Condition, prolonged swimming performance and muscle metabolic capacities of cod Gadus morhua
1 Université Laval, Cité Universitaire, Québec, G1K7P4,
Canada.
2 Ministère des Pêches et des Océans, Institut
Maurice-Lamontagne, 850, route de la Mer, CP 1000, Mont-Joli, Québec,
G5H 3Z4, Canada
3 Fisheries and Marine Institute of Memorial University of Newfoundland, PO
Box 4920, St John's, Newfoundland, A1C 5R3, Canada
4 Department of Fisheries and Oceans, Science Branch PO Box 5667, St John's,
Newfoundland, A1C 5X1, Canada
* Author for correspondence (e-mail: Helga.Guderley{at}bio.ulaval.ca)
Accepted 21 October 2002
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Summary |
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Key words: Atlantic cod, Gadus morhua, white muscle, red muscle, aerobic metabolism, anaerobic metabolism, longitudinal variation, prolonged swimming
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Introduction |
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Vertebrate muscle can power movements covering a wide range of speeds and
durations (Jayne and Lauder,
1994), mainly due to the existence of fibre types with different
contractile and metabolic properties. The body musculature of fish is
principally composed of red and white fibres, although intermediate pink
fibres exist (Johnston, 1981
;
Patterson et al., 1974
;
Akster, 1985
;
Akster et al., 1985
). The bulk
of fish muscle is composed of fast-twitch glycolytic (white) fibres
(Bone et al., 1978
;
Webb, 1978
). The slow-twitch
oxidative (red) fibres are confined to a small section of the skeletal
musculature beneath the lateral line, the relative importance of which
increases towards the tail (Bone,
1966
; Bone et al.,
1978
; Videler,
1993
). Pink fibres lie between white and red fibres and have
intermediate metabolic capacities
(Coughlin and Rome, 1996
;
Coughlin et al., 1996
).
Although sustained swimming principally relies upon red fibres, which are
resistant to fatigue and have a slow shortening speed
(Bone et al., 1978
), the pink
fibres may be important in sustained swimming due to their intermediate
characteristics (faster rate of relaxation and maximum velocity of shortening)
(Coughlin et al., 1996
). The
relative proportion of fibre types reflects the locomotory style of the
species (Bone, 1966
).
Accordingly, fish species that are specialised for high-speed, sustained
swimming have a greater proportion of red fibres in their musculature. When
the swimming speed increases, the tailbeat frequency rises and white fibres
are increasingly recruited (Bone et al.,
1978
; Johnston and Moon,
1980
). Short powerful sprints of activity are primarily supported
by the contraction of white glycolytic fibres. White fibres may also be
recruited during sustained swimming
(Burgetz et al., 1998
).
Recruitment of muscle fibres during undulatory swimming changes along the
fish body, with individual species differing in their recruitment patterns
(van Leeuwen et al., 1990;
Rome 1992
;
Wardle and Videler, 1993
;
Jayne and Lauder, 1995
;
Thys et al., 2001
). Gadoid
fishes, such as cod, use subcarangiform swimming, where swimming is powered by
the myotomal musculature and the caudal fin. Subcarangiform swimming leads to
the inclusion of a complete propulsive wave within the body length; however,
major increases in amplitude are restricted to the posterior half to third of
the body (Webb, 1978
). The
power produced by white fibres in the more rostral sections is transmitted
caudally, stretching the caudal fibres during their activation
(Altringham et al., 1993
;
Davies et al., 1995
;
Johnston et al., 1995
). The
requirements of tension development during transmission of force to the tail
may explain the higher catabolic capacities of white muscle from the caudal
region of Atlantic cod (Martínez et
al., 2000
).
Although much is known about how fish use their different muscle fibres
during swimming, little is known about the impact of energetic status upon
swimming performance or about the physiological determinants of swimming
capacity. A fish's energetic condition has a pronounced impact upon the
metabolic and contractile capacities of muscle and upon the availability of
fuels for swimming (Moon and Johnston,
1980; Sullivan and Somero,
1983
; Black and Love,
1986
; Kiessling et al.,
1990
; Lambert and Dutil,
1997a
). Starvation decreases the activities of muscle enzymes and
the concentrations of contractile proteins
(Beardall and Johnston, 1983
;
Houlihan et al., 1988
). The
responses to starvation are more pronounced in white than red fibres (Beardall
and Johnston, 1983
,
1985
;
Lowery and Somero, 1990
),
suggesting that endurance at sustained swimming speeds would be spared during
decreases in energetic status. On the other hand, virtually all protocols
measuring sustained and prolonged swimming lead to recruitment of white muscle
(Burgetz et al., 1998
;
McDonald et al., 1998
;
Reidy et al., 2000
). Thus, we
reasoned that simultaneous study of swimming endurance at prolonged speeds and
its potential biochemical determinants would allow us to determine whether
endurance is best predicted by oxidative or glycolytic capacities.
In the Northwest Atlantic Ocean, cod can experience long periods (8 months)
with low food availability (Lilly,
1994; Kulka et al.,
1995
). These lead to seasonal reductions in their energetic status
(condition) and muscle metabolic capacities
(Guderley et al., 1996
;
von Herbing and Boutilier,
1996
; Lambert and Dutil,
1997b
; Martínez et al.,
1999
), which result in increased natural mortality, particularly
during the spawning and migration periods
(Dutil and Lambert, 2000
). If
reductions in condition diminish swimming performance, they may well increase
the vulnerability of cod to predation and capture by mobile fishing gears.
Given the economic importance of the cod, knowledge of the link between
condition and swimming performance is of both practical and fundamental
interest.
This paper describes the effects of condition on the swimming endurance of
cod from Newfoundland waters. We established two groups of fish: (i) cod that
were fed twice a week for 16 weeks and (ii) cod that were starved for 16
weeks. We then compared the swimming endurance of the fed and starved cod. We
measured endurance at speeds greater than the maximum sustained swimming
speeds (Umax) published for this species
(Beamish, 1978;
He, 1991
), to assure the
participation of red and white muscle. We assessed the metabolic capacities of
white and red muscle sampled at three locations along the body (behind the
head, at the middle of the body and at the caudal peduncle), by measuring the
activity of four glycolytic enzymes: phosphofructokinase (PFK), pyruvate
kinase (PK), creatine kinase (CK) and lactate dehydrogenase (LDH), two
mitochondrial enzymes: cytochrome c oxidase (CCO) and citrate
synthase (CS), and a biosynthetic enzyme, nucleoside diphosphate kinase
(NDPK). We also measured the concentrations of water, glycogen and protein, in
red and white muscle sampled at these locations. Lactate content was
determined on white muscle biopsies taken at the middle of the body
immediately after the endurance test. Growth rates were calculated from
changes in mass and length over the 16 weeks. During each swimming test, we
noted the swimming behaviour, including the number of burstcoast
movements made by the fish. These data were used to examine the links between
condition, enzyme levels in white and red muscle along the body and endurance
swimming of cod.
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Materials and methods |
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Endurance test
Endurance was tested using a swimming flume, following the methods of
Winger et al. (2000).
Individual cod underwent a training routine before beginning the endurance
test. This routine began with a minimum 10 min habituation in the flume at a
speed of 0.25 body lengths per second (BL s-1), followed
by a 10 min orientational swim at 0.5 BL s-1. The swimming
speed was gradually increased from 0.5 to 1.0 BL s-1 over
5 min. The fish were allowed 5 min of swimming at 1.0 BL
s-1 before gradually increasing the swimming speed to the target
speed of 1.8 BL s-1, a speed greater than the
Ucrit of cod at these temperatures
(He, 1991
;
Winger et al., 2000
). Swimming
was encouraged using pairs of electrodes in the downstream end of the swimming
flume. A pulsing stimulus (2 Hz) with peak voltage of 15 V was applied to
encourage the fish to swim against the flow until exhaustion. A fish was
considered exhausted when it was unable to lift off the downstream electric
net after 10 s. When individual endurance exceeded 200 min, the tests were
terminated. Water temperature during the swimming trials ranged from
10-14°C; no significant impact of water temperature on swimming endurance
or any of the performance parameters was apparent. Swimming trials were filmed
using a Sony® CCD-TR500 video camera (30 frames s-1). Video
footage of the swimming fish was analysed using a Panasonic® time-lapse
video recorder (model AG-6730) to determine the number of burstcoast
movements made by the fish during the swimming test, as well as to examine the
overall swimming behaviour.
Tissue sampling
Immediately after the swim test, we took a biopsy of white muscle below the
first dorsal fin, according to Mair
(1989). The cod were allowed
to recuperate in a holding tank for 72 h before being anaesthetised with
2-phenoxyethanol at a concentration of 0.125 ml l-1 in seawater at
ambient temperature. The cod were killed by a blow to the head, measured and
weighed. White and red muscle (3-5 g for white, 1-2 g for red) were sampled at
three sites along the length of the fish body: (1) just behind the head, (2)
at the middle of the second dorsal fin of the fish and (3) in the caudal
region. All samples were weighed (to ±0.1 g). White muscle was sampled
above the lateral line, while red muscle was taken at the level of the lateral
line (Fig. 1). To avoid
contamination of the white muscle samples by red or pink fibres, white muscle
samples were dissected deep in the trunk. The rostral red muscle may have been
contaminated by pink fibres, however, given the thinness of the red muscle
layer and the difficulty of identifying pink fibres. Samples of white and red
muscle were immediately frozen in liquid nitrogen, then stored at -70°C
before transport on dry ice to Université Laval where they were again
stored at -70°C until biochemical assays were done.
|
Tissue extraction
Tissue extracts were prepared by homogenising samples in 10 volumes of 50
mmol l-1 imidazole HCl, 2 mmol l-1 MgCl2, 5
mmol l-1 ethylene diamine tetraacetic acid (EDTA), 1 mmol
l-1 reduced glutathione and 0.1% Triton X-100, pH 7.5, using a
Polytron homogeniser (Brinkmann Instruments, Switzerland) for three 20 s
periods. The samples were maintained on ice during and between periods of
homogenisation.
Enzyme activity assays
All enzyme activities, except for creatine kinase, were measured according
to Couture et al. (1998). For
creatine kinase (E.C.2.7.3.2CK), the reaction mixture contained: 75 mmol
l-1 Tris-HCl, 5 mmol l-1
MgCl2.6H2O, 4 mmol l-1 glucose, 0.75 mmol
l-1 ADP, 5 mmol l-1 AMP, 0.3 mmol l-1 NADP,
24 mmol l-1 phosphocreatine (omitted in control), hexokinase and
glucose-6-phosphate dehydrogenase in excess, pH 7.6. Activities are expressed
in international units (i.u.; µmol substrate transformed to product
min-1 g-1 tissue wet mass. Muscle enzyme activities were
measured in the order: PFK, PK, CK, LDH, CS, CCO and NDPK. All assays were run
in duplicate.
Concentration of muscle protein, glycogen, lactate and muscle water
content
Protein concentration in muscle extracts was measured using bicinchoninic
acid (Smith et al., 1985).
Muscle water content was determined after drying 2 g of muscle for 48 h at
60°C. Glycogen content was measured in muscle samples taken at the time of
death (72 h after the end of the swimming tests). Lactate content was
determined on white muscle biopsies taken immediately after the endurance
test. Glycogen and lactate content were measured using the method of Keppler
and Decker (1974
).
Hematocrit
Hematocrit was determined on blood sampled immediately after death. Blood
was taken directly from the heart cavity with a heparinised microhematocrit
tube and centrifuged for 10 min using an Adams Autocrit minicentrifuge
(Clay-Adams Inc., New York, USA).
Calculations and statistical analysis
Length and total mass were used to calculate a condition factor [CF = (mass
x fork length-3)x100, where somatic mass is in g and
fork length in cm]. Somatic mass was calculated by substracting gonad mass and
stomach contents from the total mass of the fish. Liver and gonads were
weighed to calculate the hepatosomatic index HI (liver mass / somatic mass)
and the gonadosomatic index GI (gonad mass / somatic mass)
(Table 1). Individual growth
rates (% day-1) were calculated using the following equation:
![]() | (1) |
We used JMP 3.2.1 (SAS Institute Inc., Duxbury Press, USA, 1996) to examine the effect of feeding treatment and site of sampling (with repeated measures on individual fish) on enzyme activity, protein, glycogen and water contents. In these models, feeding treatment was a factor, sampling site was nested within fish and fish was nested within feeding treatment. An interaction term between feeding treatment and sampling site was included. Enzyme activity, protein, glycogen and water contents were the variables. These models were run separately for red and white muscle. Differences were considered significant at P=0.05. The a posteriori `add contrasts' function was used to establish differences due to feeding treatment at each sampling site. Longitudinal differences in enzyme activity were examined within each feeding group, using models in which site of sampling was the factor and a posteriori comparisons established specific differences.
Failure time analysis was used to assess the effect of the variables on
swimming endurance (Winger et al.,
1999,
2000
). Given that cod swam for
a minimum of 20 min before reaching the target speed (1.8 BL
s-1), we used the time swum by fish from 0.5 BL
s-1 until exhaustion as the dependent variable. This allowed us to
include the six starved cod that did not attain the target speed. Time swum
was analysed using the Cox proportional hazards model
(Cox and Oakes, 1984
;
Winger et al., 1999
). Due to
the large number of variables, as well as their probable colinearity, we
preselected variables before their inclusion. First, failure time analyses
were performed for each variable to identify those that showed a significant
(P<0.15) relationship with the endurance hazard rate. A stepwise
failure time analysis was then performed on these selected variables. The
criterion for entry and removal of a variable into the model was the
significance of the
2 score statistic (P<0.05 to
stay in the model). Once the model was built, we checked the colinearity
between the remaining variables, removing variables with marked colinearity
(statistical condition index >30). Models were built using the PHREG
procedure and colinearity was analysed using the REG procedure in SAS system
6.12 (SAS institute Inc., Cary, NC, USA, 1996-1999).
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Results |
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Effects of feeding regime on biochemical parameters
The impact of starvation upon enzyme levels was more pronounced in white
than in red muscle (Figs 2,
3). Starvation significantly
decreased the activity of all enzymes measured in white muscle
(P<0.0001). This effect was greater for the glycolytic than the
mitochondrial enzymes (58-86% reductions for the former versus 40-59%
decreases for the latter). The decrease in NDPK activity was intermediate. The
site of sampling affected the activity of several enzymes
(P<0.05), particularly in fed cod; PFK and LDH were higher in the
last third of the body while NDPK showed the opposite pattern. As starvation
attenuated the effect of position, an interaction between feeding regime and
site of sampling in white muscle was observed for PFK, PK, CK, LDH
(P<0.05) and NDPK (P=0.0001). CCO activities in white
muscle increased from head to tail in starved cod. Starvation significantly
reduced the activity of the enzymes measured in red muscle
(Fig. 3) (PFK, PK, CK and LDH:
P<0.0001; CS, P=0.0103; CCO, P=0.0241; NDPK,
P=0.0013), but the changes were smaller than in white muscle. Again
decreases were more pronounced for glycolytic than mitochondrial enzymes
(28-67% for glycolytic enzymes versus 1.5-30% for mitochondrial
enzymes) and NDPK was intermediate (0.6-30%). In red muscle, strong
longitudinal differences were found for the mitochondrial enzymes, while the
longitudinal differences for glycolytic enzymes were less pronounced. For both
starved and fed cod, the activity of CCO, CS and CK differed with the site of
sampling (P<0.01). For PK and NDPK an effect of position was only
apparent in fed cod (interaction between site and feeding treatment,
P<0.05), whereas for LDH the effect was only apparent in starved
cod. In red muscle sampled behind the head and at the middle of the body, the
activity of the mitochondrial enzymes was not reduced by starvation. Red
muscle NDPK levels were only affected by starvation in the sample taken behind
the head.
|
|
Starvation decreased protein concentrations by up to 15% in white muscle (P=0.0003) and up to 19% in red muscle (P<0.0001). The site of sampling only affected protein concentration in red muscle of starved cod (Fig. 4).
|
In both red and white muscle and at each site of sampling, glycogen and water content changed with feeding (P<0.0001) (Fig. 5). Glycogen concentrations were higher in red than white muscle (P<0.0001). Glycogen content in white muscle was up to 12 times higher in fed than starved cod, whereas in red muscle this difference was sixfold. In red and white muscle, decreases in glycogen content were similar at the three sampling sites and glycogen levels did not differ with sampling site. On the other hand, water content changed with site of sampling in both muscles, particularly in fed cod. Significant interactions between feeding regime and the site of sampling were only observed for water content in red muscle (P=0.006).
|
White muscle lactate concentration at the end of the endurance tests was 1.6 times higher in fed than in starved cod (P=0.036) (Fig. 6). A similar result was found for the burstcoast movements during the tests (2.5 times; P<0.0001). However, burstcoast movements were not correlated with lactate concentration in either group (P=0.16). The time and distance swum were 3.4- and 4.7-fold higher in fed than starved cod (time swum, P=0.022; distance swum, P=0.019) (Fig. 7).
|
|
Determinants of swimming performance
Of 33 cod, 6 did not achieve the target speed, 24 became exhausted during
the test and 3 swam to the end. Although we had more females than males, and
although females were slower than males, sex did not affect the time swum
(P>0.05). Of all the variables included in the failure time
analyses, only three were significant determinants of the time cod swam and
explained 87% of the variance: (i) the number of burstcoast movements,
(ii) LDH activity in white muscle at the caudal peduncle, and (iii) CCO
activity in white muscle at the caudal peduncle. Of these variables, the
number of burstcoast movements was the most important
(P<0.0001, r2=0.81) and positively influenced
the time swum. LDH in the caudal white muscle samples was next in importance
(P=0.0002) and the mitochondrial enzyme, CCO, in caudal white muscle
was third (P=0.02) (Table
2). Because we were interested in identifying the biochemical or
morphological variables that explain the length of time that cod were able to
swim, we constructed a model without burstcoast movements. This model
showed that condition factor and heart mass explained 60% of the variability
of the length of time swum by cod. Condition factor was positively related
(P<0.0001, r2=0.41), while heart mass was
negatively related to time swum (P=0.0014,
r2=0.18) (Table
3).
|
|
Given that the number of burstcoast movements was a major determinant of cod endurance, we constructed a model to examine which biochemical or morphological variables could explain the number of burstcoasts made by the fish during prolonged swimming. This model showed that the condition factor (P<0.0001, r2=0.54), gill arches (P=0.004, r2=0.10) and PFK activity in caudal samples of red muscle (P=0.03, r2=0.05) explained 69% of the variability of this swimming pattern. The condition factor and PFK activity positively influenced burstcoast movements whereas the gill arches were negatively linked with these movements (Table 4).
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Discussion |
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Starvation had a greater impact upon glycolytic than mitochondrial enzymes,
particularly in white muscle. Our results confirm those reported for plaice
and cod (Moon and Johnston,
1980; Martínez et al.,
2002
). In the present study, we extend this pattern to red muscle
of cod, in which starvation led to marked reductions in glycolytic enzyme
activities while leaving mitochondrial activities virtually unchanged.
Further, starvation led to the virtual disappearance of the longitudinal
variation of glycolytic enzyme activities in white muscle but only slightly
attenuated positional differences in mitochondrial enzyme activities in red
muscle.
The pronounced impact of energetic condition upon muscle metabolic
capacities allowed us to demonstrate that capacities of white fibres are
central determinants of prolonged swimming performance. The endurance of cod
was most closely linked with the number of burstcoast movements during
the swimming tests. Burstcoast swimming is considered an intermittent
(unsteady) swimming behaviour, powered by white fibres. Webb
(1994) suggests that it may be
used as a gait during swimming over a portion of an individual's performance
range or as a method to conserve energy at prolonged swimming speeds.
Theoretical modelling suggests that burstcoast swimming is up to 2.5
times less costly than steady swimming
(Videler and Weihs, 1982
).
This swimming behaviour is observed in cod during Ucrit
protocols (Nelson et al.,
1994
,
1996
;
Reidy et al., 2000
). Our
results confirm that during aerobic exercise (i.e. sustained swimming), fish
are able to recruit white fibres (Rome,
1992
; Burgetz et al.,
1998
). Further, we found that swimming endurance was significantly
related to the activity of CCO and LDH in caudal samples of white muscle. As
most of the cod's muscle mass is composed of white fibres, their use during
endurance swimming would appear to be advantageous.
Given the central role of burstcoast movements in endurance
swimming, we examined the determinants of this swimming behaviour. Cod with
higher condition factors and higher red muscle PFK activity performed more
burstcoast movements, whereas those with larger gill arches performed
fewer burstcoast movements. Heart mass, which was closely related to
gill arch mass, was also negatively linked with burstcoast movements.
These relationships suggest a compromise between aerobic performance and
anaerobic burstcoast swimming such as found by Reidy et al.
(2000). As starvation only had
a limited impact on gill arch and heart size, but markedly reduced condition
factor and muscle enzyme activities, the trade-off between aerobic and
anaerobic swimming capacities should be independent of feeding status. In
agreement with this, negative relationships between burstcoast
movements and gill arch mass (or heart mass) were observed in both treatment
groups, which leads to the apparent paradox that cod with better capacity for
oxygen uptake and distribution actually showed decreased prolonged swimming
capacity, due to reduced reliance upon burstcoast movements.
Muscle activity changes from front to rear during swimming
(Jayne and Lauder, 1995;
Thys, 1997
). Rostral muscle
fibres generate power while shortening, whereas caudally active fibres resist
stretching (negative work). The duration of the activity of the rostral fibres
is longer than that of caudal fibres, but the time of relaxation of caudal
white muscle fibres is slower than that of rostral ones. On the other hand,
the rate at which caudal muscle relaxes is critical, because while ensuring
force transmission during stretching, this rate determines the overall thrust
produced by the tail region, which ultimately affects the performance of the
whole organism (Swank et al.,
1997
). Thus, maximum tail beat frequency depends largely on the
properties of the caudal fibres. Our results show that caudal muscle fibres
have a high capacity for power generation. Given the decrease in fish muscle
mass approaching the tail as well as the central role of these fibres in force
transmission, it is crucial to maintain a high capacity for caudal power
development. This may explain why enzyme activities in the caudal samples of
white and red muscle were correlated with swimming endurance.
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Acknowledgments |
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