seems to be additive. In his
review, Wieser (1994) concluded that, “the non-linear relationship between cost and rate of
growth may be predominantly due to the changes in protein turnover”. However, he still argued
the possibility of the compensatory budgeting and represented the alternative model of Pirt (1982)
which assumes that “maintenance metabolism is not only dependent on experimental conditions
but also on the rate of growth itself ”. This maintenance model has two components: a constant
component and a component decreasing proportionally with growth rate (Wieser 1994). We
suggest that, in the case of larval whitefish, this is mainly a methodological problem. If the cost
components could be measured precisely (i.e. the maintenance component includes only mainte-
nance costs) then at least in long-term budgets (Lucas 1996) the simple additive energy budget
model proposed by Winberg (1956) is suitable also for larval coregonids. The duration of the ap-
parent heat increment after feeding is several hours to several days depending on fish size, temper-
ature, ration etc. (Jobling 1994; Blaikie and Kerr 1996), and the increased maintenance costs in the
feeding respirometer experiments were likely due to the longer duration of the apparent heat in-
crement when whitefish larvae were fed on higher number of Artemia nauplii. In other words, the
heat increment of feeding was not finished before the next feeding period and some part of the RF
was measured in RM, thus overestimating its proportion especially in the high ration experiments.
The slopes of the regression between RF and PG expressed the costs of growth for larval corego-
nids (RF/PG, Wieser 1994) and at 15°C the slope represented 17.3 µmolO2 mg-1 dry body mass
20 THE BIG FISH BANG

(using the dry body mass : fresh body mass ratio of 0.173 from Wieser and Medgyesy (1990b) and
30 mg fresh body mass in the beginning of the growth period). Our RF/PG is, therefore, only slight-
ly higher than the “consensus value” (16 µmolO2 mg-1 dry body mass) of Wieser (1994) for the
average efficiency of the transformation of metabolizable energy into production in a wide range
of organisms. If the feeding activity (on average 31% of total RF, n=4) is subtracted from the RF, the
cost of growth equals 12.3 µmol O2 mg-1 dry body mass. At lower temperature the RF/PG appears
to be lower, but due to higher variation in the data the exact values were not calculated.
The additive energy budget model assumes the independence of the different components. The
swimming respirometer experiments were designed to test this assumption and they confirmed that
the digestion and swimming costs were independent. In spite of the high swimming speed, the costs
of digestion increased in relation to the food ration. Active metabolic rates remained fairly low in our
swimming experiments and were slightly higher in the feeding respirometer experiments. However,
the swimming tests showed that whitefish larvae managed to maintain their position in the current
for no longer than 6-7 minutes, and thus they had to perform at their maximum capacity. The
oxygen debt (the oxygen consumption was recorded only for 7 minutes) may partly explain the rela-
tively low activity costs observed and total metabolic costs were possibly slightly underestimated.
The duration of the swimming experiments was short and the effects of activity on the growth
rates and growth efficiencies could not be estimated. Simultaneous long-term swimming and
feeding experiments would be needed to clarify the long-term relation between activity and diges-
tion costs. The effect of the unfavourable feeding and growing conditions as well as individual
growth strategies and growth efficiencies of larval fish also need further research. Conover and
Schultz (1997) proposed a possible trade-off between predator avoidance probability and growth
investment; then a larva with a more conservative energetic investment in growth would have a
higher capacity to allocate energy to predator evasion.
Several bioenergetics models constructed for juvenile and larval fish (e.g. Dabrowski et al.1989;
Post 1990; Karjalainen et al. 1997; Huuskonen et al. 1998) are based on the additive model originally
developed for adult fish. Our results suggest that the theoretical base of modelling larval coregonid fish
energetics under favourable feeding conditions is firm. Huuskonen et al. (1998) evaluated the validity
of a bioenergetics model constructed for whitefish using the same feeding respirometer data as in this
study. They found that the model was able to predict the food consumption of whitefish reasonably
well under experimental conditions. The consumption rates of fast-growing larvae were also estimat-
ed satisfactorily. Furthermore, our results show that the scope for activity of larval whitefish is tight
and the effects of changes in this component (e.g. due to predator avoidance or wind-induced cur-
rents) on the food consumption estimates seem to be negligible. In general, Kooijman (2001) argued
that “costs of feeding and movements that are part of the routine repertoire are usually insignificant
with respect to the total energy budget”. On the contrary, the unknown activity costs are considered
to be one of the weakest points in the current bioenergetics models of adult fish (Ney 1993).

Acknowledegements
We thank Mervi Kinnunen and Anna Väisänen for their help during respirometer experiments and
prof. Roger Jones who checked the English. Comments of two anonymous referees were valuable.
 ADDITIVE A L L O C AT I O N O F M E TA B O L I C C O S T S 21

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