Journal of Fish Biology (2003) 63, 956–969
doi:10.1046/j.1095-8649.2003.00203.x, available online at http://www.blackwell-synergy.com
Development and validation of a bioenergetics model for
juvenile and adult burbot
J.-P. J. P Ä Ä K K Ö N E N *, O. T I K K A N E N
AND
J. K A R J A L A I N E N
Department of Biological and Environmental Science, University of Jyväskylä,
P. O. Box 35, Jyväskylä FIN-40351, Finland
(Received 2 July 2002, Accepted 23 July 2003)
Oxygen consumption of juvenile and adult burbot Lota lota was measured in an intermittent-flow
respirometer to determine the effect of temperature and fish body mass on metabolic rate. These
results were combined with data from earlier experiments and the ‘Wisconsin bioenergetics’ model
was constructed. The model was validated under laboratory conditions by comparing observed
and predicted food consumption and growth of burbot fed on dead vendace Coregonus albula.
There was a good correspondence between observed and estimated growth and food consumption
under experimental conditions: the mean absolute per cent errors of growth and food consumption
were 48 and 240%. Estimated values with the new model were an improvement over the Atlantic
cod Gadus morhua model previously used for burbot. In the field, the reliability of food consumption estimates was verified by using polychlorinated biphenyls (PCB) accumulation as an indirect
indicator of the food consumption rate. The total PCB concentration of nine out of 13 burbot was
estimated accurately. Thus, the burbot model produced good estimates of food consumption, even
# 2003 The Fisheries Society of the British Isles
under field conditions.
Key words: bioenergetics; burbot; Lota lota; oxygen consumption; PCB.
INTRODUCTION
The burbot Lota lota L., the only true freshwater gadoid, is distributed throughout the Holarctic region (McPhail & Paragamian, 2000). The burbot is a
nocturnal bottom dwelling fish that is often found at temperatures <13 C
and is the top predator in several environments. The biology of burbot is still
poorly understood, although several studies on juvenile and adult burbot have
examined their physiology (Pääkkönen & Marjomäki, 1997, 2000; Johnson
et al., 1999) and ecology (Carl, 1995; Wang & Appenzeller, 1998; Fischer,
1999, 2000a, b; Paragamian et al., 1999; Hofmann & Fischer, 2001). Since the
diet of burbot overlaps that of other piscivorous species, a question has been
raised whether the burbot competes for food with economically valuable fish
species (Carl, 1992, 1995; Edsall et al., 1993; Rudstam et al., 1995; Fratt et al.,
1997; Tolonen et al., 1999). Due to the lack of information on burbot feeding processes and the effect of temperature on its physiology, estimates of food
*Author to whom correspondence should be addressed. Tel.: þ358 142602338; fax: þ358 142602321;
email: [email protected]
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BIOENERGETICS OF BURBOT
957
consumption rates have been based on the physiological variables of marine
gadoids (Rudstam et al., 1995). Therefore, a bioenergetics model based on physiological variables determined for this widespread species is needed to estimate food
consumption of burbot populations in freshwater food webs.
Bioenergetics quantifies the exchanges and transformations of energy and
matter between organisms and their environment. With fish bioenergetics
models, food consumption can be estimated from the growth rates of individual
fish. Modelling has proven useful in estimating the food consumption of several
fish species (Kitchell et al., 1977; Stewart et al., 1983; Hewett & Johnson, 1992;
Rudstam et al., 1995; Karjalainen et al., 1997).
In this study, a bioenergetics model was constructed for burbot using the
‘Wisconsin-type model’ developed by Kitchell et al. (1977) and Hewett &
Johnson (1992). Construction of the model requires the experimental derivation
of the main components (rate of metabolism, waste production and maximum
food consumption) of the balanced energy budget of fishes (Winberg, 1956;
Kitchell et al., 1977). Information from previous work (Pääkkönen & Lyytikäinen,
2000; Pääkkönen & Marjomäki, 2000) was combined with new measurements of the metabolism and temperature tolerance of adult and juvenile
burbot. After model construction, predictions of food consumption derived
from observed growth by the new and previous (Rudstam et al., 1995) burbot
model were compared with food consumption observed under experimental
conditions. The experiments were independent of those used for variable
development, thereby allowing the assessment of model performance and its suitability for estimating food consumption in the burbot, a sedentary, piscivorous fish
species. The reliability of food consumption estimates was also verified in the field
by using polychlorinated biphenyls (PCB) accumulation as an indirect indicator of
the individual food consumption rate. Multiple approaches, including field and
experimental testing, can allow for a reasonably thorough evaluation of fish
bioenergetics models (Madenjian et al., 2000).
MATERIALS AND METHODS
R E S PI R O M E T R Y
Juvenile burbot (fresh mass 59–123 g, n ¼ 37) were electrofished from Lake Konnevesi
(62 370 N; 26 210 E), central Finland, in August and September 2000. Captured fish were
transported to the laboratory at the University of Jyväskylä, where they were held in
aquaria and fed on earthworms before experiments. For oxygen consumption measurements, one fish was placed in each respirometry chamber. Oxygen consumption of
juvenile burbot was studied at 10, 12, 14, 16, 18, 20 and 22 C. Water temperature from
the rearing temperature to the experimental temperature was changed at a maximum of
2 C day1. Fish were held for 24 h at the experimental temperature prior to measurements being taken and no long-term acclimation to the experimental temperature was
carried out. All measurement sessions lasted 24 h and fish were killed with an overdose of
anaesthetic (MS-222) and weighed after the sessions. Fish age was determined from the
otoliths: two of the fish were 0 years and the rest were 1 year.
Adult burbot (fresh mass 752–8566 g, n ¼ 12) were caught by trap nets from Lake
Päijänne (62 100 N; 25 450 E), central Finland, during the spawning season in February–
March. The burbot were held in the laboratory at the University of Jyväskylä in 1 m3
steel tanks at 2–4 C and were fed once a week on dead vendace Coregonus albula (L.).
Prior to the experiment, the fish were moved to acclimation tanks where they were
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J . - P . J . P Ä Ä K K Ö N E N E T A L .
acclimated for 2–3 days to the initial experimental temperature. Food was offered to the
burbot during acclimation, but only some fish ate. Burbot were weighed individually
before transfer to the respirometry chambers (one fish per chamber). Oxygen consumption measurements were taken at 7, 13, 18 and 25 C. The measurement session at 7 C
lasted 120 h and the remaining sessions took 48 h each. After a measurement session the
burbot were transferred to the acclimation tank and were allowed to acclimate to the next
experimental temperature for 2–3 days. The maximum rate of temperature change was
3 C day1. Two burbot which escaped and died during the acclimation were replaced
with new individuals. In addition, data from a previous investigation (Pääkkönen &
Lyytikäinen, 2000) of oxygen consumption of adult burbot at 21 C (n ¼ 19) were
reanalysed and used in this study.
Oxygen consumption of burbot was measured in an intermittent-flow respirometer
equipped with a polarographic oxygen sensor (YSI 5750). The respirometer system included
three acrylic chambers with two different volumes of 147–148 and 3980–8780 ml for juvenile
and adult burbot, respectively. Oxygen consumption in each chamber was recorded for 15 min
every hour and the average rate during this period extrapolated to obtain an hourly value. The
oxygen electrode chamber and the fish chambers were flushed with fully aerated water for 15
and 45 min, respectively, every hour. The oxygen consumption of the empty respirometer
chambers (without fish) were measured before and after fish measurements and the bacterial
consumption was subtracted from the total oxygen decline. The routine rate of oxygen
consumption (Rr; mmol g1 h1) was the average of all hourly measurements (n ¼ 18), excluding the three highest and three lowest values during experiment which were used to calculate
maximum and minimum rates of oxygen consumption (Rmax and Rmin, respectively). The flow
rate of water in the chambers was low and in this respect the system was almost static.
C O N ST R U C T I O N O F T H E B U R B O T M O D E L
A bioenergetics model was constructed for burbot in the framework of the Fish Bioenergetics 3.0 software (Wisconsin-type model originally developed by Hewett & Johnson,
1992). The Wisconsin model requires the mass and temperature dependence of three main
components (maximum food consumption, metabolism and production of wastes) to be
formulated mathematically from experimental data. The present maximum food consumption functions were based on earlier experiments examining the feeding of burbot at
different temperatures (Pääkkönen & Marjomäki, 2000). Water temperatures ranged
from 24 to 234 C and fresh masses of fish from 104 to 353 g. These experimental
data were used to fit the maximum consumption (Cmax) function for burbot:
Cmax ¼ aMbf(T), where M is the mass of burbot (g), a is intercept of the allometric mass
function, b is the slope of the allometric mass function and f(T) is dome-shaped temperature dependence function (Kitchell et al., 1977). The f(T) is defined as:
h
i
fðTÞ ¼ ðTmaxC TÞðTmaxC ToptC Þ1
n
n
ffi2 o
pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi2 o 00025 z2 pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
ð1þ40y1 Þ
½ðTmaxC T ÞðTmaxC ToptC Þ1 1
00025 z2
ð1þ40y Þ
e
,
where TmaxC is the maximum water temperature above which consumption ceases, ToptC is
the optimum water temperature and T is water temperature. A ToptC temperature of 14 C
from previous feeding experiment was used (Pääkkönen & Marjomäki, 2000).
Parameters Z and Y are defined as: Z ¼ ln(CQ)(TmaxC ToptC) and Y ¼ ln(CQ)
(TmaxC ToptC þ2), where CQ is the Q10 rate.
Metabolic cost functions were derived from the respirometry data by the equation:
Rrtm ¼ aMbf(T)ACT, where Rrtm is the mass-specific respiration rate (g O2 g1 day1), M is fish
mass (g), f(T) is the temperature dependence function, ACT is an activity multiplier and a and b
are fitted constants. The temperaturendependence function
[f(T), Kitchell eto al., 1977] is defined
o n
h
i
pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi2
1
00025 z2
ð1þ40y Þ
pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi2
1
00025 z2
ð1þ40y Þ
½ðTlethal TÞðTlethal ToptR Þ1 as: fðT Þ ¼ ðTlethal TÞðTlethal ToptR Þ1
,
e
where Tlethal is the lethal water temperature ( C), ToptR is the optimum water
temperature for respiration and T is water temperature. Parameters Z and Y are defined
as: Z ¼ ln(RQ)(Tlethal ToptR) and Y ¼ ln(RQ)(Tlethal ToptR þ 2), where RQ is the Q10
rate for respiration.
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BIOENERGETICS OF BURBOT
959
The Tlethal was estimated for burbot (fresh mass 777–2920 g, total length LT, 250–370 mm,
n ¼ 20) by acclimating five fish to four temperatures ranging from 2 to 21 C. Water temperature from the rearing temperature to the experimental temperature was changed at a
maximum of 2 C day1. Fish were acclimatized for a week at constant temperature prior to
measurements. Acclimated fish were transferred to an experiment chamber and the water
temperature was then increased at a rate of 18 C h1 as suggested by Becker & Genoway
(1979). The average temperatures at which fish lost its equilibrium and the opercular movements stopped were calculated. The lethal temperature (Tlethal) was the temperature when loss
in equilibrium was observed on fish that had been acclimated at 12 C. Burbot are seldom
observed at temperatures >12 C in lakes with cool epilimnia (Carl, 1995). Therefore, it
represents the upper limit that adult burbot are generally able to tolerate in the lakes.
Consumption and respiration models were fitted iteratively by the quasi-Newton method
using the Statistica computer programme (Statsoft, 1997). Burbot usually lay motionless on the
bottom of the aquarium, but they increased their swimming activity considerably when food
was offered. The swimming activity ceased soon after feeding and cleaning of aquarium were
stopped. Thus, feeding-induced oxygen consumption was modelled from the respirometry data
by a simple activity multiplier (ACT), which was calculated by multiplying feeding hours (4 h) in
validation experiments by the mean Rr and the ratio between
Rmax and Rr. The resultantvalue
1
was then related to mean Rr during 24 h: ACT ¼ 1 þ 0:0417b4Rr ðRmax R1
r ÞcRmax .
Thus, the mean value of activity multipliers at different temperatures was used in the
burbot model. Specific dynamic action (SDA) was estimated to be 16% of assimilated energy
for burbot (Pääkkönen & Lyytikäinen, 2000).
Waste production by burbot fed on fish meals was not estimated experimentally but
the energy loss to egestion and excretion was based on the values for other piscivorous
fishes (Hewett & Johnson, 1992). In the burbot model, the coefficients were 017 and 009
for egestion and excretion, respectively.
Johnson et al. (1999) found that burbot size had no effect on energy density. Hence, the
reported mean energy content value of 5125 J g1 was used for burbot (Johnson et al.,
1999). An energy content value of 4636 J g1 was used for vendace (Pääkkönen &
Marjomäki, 1997).
VALIDATION OF THE BURBOT MODEL
The bioenergetics model was used to predict the food consumption of burbot under
experimental conditions. The food consumption estimate was based on the mass change
of fish during the experiment. In addition, the growth of burbot was estimated by the
model based on the observed food consumption. The bioenergetics model was validated
by comparing the observed and estimated food consumption and growth estimates. Four
criteria have been used for validation
1993): (1) the mean absolute
nPh (Mayer & Butler,
io
yo yp jyo j1 n1 , where yo represent observed
percentage error E%, E% ¼ 100
values, yp predicted values and n the number of pairs; (2) modelling efficiency Ef,
hP
ihP
i1
Ef ¼ 1 ðyo ym Þ2
ðyo ym Þ2 , where ym is the mean of observed values; (3)
the regression coefficient (r2) of the linear regression between observed and predicted
values; (4) the location of the regression line (constant a, slope b). The difference of
constant a from 0 and slope b from 1 was tested by the t-test.
In the validation experiment, the food consumption of burbot (n ¼ 12, mean
mass ¼ 3273, range 1531–5959 g) was measured at 12, 15 and 19 C. Burbot were held
separately in 12 aquaria from 7 to 14 days. The fresh mass (001 g) was measured prior to
the experiment and 3 days after the last meal. The burbot were fed daily with a meal
consisting of whole dead vendace. The size of the offered meal was 10% of the fresh mass
of the burbot at the beginning of the experiment. Vendace were placed at the bottom of
the aquaria and burbot were allowed to feed for at least 3 h. A photoperiod of 6 L:18D
was used; a meal was offered 1 h before the light was switched off.
In the field, the growth of burbot (n ¼ 13) from Lake Päijänne was estimated from the
backcalculated LT at age. Measurements for backcalculation of LT were made on each whole
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J . - P . J . P Ä Ä K K Ö N E N E T A L .
otolith along the proximal axis from the focus to each annulus and the edge. Length at age was
backcalculated from the equation: LTn ¼ (snstot1)0737LT, where LTn is length at age n, sn is
radius of the nth annulus from focus of otolith, stot is total radius of the otolith. The
bioenergetics model was used for each fish to determine the food consumption required for
annual growth. Temperature regimes were set to resemble the environment in the deep basins
of large lake (i.e. 2–4 C during October–April and 5–8 C during March–September).
The food of burbot was divided into invertebrates (Mysis relicta Loven) and fishes (perch
Perca fluviatilis L and vendace, categories of the latter based on the burbot diet data
collected from Lake Päijänne; Pääkkönen, 2000). The PCB concentration of vendace and
perch in Lake Päijänne was 50 and 49 ng g1 in the 1970s and 1990s (Hattula et al., 1978;
Kiviranta et al., 2000; Korhonen, 2000). Särkkä et al. (1978) measured a PCB concentration
of 44 ng g1 for zoobenthos predators in Lake Päijänne. Kucklick & Baker (1998) analysed
a minimum PCB concentration of 56 ng g1 in small M. relicta in Lake Superior, North
America. Hence, an average PCB concentration of 50 ng g1 (wet mass) was assumed for
both prey categories. The total PCB concentration (mg g1 wet mass) of burbot was
analysed by GC-ECD (sum of congeners PCB 18, 28, 44, 52, 101, 105, 118, 128, 137, 138,
153, 156, 159, 169, 180 and 209). The mean PCB assimilation efficiency of burbot was
estimated experimentally as 071 in a 4 week exposure test to four different PCB congeners
(PCB 18, PCB 44, PCB 137 and PCB 169) (J.-P. Pääkkönen, unpubl. data). The total food
consumption of 5 to 7 year-old burbot, the mean PCB concentration of prey and the
assimilation efficiency were used to calculate total lifetime PCB accumulation value (PCBtot)
by using the bioenergetics model. The observed PCB concentrations of individual burbot
were then compared with those estimated from the model on the basis of food consumption.
RESULTS
RESPIROMETRY
The mass-specific routine rate of oxygen consumption (mmol g1 h1) of
juvenile and adult burbot increased with water temperature and was lower in
adults (Fig. 1). The temperature and mass dependence of Rr of juvenile and
adult burbot was described by the function: Rr ¼ 5475M0209e0034T, (r2 ¼ 084,
n ¼ 96, P < 0005 for all variables) where M is the fresh body mass (g) of burbot
and T is the ambient water temperature ( C).
Rr, Rmax and Rmin of adult burbot increased with temperature (Kruskal–
Wallis H, d.f. ¼ 3, n ¼ 42, P < 0001; Fig. 2). The Rr of adult burbot approached
the observed Rmax values as the temperature increased. The ratio of Rmax to Rr
decreased from 193 to 127 in the temperature range 70–249 C (Kruskal–
Wallis H, d.f. ¼ 3, n ¼ 42, P < 0001), but Rmin : Rr did not change significantly
with temperature (Kruskal–Wallis H, d.f. ¼ 3, n ¼ 42, P ¼ 0690).
C O N ST R U C T I O N O F T H E B U R B O T M O D E L
The temperature and mass dependence of the maximum food consumption
rate (Cmax; g g1 day1) of juvenile and adult burbot was described by the
function: Cmax ¼ 0074M02982f(T).
The mass-specific respiration rate (Rrtm) of juvenile and adult burbot was
described by the function: Rrtm ¼ 00985M0186f(T)126, where 126 is the activity
multiplier (ACT). ACT declined from 132 to 121 as the temperature was raised
from 70 to 249 C. The mean S.D. ACT of 126 005 was used in the bioenergetics model for burbot.
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BIOENERGETICS OF BURBOT
12
10
Rr (µmol g–1 h–1)
8
6
4
2
0
0
2
4
6
8
10
12
14
16
18
20
22
24
26
Temperature (° C)
FIG. 1. Temperature-dependent routine rate of oxygen consumption in juvenile (&, 586–1225 g, n ¼ 37)
and adult (^, 752–8566 g, n ¼ 43) burbot. Value at 21 C obtained from Pääkkönen & Lyytikäinen
(2000).
The acclimation temperature (AT) had a significant effect on the temperature at
which loss of equilibrium or the cessation of opercular movement was observed
(Kruskall–Wallis H, d.f. ¼ 3, n ¼ 20, P < 0001; Fig. 3). Loss of equilibrium and the
cessation of opercular movement were significantly different at lower acclimation
temperatures (Mann–Whitney U, P < 0001), but no difference between loss of
equilibrium and the cessation of opercular movement was observed at acclimation
temperatures 198 and 207 C (Mann–Whitney U, P ¼ 0312). For the bioenergetics modelling, a Tlethal of 27 C at the acclimation temperature of 12 C was
observed. The optimum temperature for respiration of burbot was estimated to be
23 C, which was intermediate of two highest temperatures of the oxygen consumption experiment. All variables for the burbot model are presented in Table I.
VALIDATION OF THE BURBOT MODEL
In the validation experiments, the mean E% of the bioenergetics model were
48 and 240% and the Ef were 099 and 095 for growth and food consumption,
respectively (Fig. 4). The regression equation calculated between estimated
(M2est) and observed mass (M2) at the end of experiments was:
M2est ¼ 0993 M2 þ 14590 (n ¼ 12, r2 ¼ 0996, P < 0001).
For food consumption, the regression between estimated and observed values
was: Cest ¼ 0916C 7466 (n ¼ 12; r2 ¼ 0913, P < 0001). The constant a of the
fitted regression lines did not differ significantly from 0 (t-test, a ¼ 0, d.f. ¼ 22,
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6
Oxygen consumption(µmol g–1 h–1)
5
4
3
2
1
0
0
5
10
15
20
25
30
Temperature (° C)
FIG. 2. The mean routine (þ), minimum (^) and maximum (&) rates of oxygen consumption of adult
burbot at different temperatures.
P > 005) and the slope b did not differ significantly from 1 (t-test, b ¼ 1, d.f. ¼ 22,
P > 005). The distribution of residuals did not differ significantly from a normal
distribution in either regression (Kolmogorov-Smirnov; P > 005). The residuals
between observed and predicted growth or consumption did not correlate with
temperature, mass or observed consumption (Pearson r, P > 005).
In field, the total PCB concentrations of nine out of 13 burbot were predicted
accurately (Fig. 5). The accumulation of PCBs in fish was assumed to occur only
via food consumption and a good fit between observed and estimated PCB concentrations indicated a good fit between observed and predicted food consumption.
DISCUSSION
Water temperature and fish mass had significant effects on the metabolic rate
of burbot. Oxygen consumption increased in juvenile and adult fish as temperature increased and the smallest fish consumed more oxygen per unit mass as
expected. The mass-specific oxygen consumption rates of adult burbot were
close to those reported for Atlantic cod Gadus morhua L., but the optimum of
metabolic rates was higher than that suggested for Atlantic cod (13–15 C)
(Claireaux et al., 2000). Fischer (2000b) examined the respiration rates and
activity of juvenile burbot fed on different bottom substrata and reported
daytime (passive period) oxygen consumption rates that were in agreement
with the present results for juvenile burbot at 10–14 C. Indeed, juvenile burbot
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BIOENERGETICS OF BURBOT
Temperature (° C)
35
30
25
20
0
5
10
15
20
25
Acclimation temperature (° C)
FIG. 3. The loss of equilibrium (---, y ¼ 0371x þ 2248, r2 ¼ 0916; P < 0001) and end of operculum movements (
, y ¼ 0255x þ 2505, r2 ¼ 0858, P > 0001) in relation to the acclimation temperatures.
were passive in respirometry chambers and exhibited no stress-induced increase
in metabolic rates.
In critical maximum temperature (CMT) studies water must be heated fast
enough to allow deep-body temperatures to parallel test temperatures without a
significant time lag and the test organism must not acclimate upward. An
increase rate of 18 C h1 is appropriate for routine CMT determinations and
permits accurate determination of loss of equilibrium and death times and
temperatures (Becker & Genoway, 1979). The observed CMT of burbot were
high for a cold water fish species. Burbot that were adapted to cold water
(<10 C) were able to survive at the temperatures >20 C. In lakes, adult burbot
prefer cool water areas (<13 C) and are usually below the thermocline (Edsall
et al., 1993; Carl, 1995). The preferred temperatures recorded in lakes are well
below the observed critical temperatures in this study. The wide temperature
tolerance of the burbot enables it to utilize larger water volumes, if necessary, to
seek food in shallow water areas or the epilimnion. The burbot also lives in
rivers and shallow reservoirs, where water temperatures during summer can be
considerably higher (>15 C) than in the profundal areas of lakes and where
there are no cool water refuges (Vogt, 1978; Breeser et al., 1988). Tolerance of
high water temperatures also enables short visits to warmer waters (>20 C), as
observed in Lake Opeongo (Carl, 1995). The burbot is able to feed at a
relatively high temperature (Pääkkönen & Marjomäki, 2000). The Rr
approached the maximum rate of oxygen consumption (Rmax) at the highest
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TABLE I. Equations and parameter values used in the bioenergetics model for burbot
Symbol
Description
Value
Consumption (C) C ¼ PaMbf(T)
Fitted parameter
Intercept for 1 g fish at ToptC
Coefficient of the mass dependence
Maximum temperature ( C)
Optimum temperature ( C)
Q10 value for consumption
P
a
b
TmaxC
ToptC
CQ
00747
02682
28
14
253
Metabolism (R) R ¼ aMbf(T)ACT; RSDA ¼ SDA (C F)
Intercept for 1 g fish at RTO (g g1 day1)
Coefficient of the mass dependence
Maximum lethal temperature ( C)
Optimum temperature ( C)
Q10 value for respiration
Activity multiplier
Specific dynamic action
a
b
Tlethal
ToptR
RQ
ACT
SDA
Egestion (F) and excretion (U), F ¼ fC; U ¼ e(C F)
f
Proportion of consumed food egested
e
Proportion of consumed food excreted
000985
0186
27
23
152
126
016
017
009
experimental temperature (25 C), suggesting harmful effects on the metabolism
of burbot and thus a lower maximum aerobic performance. At high water
temperatures, however, the metabolic costs may exceed the energy obtained
from food, which leads to a decrease in growth. Gut blood flow in fishes are
known to decrease as a result of blood redistribution to support other activities,
which may result in food conversion and growth that are sub-optimal (Farrell
et al., 2001).
The diet of adult burbot varies seasonally: in the winter, and in cool water, it is
dominated by fishes [vendace, smelt Osmerus eperlanus (L.), ruffe Gymnocephalus
cernuus (L.)], but in warmer summer months, invertebrates (M. relicta and Pallasea
quadrispinosa G.O. Sars) become common in burbot diet, their occurrence decreasing towards the winter (Pääkkönen, 2000). The lipid concentration is dependent on
the type of diet. Hop et al. (1997) observed differences in the energy content of
another gadoid, the Arctic cod Boreogadus saida (Lepechin), between fish and
invertebrate meals. A lipid concentration of 70% has been recorded for M. relicta
(Morrison et al., 1999) and 36% for the vendace (J.-P. Pääkkönen, unpubl. data).
Burbot may compensate for an increase in metabolism by increasing the proportion
of species in the diet that have a higher energy content (i.e. invertebrates). Its high
critical maximum temperature, high optimum temperature for metabolism and
ability to feed at high temperatures, however, enables the burbot to succeed in a
variety of environments.
The bioenergetics model developed for burbot in this study accurately predicted the food consumption and growth of fish under experimental conditions,
having modelling efficiencies (Ef) of >095. In previous studies, the
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700
(a)
600
Estimated mass (g)
500
400
300
200
100
0
0
100
200
300
400
500
600
700
Observed mass (g)
150
Estimated consumption (g)
(b)
100
50
0
0
50
100
150
Observed consumption (g)
FIG. 4. The observed and bioenergetics model estimated (a) masses and (b) food consumptions of burbot
in the validation experiment.
, the estimated and observed values are equal. ---, the fitted
regression line (see text for regression equations).
bioenergetics model variable values adapted from Atlantic cod experiments have
been used as a substitute for burbot (Rudstam et al., 1995). The Atlantic cod
variable values were also used to predict the consumption and growth of burbot
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2003 The Fisheries Society of the British Isles, Journal of Fish Biology 2003, 63, 956–969
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J . - P . J . P Ä Ä K K Ö N E N E T A L .
0.10
Total PCB concentration (mg kg–1)
0.09
0.08
0.07
0.06
0.05
0.04
0.03
0.02
0.01
0
280
320
360
400
440
480
Length (mm)
FIG. 5. The observed (^) and estimated (h) total PCB concentrations at total length of burbot (n ¼ 13)
captured from Lake Päijänne. Total PCB concentrations were estimated by the bioenergetics
model.
in the validation experiments and the Ef and E% for the ‘cod’ model were 089
and 428% for consumption and 099 and 63% for growth, respectively. Thus,
the ‘cod’ model predicted the consumption and growth of burbot well, although
food consumption under experimental conditions was underestimated more
than in the model developed for burbot.
Validation of the food consumption predictions of bioenergetics models
under field conditions has rarely been performed. Where validation has been
carried out it has generally been based on a comparison between two models,
typically between an evacuation rate model and a bioenergetics model (Hansson
et al., 1996; Schaeffer et al., 1999). In the present study highly resistant and
lipophilic PCBs were used as ‘label compounds’ in the validation of the food
consumption of burbot in Lake Päijänne. Madenjian et al. (2000) used a similar
approach when they compared the PCB accumulation efficiency of lake trout
Salvelinus namaycush (Walbaum) under experimental and field conditions. In
Lake Päijänne, the total PCB concentration of nine of 13 burbot was predicted
well. Furthermore, all those four individuals, whose observed values were higher
than the predicted ones, were males. The sexual difference in contaminant
accumulation rates of burbot has been also observed in walleye Stizostedion
vitreum (Mitchill) (Madenjian et al., 1998).
One of the major benefits of bioenergetic model construction is that the
development work identifies gaps in the scientific knowledge, and this was
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2003 The Fisheries Society of the British Isles, Journal of Fish Biology 2003, 63, 956–969
BIOENERGETICS OF BURBOT
967
true here. Future studies should focus on why burbot inhabits the cool parts of
lakes, where temperatures are clearly below its physiological temperature optimum. One explanation may be connected to the ability of burbot to ingest large
amounts of food. Also, the morphology of the burbot heart has recently been
shown to differ from what of other teleost freshwater fishes and these differences have been suggested to be structural adaptations to the cold water (Tiitu
& Vornanen, 2002). Furthermore, the increased blood flow from intestine to
liver may affect the ability of burbot to tolerate higher temperatures. A second
important issue is to estimate the variation in assimilation efficiencies and other
physiological variables between burbot individuals. Individual variation may
explain the weaker model fit between the observed and predicted food consumptions than between growth estimates. In summary, the burbot model
presented in this study seems to produce good estimates of food consumption
even under field conditions and hence can be used as a tool to incorporate the
role of burbot into lake food web studies.
All experimental protocols were inspected and approved by the laboratory animal
committee of the University of Jyväskylä. We thank A.-L. Rantalainen for the PCB
analysis and R. Siddall for checking the English. This work was financially supported by
the Maj and Tor Nessling Foundation.
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