Thermal plasticity of skeletal muscle phenotype in ectothermic vertebrates and its significance for locomotory behaviour
Gatty Marine Laboratory, School of Biology, University of St Andrews, St Andrews, Fife KY16 8LB, Scotland, UK
*
e-mail:
iaj{at}st-and.ac.uk
(web-site:
http://www.st-and.ac.ukfmrg
)
Accepted 13 May 2002
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Summary |
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Key words: temperature acclimation, muscle fibre type, phenotypic plasticity, ectotherm, locomotion
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Introduction |
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The nature and magnitude of temperature acclimation responses observed at
the whole-animal level and the underlying mechanisms at lower levels of
organisation vary among species and during ontogeny, probably reflecting
differences both in ecology and in habitat temperatures
(Wakeling et al., 2000;
Cole and Johnston, 2001
).
Relatively little is known about the evolutionary significance of temperature
acclimation responses. It has often been assumed that acclimation responses
are adaptive and enhance the fitness of an organism in its new environment,
the so-called `beneficial acclimation hypothesis'
(Leroi et al., 1994
;
Huey and Berrigan, 1996
). Yet
several studies that have set out to test this hypothesis have rejected it
(Leroi et al., 1994
;
Zamudio et al., 1995
;
Bennett and Lenski, 1997
;
Gibbs et al., 1998
;
Huey et al., 1999
). However,
many of these studies have examined acclimation during early development,
leading to some discussion of the validity of the tests because of the
confounding effects of developmental plasticity
(Wilson and Franklin,
2001
).
For many organisms, locomotion is the key to survival. It provides prey,
enables migration and facilitates mating and the avoidance of predators. The
majority of studies on skeletal muscle performance have focused on the two
main types of muscle fibres, fast- and slow-twitch. The fast muscle fibres are
generally recruited for high-force, anaerobic activities such as prey capture
and escape responses, whilst the slow fibres are recruited during low-force
contractions (Bone, 1966;
Josephson, 1993
). Many studies
have used forced exercise models to investigate the thermal plasticity of
sustained activity involving flumes (e.g.
Fry and Hart, 1948
;
Johnston, 1993
;
Rome and Swank, 2001
) or
treadmills (Feder, 1986
).
However, during foraging, many ectotherms utilise intermittent patterns of
locomotion in which pauses significantly increase the detection rates of prey
items (Getty and Pulliam,
1991
). Responsiveness to external stimuli during escape behaviour
is also a function of acclimation temperature
(Tiiska and Lagerspetz, 1999
).
It is therefore important to consider the sensory and brain function in
addition to motor processes to evaluate the behavioural significance of
temperature acclimation responses.
In this review, we consider the relationship between the thermal plasticity of muscle phenotype and locomotory performance at the whole-animal level in ectothermic vertebrates and discuss the variety and evolutionary significance of the responses observed. Unfortunately, integrative studies at the gene, protein, muscle and whole-animal level are rare. Even those investigations focused on one or more levels of organisation are restricted to a relatively few species.
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Integrative approaches for investigating the thermal plasticity of locomotor performance |
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Biomechanics the work loop technique
The work loop technique, developed by Machin and Pringle
(1959), is the main approach
used to investigating the biomechanics of muscle under conditions simulating
normal locomotion. In some cases, muscles undergo cyclical length changes at a
constant frequency. In a classic paper, Josephson
(1985
) studied one such case,
the synchronous muscle of a moth, and exploited the work loop technique to
estimate the power requirements of flight. Isolated fibre bundles were
subjected to sinusoidal length changes at 25 Hz, corresponding to the wingbeat
frequency at 30°C, and the muscle was phasically stimulated during each
length change cycle. By optimising the strain and phase of stimulation,
Josephson (1985
) was able to
estimate the power output by plotting muscle force against fibre length to
produce a work loop. The area of the loop represents the work performed during
shortening minus the work put into the muscle during the lengthening phase.
The mechanical power output was calculated as the net work per cycle
multiplied by the frequency.
Altringham and Johnston
(1990) used the same approach
to investigate the performance of isolated slow and fast muscle fibres in the
short-horn sculpin Myoxocephalus scorpius over the range of
frequencies used during (steady) swimming. The number and timing of stimuli
were adjusted at each cycle frequency to maximise power output at 5°C.
Slow and fast muscle fibres produced their maximum power outputs of 5-8 and
25-35 W kg-1 wet muscle mass at 2 and 5-7 Hz, respectively. In the
case of the slow muscle, its contraction kinetics was too slow to generate any
positive work above 8Hz. This study illustrated why it is necessary to have
muscle fibre types with a spectrum of contraction kinetics for locomotion over
a wide range of speeds. The intrinsic unloaded shortening speed
(Vmax) is an important parameter because the ratio of
shortening speed (V) to Vmax determines the force
generated. Potentially, activation times, relaxation rates,
Vmax and the duration and phase of stimulation all
contribute to the shape of the work loop obtained and, hence, to the power
delivered by the muscle (Josephson,
1993
).
In vivo muscles may not function under the conditions required for
maximum power generation. Rome and Swank
(1992) optimised work loop
parameters for red myotomal muscle in the scup (Stenotomus chrysops
L.) at 20 and 10°C. At 20°C, maximum power output was 27.9 W
kg-1 wet muscle mass at 5Hz compared with 12.8 W kg-1
wet muscle mass at 2.5Hz at 10°C, resulting in a Q10 of 2.2.
Using the sarcomere length changes and tailbeat frequencies measured for scup
during steady swimming, it was concluded that the red muscle probably produces
close to its optimum power at 20°C. In contrast, although the optimum
frequency at 10°C was 2.5Hz, scup do not swim at such low tailbeat
frequencies. Thus, it is important to consider the actual constraints under
which the muscle is operating in vivo to assess performance at
different temperatures and/or acclimation states.
The trend over the last 10 years has been to combine work loop experiments
with studies of whole-animal performance to provide more realistic values of
muscle strain and stimulation patterns
(Josephson, 1993;
Franklin and Johnston, 1997
;
James and Johnston, 1998
;
Swank and Rome, 2001
). Several
approaches are available for relating muscle function to body movements.
Sarcomere length changes can be either calculated from changes in limb angles
or body shape (e.g. Rome and Sosnicki,
1991
) or measured directly using surgically implanted
sonomicrometry crystals (Franklin and
Johnston, 1997
; James and
Johnston, 1998
). The distance between two piezoelectric crystals
during lengthening and shortening of the muscle is recorded using alterations
in the transit time of ultrasound. Sonomicrometry can be synchronised with
electromyographic (EMG) electrodes, which provide information on the phase and
duration of muscle activation.
Fish swimming involves alternate contractions of serially arranged
myotomes, which have a complex internal and external geometry that varies
along the length of the trunk (van
Leeuwen, 1999). EMG duty cycle and the timing of muscle activation
vary along the body and between fibre types (Coughlin and Rome, 1990). The use
of in vivo parameters of muscle strain and stimulation in work loop
experiments enables the role of muscles at different body positions to be
investigated. In several species, muscle fibres in myotomes towards the caudal
fin were activated earlier in the cycle than more anterior muscles, resulting
in force generation during lengthening for both steady swimming
(Altringham et al., 1993
) and
fast-starts (Johnston et al.,
1995b
; Wakeling et al.,
1999
). As a result, the muscle initially does negative work, but
the resulting increase in stiffness is thought to play a role in power
transmission down the trunk. Elastic energy storage is probably important in
most locomotory activities, particularly during running and jumping in
terrestrial animals (Biewener and Roberts,
2000
). In work loop experiments, muscle fibres are usually
attached so as to minimise the influence of serial elastic structures such as
tendons, and this is a potential limitation of such experiments.
Whole-animal performance
In fish, locomotory performance is usually studied using high-speed
cinematography or video films enabling the velocity and acceleration during
steady swimming or fast-starts to be determined. More recent studies have
examined the velocity of the wave of curvature travelling down the body of the
fish because this is linked to the speed of swimming, particularly during
fast-starts (Wakeling and Johnston,
1998; Temple et al.,
2000
). The power for swimming is generated by the muscles.
Estimates of the hydrodynamic power requirements for swimming can therefore be
used to predict a minimum value for muscle power output
(van Leeuwen et al., 1990
;
Frith and Blake, 1995
;
Wakeling and Johnston, 1998
;
Wakeling et al., 1999
).
Values of predicted muscle power requirements using this approach have been
found to correlate well with measurements of power output involving work loop
experiments (Wakeling and Johnston,
1998
; Temple et al.,
2000
).
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Short-term responses to temperature change |
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In a study with common carp subjected to forced exercise, it was shown that
the threshold speed at which fast muscle fibres were first recruited decreased
as the temperature was lowered (Rome et
al., 1984). Thus, over the short term, the carp were able to
achieve the same level of performance by recruiting faster-contracting muscle
fibre types, but at the expense of relatively rapid fatigue. In the scup, pink
muslce, which has a faster relaxation rate and is active for a shorter time
than the red muscle, was found to be recruited at lower swimming speeds
following an acute drop in temperature
(Rome et al., 2000
). The
effects of an acute decrease in temperature on fast-start performance have
also been studied in detail for the common carp
(Wakeling et al., 2000
). At
low temperatures, the magnitude of body bending, muscle strain and contraction
duration all increased, and this was associated with a lower hydrodynamic
efficiency (Wakeling et al.,
2000
).
The reduced locomotory performance of some anuran amphibians at low
temperature is also at least partially explained by a decrease in muscle power
(Hirano and Rome, 1984;
John-Alder et al., 1989
).
However, in the frog Rana temporaria, the Q10 for both
jump take-off velocity and mean swimming velocity was shown to be lower than
the Q10 for muscle power output determined from work loop
experiments (Navas et al.,
1999
). The mean muscle power output during take-off at 10°C
was only 34% of the calculated requirements for the whole animal, suggesting
the involvement of the storage of elastic strain energy
(Navas et al., 1999
), as has
been suggested for the Cuban tree frog Osteopilus septentrionalis
(Peplowski and Marsh, 1997
).
Short-term changes in acidbase balance following a temperature change
have the potential to affect muscle performance. Boutilier et al.
(1987
) reported nonlinear
changes in intracellular pH (pHi) with temperature (T) in various
striated muscles of the toad Bufo marinus, equivalent to a
pHi/
T of -0.14 to -0.023°C min-1 over
the range 10-30°C. Renaud and Stevens
(1984
) working with isolated
sartorius muscle from Bufo bufo, calculated that the predicted change
in intracellular pH on cooling from 25 to 5°C was sufficient to increase
maximum force and, hence, power during isotonic shortening, perhaps providing
a short-term mechanism for compensation to low temperature.
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Seasonal acclimatisation of muscle phenotype and locomotory behaviour |
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Fish
During the adaptive radiation of the teleosts, temperature acclimation
responses in muscle have presumably evolved independently on numerous
occasions, and a diversity of molecular mechanisms is therefore to be
expected. It is important to include a phylogenetic perspective in analysing
the thermal plasticity of locomotory behaviour in terms of the underlying
physiological and molecular mechanisms, although such an approach has rarely
been adopted in the literature.
Cypriniformes
Cypriniformes of the genus Cyprinus and Carassius (Family
Cyprinidae) are temperate freshwater fish with a wide geographic distribution
in temperate regions. Fry and Hart
(1948) were among the first to
document the remarkable thermal plasticity of swimming performance in the
goldfish (Carassius auratus L.) on the basis of experiments in a
rotating chamber. Goldfish were acclimated to different temperatures for
several weeks prior to measuring maximum sustained cruising speed over a 2 min
period at a range of temperatures (5-35°C). It is likely that both slow
and fast muscle fibres would have made significant contributions to total
power requirements in these experiments. Acclimation to a higher temperature
extended the thermal range for activity and shifted the optimum temperature
for performance (Fig. 2). Cold
acclimation improved locomotory performance at low temperatures but was
associated with a marked trade-off in performance at high temperatures and
vice versa (Fig. 2).
The relationship between test temperature and the maximum swimming speed over
the first two tail beats of an escape response in goldfish acclimated to
either 10 or 35°C is shown in Fig.
3A. Escape responses are probably exclusively powered by
contraction of the fast myotomal muscle.
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Several weeks after transfer from 20 to 10°C, the swimming speed at
which common carp first recruit their fast muscle fibres increased relative to
that of fish acutely exposed to 10°C
(Rome et al., 1985). Similar
results were obtained in striped bass (Morone saxatilis) swimming at
15°C, resulting in a threshold speed for fast muscle recruitment of 2.46
L s-1 in 9 °C-acclimated individuals and 1.84
L s-1 in 25 °C-acclimated individuals
(Sisson and Sidell, 1987
),
where L is body length. In both these species, the relationship
between tailbeat frequency and swimming speed was independent of acclimation
temperature (Sissons and Sidell,
1987
; Rome et al.,
1985
).
The increased swimming speed at which fast muscle fibres are first
recruited following cold acclimation partly reflects a greater volume of red
muscle, largely due to an increase in the number of slow fibres: goldfish
(Johnston and Lucking, 1978);
striped bass (Jones and Sidell,
1982
). Temperature acclimation responses are reversible and
involve changes in the contractile and metabolic phenotype of individual
fibres. For example, Langfeld et al.
(1991
) found that red pectoral
fin adductor muscle fibres in the common carp expressed exclusively slow-type
myosin light chain isoforms at an acclimation temperature of 20 °C, but a
significant proportion of fast myosin light chains at an acclimation
temperature of 8 °C. Maximum shortening velocity
(Vmax) was 17 % higher at 8 °C in the cold- than in
the warm-acclimated fish, and this was probably attributable to the expression
of fast myosin light chains in slow muscle since there was no evidence for
changes in myosin heavy chain composition
(Langfeld et al., 1991
).
In goldfish and common carp, the contractile performance of fast muscle
fibres is improved at low temperatures following cold acclimation. Johnston et
al. (1975) found that
Mg2+-Ca2+-activated fast muscle myofibrillar ATPase
activity was higher at all assay temperatures in 1 °C- than in 26
°C-acclimated goldfish. Cold-acclimation was also associated with an
increased susceptibility of the ATPase activity of isolated myofibrils to
denaturation at 37 °C, suggesting changes in the tertiary structure of
myosin. Similar changes in myofibrillar ATPase activity with temperature
acclimation were subsequently reported for common carp
(Hwang et al., 1990
) and for
several other cyprinid species (Heap et
al., 1985
). Experiments with skinned muscle fibres showed that
both maximum force production and maximum shortening velocity increased at low
temperatures following cold acclimation in both slow and fast muscle types in
the common carp (Johnston et al.,
1985
). Changes in the relative proportion of myosin light chain 3
(LC3f) to myosin light chain 1 (LC1f) with acclimation
temperature are thought to contribute to the observed adjustments in
Vmax of fast muscle fibres
(Crockford and Johnston,
1990
). The molar ratios of LC3f/LC1f mRNAs
were significantly higher in 30 °C- (3.93) than 10 °C-acclimated
(3.10) carp (Hirayama et al.,
1997
). In addition, Hirayama et al.
(1998
) found two types of mRNA
encoding myosin regulatory light chain in carp fast skeletal muscle that had
different numbers of polyadenylation signals prior to the poly(A) tail and
showed altered expression following temperature acclimation.
Watabe and co-workers have elegantly shown that fast muscle contains
multiple isoforms of myosin heavy chain and that their relative proportions
change with acclimation temperature
(Watabe et al., 1995). Imai
et al. (1997
) isolated cDNA
clones encoding light meromyosin (LMM) from 10 °C-, 20 °C- and 30
°C-acclimated carp. The type of mRNA transcribed and the proportions of
each isoform were found to be a function of acclimation temperature
(Imai et al., 1997
). In spite
of the 95.6 % identity between the 10 °C- and 30 °C-type LMM isoforms
(Imai et al., 1997
), there
were marked differences in thermodynamic properties
(Nakaya et al., 1997
), which
are thought to reflect amino acid substitutions in the C-terminal half of the
LMM (Kakinuma et al., 1998
).
Kakinuma et al. (1998
)
suggested that the lower thermostability of the 10 °C-type LMM would aid
energy transduction from the S1 heads to the thick filaments, thus
facilitating contraction in cold-acclimated carp. Hirayama and Watabe
(1997
) also found isoform
differences in the first 60 amino acid residues from the N terminus in the
crossbridge head of myosin subfragment-1.
In common carp, acclimation from 20 to 8 °C was shown to result in an
increase in the rate of relaxation of the fast muscle fibres at 8 °C
(Johnston et al., 1990). This
was associated with an increase in the activity of sarcoplasmic reticulum (SR)
Ca2+-ATPase but no change in the surface or volume density of SR
vesicles (Fleming et al.,
1990
) or the pCa/tension relationship of skinned muscle fibres
(Johnston et al., 1990
).
Although adjustments to relaxation rate with cold acclimation are apparently
common, there appear to be several ways in which this can achieved
(Table 1). For example, in
goldfish, the surface density of SR was found to be significantly higher in
fish acclimated to 5°C than in those acclimated to 0°C (Penney and
Goldspink, 1990). In the closely related crucian carp Carassius
carassius, the specific activity of SR Ca2+-ATPase was
increased following acclimation from 22 to 2°C, but the amount of enzyme
was reduced, resulting in no net change in activity
(Vornanen et al., 1999
). The
extent to which these different findings represent genuine species differences
in the mechanism of the acclimation response or simply reflect variations in
acclimation conditions remains to be ascertained.
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Johnson and Bennett (1995)
compared temperature acclimation responses in the goldfish and the killifish
(Fundulus heteroclitus) at the biochemical, cellular and whole-animal
levels of organisation in the same set of experiments. When tested at
10°C, goldfish acclimated to 10°C showed a six- to eightfold increase
in the speed (Fig. 3A) and
turning velocity of fast-start escape responses compared with fish acclimated
to 35°C. This was associated with altered myosin heavy chain isoform
expression, a fivefold increase in fast muscle myofibrillar ATPase activity
and a 100% decrease in isometric twitch contraction time
(Table 1). In contrast, the
killifish showed no changes in MyHC isoform expression and a much more modest
increase in ATPase activity (55%) and decrease in twitch contraction time
(35%) following acclimation to the same temperature. Temperature acclimation
modified the relationship between maximum swimming speed and test temperature
in a similar fashion in the two species, although the magnitude of the
response was much smaller in the killifish
(Fig. 3A,B). The Q10
for maximum velocity in C-start behaviour in 35°C-acclimated fish,
calculated over the range 10-35°C, was substantially lower (1.2) in the
killifish than in the goldfish (2.0)
(Johnson and Bennett, 1995
).
The much better coldwater performance of the killifish than of the goldfish
following acute temperature transfer in 35°C-acclimated individuals was
therefore associated with a smaller temperature acclimation response at the
tissue level.
Juvenile and adult stages of common carp can survive overwintering in
ice-covered ponds, whereas the embryonic stages require a minimum temperature
of at least 15°C to pass through normal development. Common carp spawn in
the summer at or above 20°C, and the cold-tolerance of the larvae and
early juveniles gradually increases as the season progresses. To investigate
the development of the acclimation response, Wakeling et al.
(2000) reared one group of
carp larvae at a constant temperature of 21°C and cooled other groups to
either 8 or 15°C with a time course that mimicked seasonal cooling.
Fast-start performance and fast muscle myofibrillar ATPase activity were found
to be independent of acclimation temperature in carp less that 37 mm in total
length (TL). In carp, greater than 37 mm TL, acclimation to
8°C resulted in an increase in myofibrillar ATPase at all assay
temperatures. The MyHC peptide map characteristic of cold-acclimated adult
stages was also not observed until 37 mm TL in the 8°C group
(Fig. 4).
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Cole and Johnston (2001)
used a statistical model to compare the time course of the change in fast
muscle myofibrillar ATPase activity in fry with mean starting total lengths of
30 and 44 mm. A significant increase in myofibrillar ATPase activity was
observed after 2-3 weeks in the 44 mm group, but not until 4-5 weeks in the 30
mm group after they had reached 37 mm TL. The development of the
temperature acclimation response for myofibrillar ATPase and MyHC expression
appears to be a function of maturity state and is presumably established prior
to the onset of the first winter (Cole and
Johnston, 2001
).
Scorpaeniformes
The short-horn sculpin (Myoxocephalus scorpius) and long-spined
sea scorpion (Taurulus bubalis) (Family Cottidae) are shallow-water,
temperate, marine teleosts. Adult short-horn sculpin are usually found at a
depth of 30-50 m, where temperatures follow seasonal means, whilst juveniles
and all stages of long-spined sea scorpion are found in the more variable
thermal environment associated with rock pools and the shallow sublittoral
zone (Foster, 1969;
King and Fives, 1983
). In St
Andrews Bay, Scotland, the typical mean winter and summer sea temperatures are
5 and 15°C respectively (Beddow et al.,
1995
). The ability to modify escape performance following
acclimation to the mean winter and summer temperatures was found to vary
during ontogeny in the short-horn sculpin but not in the long-spined sea
scorpion, perhaps reflecting differences in thermal niche distributions
between these two closely related Cottidae species
(Temple and Johnston,
1998
).
Acclimation to a winter temperature of 5°C significantly improved escape performance in long-spined sea scorpion measured at 0.8°C (Fig. 3C), whereas 60% of fish acclimated to 15°C could not swim at this temperature. The velocity of the wave of curvature passing down the body was also calculated, and this was higher at 0.8°C but lower at 20°C in 5°C-acclimated than in 15°C-acclimated fish, indicating a trade-off in performance at high and low temperatures (Fig. 5A-C). Estimates of the useful hydrodynamic power output per unit muscle mass in the direction of travel, calculated from the inertial power requirements, were also significantly affected by acclimation state and were 32% higher at 0.8°C in 5°C- than in 15°C-acclimated fish (Fig. 5D). In contrast, predicted power requirements at 20°C (98 W kg-1 wet muscle mass) were 90% higher in 15°C- than in 5°C-acclimated fish (Fig. 5D).
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In contrast, in the short-horn sculpin, maximum length-specific speed
during escape responses was only significantly different between acclimation
groups at a test temperature of 20°C
(Fig. 3D). For fast-starts
filmed during prey capture, the maximum speed in the direction of the attack
was 33% greater and the tailbeat duration of the propulsive stroke was 37%
shorter at 15°C in 15°C- than in 5°C-acclimated short-horn sculpin
(Beddow et al., 1995). The
improvement in locomotory performance at 15°C was sufficient to increase
the percentage of successful predation from 23.2 to 73.4% in summer-compared
with winter-acclimatised animals (Beddow et
al., 1995
). However, acclimation from 15 to 5°C had little
impact on fast-start performance at 5°C
(Beddow et al., 1995
;
Temple and Johnston,
1998
).
Plasticity of swimming behaviour in short-horn sculpin is associated with
adaptations in the biomechanics of isolated muscle fibres. Johnson and
Johnston (1991) used the work
loop technique to investigate the maximum power output of fast muscle during
sinusoidal muscle length changes in winter- and summer-caught fish. Following
optimisation of the strain and stimulation parameters, the mean power output
delivered per cycle by the muscle at 15°C was more than twice as high in
summer-caught (30 W kg-1 wet muscle mass) as in winter-caught (9 W
kg-1 wet muscle mass) short-horn sculpin, largely because of an
increase in force during the shortening phase of the cycle
(Fig. 6A). Temple et al.
(2000
) used in vivo
information on muscle strain and the timing and duration of stimulation during
fast-starts (Fig. 6B) in
conjunction with work loop experiments with isolated muscles and obtained
broadly similar results, although somewhat higher absolute values of power
(Fig. 6C). At 15°C, the
maximum instantaneous power delivered by the fast fibres was 275.6 W
kg-1 wet muscle mass in 15°C-acclimated fish compared with
178.5 W kg-1 wet muscle mass in 5°C-acclimated fish
(Fig. 6D). In contrast,
contractile performance at 5°C was relatively independent of temperature
acclimation state, as was found for locomotory behaviour
(Fig. 6A,C,D).
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Vmax and the unloaded contraction velocity of skinned
fast-muscle fibres were 2.4 and 2.8 times higher, respectively, measured at
15°C in 15°C- than in 5°C-acclimated short-horn sculpin
(Beddow and Johnston, 1995;
Ball and Johnston, 1996
). In
contrast to temperature acclimation in common carp and goldfish,
two-dimensional gel electrophoresis and peptide mapping of purified fast
muscle myosin heavy chains revealed no myofibrillar isoforms unique to
5°C- and 15°C-acclimated fish and no change in myofibrillar ATPase
activity (Table 1). The molar
ratio of myosin light chain isoforms (LC3f:LC1f)
determined by capillary electrophoresis was significantly lower in fast muscle
from 15°C-acclimated (0.73) than from 5°C-acclimated fish (1.66)
(Ball and Johnston, 1996
).
Thus, adjustments in muscle shortening velocity at high temperatures following
summer acclimatisation in sculpin are probably achieved via changes
in the expression of myosin light chain isoforms
(Table 1).
Salmoniformes
The salmoniformes are a diverse group of mostly northern-hemisphere
freshwater or andromous fishes. Johnson et al.
(1996) investigated muscle
protein composition, contractile properties and fast-start performance in
rainbow trout (Oncorhynchus mykiss) acclimated to either 5 or
20°C for 4 weeks. Acclimation from 5 to 20°C produced no statistically
significant effect on maximum linear swimming velocity at 20°C and
resulted in only small improvements in distance moved in 40 ms (24 %) and in
angular velocity (15 %). There were no changes in the expression of the myosin
heavy chains or myofibrillar ATPase activity with acclimation. Only a minor
decrease in fast muscle twitch contraction time (11 %) was found following
acclimation to 5°C (Table
1). Interestingly, however, the myofibrillar ATPase activity
became less resistant to thermal denaturation at high temperatures following
warm-acclimation, although the mechanism was not investigated. The
Q10 for the maximum velocity of fast-starts was only 1.2 in rainbow
trout (Johnson et al., 1996
),
a value similar to that reported for the killifish
(Johnson and Bennett, 1995
).
The mechanistic basis of the low thermal dependence of locomotion in certain
species and its relationship to the magnitude of the temperature acclimation
response is a promising area for future research.
Perciformes
The Perciformes, as currently recognised, represent the largest and most
diverse order of vertebrates; they are found in almost every aquatic habitat
from the poles to the equator and include both eurythermal and stenothermal
species. Rome and Swank (2001)
investigated the recruitment of red muscle during steady swimming in scup
(Stenotomus chrysops) (family Sparidae) acclimated to either 10°C
(cold-acclimated) or 20°C (warm-acclimated) for 6 weeks. At 10°C, they
found that tailbeat frequency, muscle strain and stimulation phases were
independent of acclimation temperature, whereas the EMG duty cycle was
approximately 20% shorter in cold- than in warm-acclimated fish
(Table 1). In contrast, at
20°C, all the measured variables were similar between acclimation groups.
It was suggested that reductions in EMG duty cycle might result from altered
functioning of the pattern generator during cold-acclimation, indicating that
the nervous system has the ability to adjust to cold temperatures. In an
accompanying paper, work loop experiments were used to test the hypothesis
that the shorter stimulus duty cycle would increase muscle power output
(Swank and Rome, 2001
). The
results differed according to the anatomical position of the muscle along the
body. Integrated over the length of the fish, the power output at 10 °C
was 2.7, 8.9 and 5.8 times higher in cold- than in warm-acclimated fish
swimming at 30, 40 and 50 cm s-1, respectively. Temperature
acclimation had no effect on maximum tension, relaxation rate or unloaded
shortening speed, but resulted in an approximately 50 % faster activation rate
in cold- than in warm-acclimated individuals at 10 °C
(Table 1). By studying
cold-acclimated muscle under warm and cold in vivo acclimation
conditions, they were able to attribute 60 % of the improved power output to
adjustments in activation rate and 40 % to the reduction in stimulus duty
cycle. Such alterations following cold acclimation were thought also to
increase the efficiency of the muscle
(Swank and Rome, 2001
).
Amphibians
Studies on the thermal acclimatory capacity of amphibians at the levels of
the whole animal and isolated muscle indicate little or no phenotypic
plasticity to seasonal temperature change in most species
(Putman and Bennett, 1981;
Miller, 1982
;
Renaud and Stevens, 1983
;
Rome, 1983
;
Else and Bennett, 1987
;
Knowles and Weigl, 1990
).
However, Wilson and Franklin
(1999
) found that tadpoles of
the striped marsh frog (Limnodynastes peronii) acclimated to 10
°C for 6 weeks had maximum swimming speeds and accelerations at 10 °C
that were 47 % and 53 % higher, respectively, than those of tadpoles
acclimated to 24 °C. In contrast, the adult stages showed no temperature
acclimation response (Fig.
7A,B). Both tadpoles and adult stages of the fully aquatic
amphibian Xenopus laevis showed improvements in maximum swimming
performance following a period of temperature acclimation
(Fig. 7C,D). For example, the
minimum temperatures for burst swimming were 5 and 10 °C in tadpoles
acclimated to 12 and 30 °C, respectively. At 12 °C, maximum speed was
38 % higher in 12 °C- than in 30 °C-acclimated individuals.
Conversely, at a test temperature of 30 °C, the maximum swimming speed was
41 % faster in the warm- than in the cold-acclimated tadpoles, indicating a
trade-off between performance at high and low temperatures
(Wilson et al., 2000
). At 10
°C, the maximum swimming velocity of adults acclimated to 10 °C was 67
% faster than that of adults acclimated to 25 °C, although there was no
difference between acclimation groups at higher temperatures
(Fig. 7C,D). Isolated
gastrocnemius muscle fibres from adult X. laevis showed higher
tetanic tension and decreased relaxation times at 10 °C in 10 °C- than
in 25 °C-acclimated frogs, indicating some thermal plasticity of muscle
contractile properties (Wilson et al.,
2000
) (Fig. 7E).
One plausible hypothesis is that acclimation responses are observed only in
fully aquatic amphibians or tadpole stages that have sufficiently stable
temperature cues to initiate an acclimation response.
|
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Evolutionary significance of thermal plasticity of locomotion |
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Acclimation responses are usually tested by comparing the performance of
fish acclimated to a particular temperature with that of fish acutely
transferred to the same temperature over less than 24 h. In the case of
Cyprinus carpio, it would appear that quite large differences in
acclimation temperature were required to observe a modification in fast-start
performance at the whole-animal level. In contrast, differences in
myofibrillar ATPase activity and MyHC composition were apparent with smaller
differences between acclimation groups
(Wakeling et al., 2000).
Studies with skinned fibres isolated from fast muscle have shown that maximum
unloaded shortening speed and maximum tension generation vary continuously
with acclimation temperature (Crockford
and Johnston, 1990
). Thus, it seems that there are continuously
variable acclimation responses at lower levels of organisation, e.g. in MyHC
expression patterns and shortening speed, with a threshold for an observable
effect at the whole-animal level. This is perhaps not surprising given the
large number of energy-transfer steps between the mechanochemical transduction
of chemical energy by actomyosin ATPase and the transmission of thrust along
the surface of the body (Wakeling et al.,
2000
).
Nevertheless, the available evidence suggests that locomotory performance
is enhanced at least under some conditions following temperature acclimation.
Implicit in the `beneficial acclimation hypothesis' is the idea that
improvements in physiological variables following acclimation confer a fitness
advantage. Direct evidence for this supposition is somewhat limited with
regards to locomotory performance. Jayne and Bennett
(1990) showed that the burst
speed and stamina of garter snakes released into the wild was correlated with
their survival a year after testing. Tadpoles with a high burst swimming
performance were also more likely to survive encounters with garter snakes in
experimental mesocosms (Watkins,
1996
). Swain
(1992
) found superior burst
swimming performance in sticklebacks (Gasterosteus aculeatus) by
certain vertebral phenotypes which was matched by increases in the frequencies
of those phenotypes in the wild. It is entirely possible, however, that
increased locomotory performance following temperature acclimation may incur
other costs such as increasing encounter rates with predators, which offset
any direct fitness gains. Presumably, there must also be a trade-off between
the benefits of increased performance and the energetic costs associated with
the restructuring of myofibrils, sarcoplasmic reticulum membranes and
metabolic pathways. In no case of temperature acclimation has it been
established that the performance gains are sufficient to make a critical
contribution to survival in predatorprey encounters, although this may
well be the case. It is also entirely possible that factors such as
responsiveness to predators may be equally important to survival as maximum
locomotory performance, and this has yet to be investigated.
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Developmental plasticity to temperature |
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There have been relatively few studies on the developmental plasticity of
muscle in relation to locomotion. We have investigated developmental
plasticity to temperature in the spring-spawning Clyde stock of Atlantic
herring (Clupea harengus L.). Clyde herring deposit their eggs on the
seabed at a depth of 15-20 m at a time when sea temperatures are rising and
range from 4 to 12°C, depending upon the inter-annual variation in
oceanographic conditions. Embryos were found to emerge from the egg capsule
after around 9 days at 12°C, with this increasing to 28 days at 5°C
(Johnston et al., 1995b). At
hatching, the transparent herring larvae are 7-9 mm in total length
(TL) with a prominent primordial fin extending along the dorsal and
ventral margins of the trunk (Batty,
1984
). At this stage, the larvae swim using an anguilliform mode
of locomotion in which the amplitude of the trunk movements increases linearly
along the body. Muscle differentiation and much of organogenesis occurs over a
protracted period following yolk-sac absorption
(Blaxter, 1988
;
Johnston et al., 1997
). As the
adult pattern of paired and medial fins and associated muscles gradually
develops (12-22 mm TL), the trunk becomes more laterally compressed,
and the larvae adopt a progressively more carangiform mode of swimming in
which the head is kept relatively still and the amplitude of trunk movements
increases markedly towards the caudal fin
(Batty, 1984
). Thus, the
transfer of force to the water shifts from the whole surface of the trunk to
the caudal fin, which acts as a flexible paddle. The larvae metamorphose into
the silver juvenile stage over the size range 33-42 mm TL, by which
time development is essentially complete.
Laboratory experiments indicate that differentiation of several of the
tissues involved in locomotion is uncoupled from somatic growth in larvae
reared at different temperatures. Notochord flexion and the development of the
medial fins occurred at longer body lengths in larvae reared at 5-8°C than
in those reared at 12-15°C (Johnston
et al., 1998). The slow muscle fibres responsible for sustained
activity are initially innervated by en grappe endplates at the
myosepta. The adult multi-terminal pattern of slow muscle innervation was
established in larvae of 12-14 mm TL at 12°C, but was it delayed
until 16-19 mm TL at 5°C (Fig.
8).
|
The majority of the myofibrillar proteins exist as developmental-stage-specific isoforms resulting from multigene families or from the alternative splicing of mRNA transcripts. The body length at which the transition from embryonic/larval isoforms to adult isoforms varies with temperature, but is not the same for all proteins (Fig. 8). Thus, at 12°C, the adult isoform of myosin light chain 2 (LC2) largely replaces the embryonic LC2 in larvae of 13 mm TL, whereas this transition is delayed until the larvae are 15 mm TL at 5°C (Fig. 8). The fast muscle in herring embryos and larvae contains a large number of isoforms of troponin T (TnT), which are thought to arise from alternative splicing of a single gene. The number of TnT isoforms decreases during ontogeny, with the adult patterns of isoforms being established by 13 mm TL at 12°C, but not until 17 mm TL at 5°C (Fig. 8). The slow muscle fibres of herring larvae express the adult fast muscle isoform of myosin light chain 3 (LC3f) until 22 mm TL at 12°C, but retain LC3f until 28 mm TL at 5°C (Fig. 8). Thus, the constituent proteins of the myofibril show considerable variation with respect to body length depending on the prevailing sea temperature.
We would predict from such results that the performance and energetic cost
of swimming would be a function of the thermal history of the larvae.
Remarkably, the temperature prior to the onset of endogenous feeding was
sufficient to influence the relative timing of development of components of
the locomotory system more than a month later
(Johnston et al., 2001). Clyde
herring were reared at 5 or 12°C until first feeding and then transferred
to a common ambient temperature (Fig.
9A). The development of the dorsal and anal fin rays and
associated stiffening muscles occurred at shorter body lengths in fish
initially reared at 12°C than in those reared at 5°C
(Fig. 9B-E). This morphological
variation was associated with the adult swimming style being adopted at
shorter body lengths and with significantly improved fast-start performance in
larvae that had experienced warmer temperatures earlier in development
(Johnston et al., 2001
)
(Fig. 10). Once larvae reach
22 mm TL, the development of the motor system and associated
morphological characters is essentially complete
(Batty, 1984
) and differences
between temperature groups are no longer apparent
(Johnston et al., 2001
).
Developmental plasticity and its associated phenotypic variation can therefore
influence locomotory performance and may be of considerable ecological
importance during early larval stages when mortality is high because of
starvation and predation.
|
|
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Perspective |
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Acknowledgments |
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References |
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Altringham, J. D. and Johnston, I. A. (1986). Evolutionary adaptation to temperature in fish muscle cross bridge mechanisms tension and ATP turnover. J. Comp. Physiol. B 156,819 -821.
Altringham, J. D. and Johnston, I. A. (1990). Modelling muscle power output in a swimming fish. J. Exp. Biol. 148,396 -402.
Altringham, J. D., Wardle, C. S. and Smith, C. I.
(1993). Myotomal muscle function at different locations in the
body of a swimming fish. J. Exp. Biol.
182,191
-206.
Ball, D. and Johnston, I. A. (1996). Molecular
mechanisms underlying the plasticity of muscle contractile properties with
temperature acclimation in the marine fish Myoxocephalus scorpius.J. Exp. Biol. 199,1363
-1373.
Batty, R. S. (1984). Development of swimming movements and musculature in larval herring (Clupea harengus). J. Exp. Biol. 110,217 -229.[Abstract]
Beddow, T. A. and Johnston, I. A. (1995).
Plasticity of muscle contractile properties following temperature acclimation
in the marine fish Myoxocephalus scorpius. J. Exp.
Biol. 198,193
-201.
Beddow, T. A., van Leeuwen, J. L. and Johnston, I. A.
(1995). Swimming kinematics of fast-starts are altered by
temperature acclimation in the marine fish Myoxocephalus scorpius.J. Exp. Biol. 198,203
-208.
Bennett, A. F. and Lenski, R. E. (1997). Evolutionary adaptations to temperature. VI. Phenotypic acclimation and its evolution in Escherichia coli. Evolution 51, 36-44.
Biewener, A. A. and Roberts, T. J. (2000). Muscle and tendon contributions to work and elastic energy savings: a comparative perspective. Exerc. Sports Sci. Rev. 28, 99-107.
Blaxter, J. H. S. (1988). Pattern and variety in development. In Fish Physiology, vol.XI , part A (ed. W. S. Hoar and D. J. Randall), pp.1 -58. San Diego, CA: Academic Press.
Bone, Q. (1966). On the function of two types of muscle fibre in elasmobranch fish. J. Mar. Biol. Ass. UK 46,321 -349.
Boutilier, R. G., Glass, M. L. and Heisler, N. (1987). Blood gases, and extracellular/intracellular acidbase status as a function of temperature in the anuran amphibians Xenopus laevis and Bufo marinus. J. Exp. Biol. 130,13 -25.
Braña, F. and Xiang, J. I. (2000). Influence of incubation temperature on morphology, locomotor performance and early growth of hatchling wall lizards (Podarcis muralis). J. Exp. Zool. 286,422 -433.[Medline]
Clark, D. S. and Green, D. (1991). Seasonal variation in temperature preference of juvenile Atlantic cod (Gadus morhua), with evidence supporting an energetic basis for their diel vertical migration. Can. J. Zool. 69,1302 -1307.
Cole, N. J. and Johnston, I. A. (2001). Plasticity of myosin heavy chain expression is gradually acquired during ontogeny in the common carp (Cyprinus carpio L.). J. Comp. Physiol. 171,321 -326.
Cossins, A. R. and Bowler, K. (1987). Temperature Biology of Animals. Cambridge: Cambridge University Press. 339pp.
Coughlin, D. J. and Rome, L. C. (1999). Muscle
activity in steady swimming scup, Stenotomus chrysops, varies with
fiber type and body position. Biol. Bull.
196,145
-152.
Crawshaw, L. I., Ackerman, R. A., White, F. N. and Heath, M. E. (1982). Metabolic and acidbase changes during selection of warmer water by cold-acclimated fish. Am. J. Physiol. 242,R157 -R161.[Medline]
Crockford, T. and Johnston, I. A. (1990). Temperature acclimation and the expression of contractile protein isoforms in the skeletal muscles of the common carp (Cyprinus carpio L.). J. Comp. Physiol. B 160,23 -30.
Else, P. L. and Bennett, A. F. (1987). The thermal dependence of locomotor performance and muscle contractile function in the salamader Ambystoma tigrinum nebulosum. J. Exp. Biol. 128,219 -233.[Abstract]
Feder, M. E. (1986). Effect of thermal acclimation on locomotor energetics and locomotor performance in a lungless salamander, Desmognathus ochrophaeus. J. Exp. Biol. 121,271 -283.[Abstract]
Fleming, J. R., Crockford, T., Altringham, J. D. and Johnston, I. A. (1990). Effects of temperature acclimation on muscle relaxation in the carp: a mechanical, biochemical and ultrastructural study. J. Exp. Zool. 255,286 -295.
Foster, M. A. (1969). Ionic and osmotic regulation in three species of Cottus (Cottidae, Teleost). Comp. Biochem. Physiol. 30,751 -759.[Medline]
Franklin, C. E. and Johnston, I. A. (1997).
Muscle power output during escape responses in an Antarctic fish.
J. Exp. Biol. 200,703
-712.
Frith, H. R. and Blake, R. W. (1995). The
mechanical power output and hydromechanical efficiency of northern pike
(Esox lucius) fast-starts. J. Exp. Biol.
198,1863
-1873.
Fry, F. E. J. and Hart, J. S. (1948). Cruising speed of goldfish in relation to water temperature. J. Fish. Res. Bd. Can. 7,169 -175.
Fukuhara, O. (1990). Effects of temperature on yolk utilization, initial growth, and behaviour of unfed marine fish-larvae. Mar. Biol. 106,169 -174.
Getty, T. And Pulliam, H. R. (1991). Random prey detection with pausetravel search. Am. Nat. 138,1459 -1477.
Gibbs, A. G., Louie, A. K. and Ayala, J. A.
(1998). Effects of temperature on cuticular lipids and water
balance in a desert Drosophila: is thermal acclimation beneficial?
J. Exp. Biol. 201,71
-80.
Guderley, H., Leroy, P. H. and Gagne, A. (2001). Thermal acclimation, growth, and burst swimming of threespine stickleback: Enzymatic correlates and influence of photoperiod. Physiol. Biochem. Zool. 74, 66-74.[Medline]
Heap, S. P., Watt, P. W. and Goldspink, G. (1985). Consequences of thermal change on the myofibrillar ATPase of five freshwater teleosts. J. Fish Biol. 26,733 -738.
Hirano, M. and Rome, L. C. (1984). Jumping performance of frogs (Rana pipiens) as a function of temperature. J. Exp. Biol. 108,429 -439.
Hirayama, Y., Kanoh, S., Nakaya, M. and Watabe, S.
(1997). The two essential light chains of carp fast skeletal
myosin, LC1 and LC3, are encoded by distinct genes and change their molar
ratio following temperature acclimation. J. Exp. Biol.
200,693
-701.
Hirayama, Y., Kobiyama, A., Ochiai, Y. and Watabe, S. (1998). Two types of mRNA encoding myosin regulatory light chain in carp fast skeletal muscle differ in their 3' non-coding regions and expression patterns following temperature acclimation. J. Exp. Biol. 201,2815 -2820.
Hirayama, Y. and Watabe, S. (1997). Structural differences in the crossbridge head of temperature-associated myosin subfragment-1 isoforms from carp fast skeletal muscle. Eur. J. Biochem. 246,380 -387.[Abstract]
Huey, R. B. and Berrigan, D. A. (1996). Testing evolutionary hypotheses of acclimation. In Animal and Temperature: Phenotpyic and Evolutionary Adaptation (ed. I. A. Johnston and A. F. Bennett), pp. 205-237. Cambridge: Cambridge University Press.
Huey, R. B., Berrigan, D. A., Gilchrist, G. W. and Herron, J. C. (1999). Testing the adaptive significance of acclimation: A strong inference approach. Am. Zool. 39,323 -336.
Hwang, G.-C., Watabe, S. and Hashimoto, K. (1990). Changes in carp myosin ATPase induced by temperature acclimation. J. Comp. Physiol. B 160,233 -239.
Imai, J.-I., Hirayama, Y., Kikuchi, K., Kakinuma, M. and Watabe,
S. (1997). cDNA cloning of myosin heavy chain isoforms from
carp fast skeletal muscle and their gene expression associated with
temperature acclimation. J. Exp. Biol.
200, 27-34.
James, R. S. and Johnston, I. A. (1998).
Scaling of muscle performance during escape responses in the fish
Myoxocephalus scorpius L. J. Exp. Biol.
201,913
-923.
Janzen, F. J. and Paukstis, G. L. (1991). Environmental sex determination in reptiles ecology, evolution and experimental design. Q. Rev. Biol. 66,147 -197.
Jayne, B. C. and Bennett, A. F. (1990). Selection on locomotor performance capacity in a natural population of garter snakes. Evolution 44,1204 -1229.
John-Alder, H. B., Barnhart, M. C. and Bennett, A. F. (1989). Thermal sensitivity of swimming performance and muscle contraction in northern and southern populations of tree frogs (Hyla crucifer). J. Exp. Biol. 142,357 -372.
Johnson, T. P. and Bennett, A. F. (1995). The
thermal acclimation of burst escape performance in fish: an integrated study
of molecular and cellular physiology and organismal performance. J.
Exp. Biol. 198,2165
-2175.
Johnson, T. P., Bennett, A. F. and McLister, J. D. (1996). Thermal dependence and acclimation of fast-start locomotion and its physiological basis in rainbow trout (Oncorhynchus mykiss). Physiol. Zool. 69,276 -292.
Johnson, T. P. and Johnston, I. A. (1991). Power output of fosh muscle fibres performing oscillatory work: effects of acute and seasonal temperature change. J. Exp. Biol. 157,409 -423.
Johnston, I. A. (1993). Phenotypic plasticity of fish muscle to temperature change. In Fish Ecophysiology (ed. J. C. Rankin and F. B. Jensen), pp.322 -340. London: Chapman & Hall.
Johnston, I. A., Cole, N. J., Abercomby, M. and Vieira, V. L. A. (1998). Embryonic temperature modulates muscle growth characteristics in larval and juvenile herring. J. Exp. Biol. 201,623 -646.[Medline]
Johnston, I. A., Cole, N. J., Vieira, V. L. A. and Davidson,
I. (1997). Temperature and developmental plasticity of muscle
phenotype in herring larvae. J. Exp. Biol.
200,849
-868.
Johnston, I. A., Davison, W. and Goldspink, G. (1975). Adaptation in Mg2+-activated myofibrillar ATPase induced by temperature acclimation. FEBS Lett. 50,293 -295.[Medline]
Johnston, I. A., Davison, W. and Goldspink, G. (1977). Energy metabolism of carp swimming muscles. J. Comp. Physiol. 114,203 -216.
Johnston, I. A., Fleming, J. D. and Crockford, T.
(1990). Thermal acclimation and muscle contractile properties in
cyprinid fish. Am. J. Physiol.
259,R231
-R236.
Johnston, I. A. and Lucking, M. (1978). Temperature induced variation in the distribution of different muscle fibre type in the goldfish (Carassius auratus). J. Comp. Physiol. 124,111 -116.
Johnston, I. A. and Sidell, B. D. (1984). Differences in temperature dependence of muscle contractile properties and myofibrillar ATPase activity in a cold-temperate fish. J. Exp. Biol. 111,179 -189.[Abstract]
Johnston, I. A., Sidell, B. D. and Driedzic, W. R. (1985). Forcevelocity characteristics and metabolism in carp muscle fibres following temperature acclimation. J. Exp. Biol. 119,239 -249.[Abstract]
Johnston, I. A., van Leeuwen, J. L., Davies, M. L. F. and
Beddow, T. (1995a). How fish power predation fast-starts.
J. Exp. Biol. 198,1851
-1861.
Johnston, I. A., Vieira, V. L. A. and Abercromby, M.
(1995b). Temperature and myogenesis in embryos of the Atlantic
herring Clupea harengus. J. Exp. Biol.
198,1389
-1403.
Johnston, I. A., Vieira, V. L. A. and Temple, G. K. (2001). Functional consequences and population differences in the developmental plasticity of muscle to temperature in Atlantic herring Clupea harengus. Mar. Ecol. Prog. Ser. 213,285 -300.
Jones, P. L. and Sidell, B. D. (1982). Metabolic responses of striped bass (Morone saxatilis) to temperature acclimation. II. Alterations in metabolic carbon sources and distributions of fiber types in locomotory muscle. J. Exp. Zool. 219,163 -171.
Josephson, R. K. (1985). Mechanical power ouput from striated muscle during cyclical contraction. J. Exp. Biol. 114,493 -512.
Josephson, R. K. (1993). Contraction dynamics and power output of skeletal muscle. Annu. Rev. Physiol. 55,527 -546.[Medline]
Kakinuma, M., Nakaya, M., Hatanaka, A., Hirayama, Y. and Watabe, S. (1998). Thermal unfolding of three acclimation temperature-associated isoforms of carp light meromyosin expressed by recombinant DNAs. Biochemistry 37,6606 -6613.[Medline]
King, P. A. and Fives, J. M. (1983). Littoral and benthic investigations on the west-coast of Ireland. XVI. The biology of the long-spined sea scorpion Taurulus bubalis (Euphrasen, 1786) in the Galway Bay area. Proc. R. Irish. Acad. B 83,215 -239.
Knowles, T. W. and Weigl, P. D. (1990). Thermal dependence of anuran burst locomotor performance. Copeia 3,796 -802.
Langfeld, K. S., Crockford, T. and Johnston, I. A. (1991). Temperature acclimation in the common carp: forcevelocity characteristics and myosin subunit composition of slow muscle fibres. J. Exp. Biol. 155,291 -304.
Lemons, D. E. and Crawshaw, L. I. (1985). Behavioural and metabolic adjustments to low temperatures in largemouth bass (Micropterus salmoides). Physiol. Zool. 58,175 -180.
Leroi, A. M., Bennett, A. F. and Lenski, R. E. (1994). Temperature acclimation and competitive fitness: an experimental test of the beneficial acclimation assumption. Proc. Natl. Acad. Sci. USA 91,1917 -1921.[Abstract]
Machin, K. E. and Pringle, J. W. S. (1959). The physiology of insect fibrillar muscle. II. Mechanical properties of beetle flight muscle. Proc. R. Soc. Lond. B 151,204 -225.
Miller, K. (1982). Effect of temperature on sprint performance in the frog Xenopus laevis and the salamander Necturus maculosus. Copeia 3, 695-698.
Nakaya, M., Kakinuma, M. and Watabe, S. (1997). Differential scanning calorimetry and CD spectrometry of acclimation temperature-associated types of carp light meromyosin. Biochemistry 36,9179 -9184.[Medline]
Navas, C. A., James, R. S., Wakeling, J. M., Kemp, K. M. and Johnston, I. A. (1999). An integrative study of the temperature dependence of whole animal and muscle performance during jumping and swimming in the frog Rana temporaria. J. Comp. Physiol. B 169,588 -596.[Medline]
Penney, R. K. and Goldspink, G. (1980). Temperature adaptation of sarcoplasmic reticulum of fish muscle. J. Therm. Biol. 5,63 -68.
Peplowski, M. M. and Marsh, R. L. (1997). Work
and power output in the hindlimb muscles of cuban tree frogs Oesteopilu
septentrionalis during jumping. J. Exp. Biol.
200,2861
-2870.
Putman, R. W. and Bennett, A. F. (1981). Thermal dependence of behavioural performance of anuran amphibians. Anim. Behav. 29,502 -509.
Renaud, J. M. and Stevens, E. D. (1983). The extent of long-term temperature compensation for jumping distance in the frog, Rana pipiens and the toad, Bufo americanus. Can. J. Zool. 61,1284 -1287.
Renaud, J. M. and Stevens, E. D. (1984). The extent of short-term and long-term compensation to temperature shown by frog and toad sartorius muscle. J. Exp. Biol. 108, 57-75.
Rome, L. C. (1983). The effect of long-term exposure to different temperatures on the mechanical performance of frog muscle. Physiol. Zool. 56, 33-40.
Rome, L. C. (1990). Influence of temperature on
muscle recruitment and muscle function in vivo. Am. J.
Physiol. 259,R210
-R222.
Rome, L. C., Loughna, P. T. and Goldspink, G. (1984). Muscle fibre recruitment as a function of swim speed and muscle temperature in carp. Am. J. Physiol. 247,R272 -R279.[Medline]
Rome, L. C., Loughna, P. T. and Goldspink, G. (1985). Temperature acclimation improves sustained swimming performance at low temperature in carp. Science 228,194 -196.
Rome, L. C. and Sosnicki, A. A. (1991).
Myofilament overlap in swimming carp. II. sarcomere length changes during
swimming. Am. J. Physiol.
260,C289
-C296.
Rome, L. C. and Swank, D. (1992). The influence of temperature on power output of scup red muscle during cyclical length changes. J. Exp. Biol. 171,261 -281.[Abstract]
Rome, L. C. and Swank, D. M. (2001). The
influence of thermal acclimation on power production during swimming. I.
In vivo stimulation and length change pattern of scup red muscle.
J. Exp. Biol. 204,409
-418.
Rome, L. C., Swank, D. M. and Coughlin, D. J.
(2000). The influence of temperature on power production during
swimming. II. Mechanics of red muscle fibres in vivo. J. Exp.
Biol. 203,333
-345.
Scheiner, S. M. (1993). Genetics and evolution of phenotypic plasticity. Annu. Rev. Ecol. Syst. 24, 35-68.
Sidell, B. D. (1980). Responses of goldfish (Carassius auratus L.) muscle to acclimation temperature: Alterations in biochemistry and proportions of different fiber types. Physiol. Zool. 53,98 -107.
Sisson, J. E. and Sidell, B. D. (1987). Effect of thermal acclimation on muscle fibre recruitment of swimming striped bass (Morone saxatilis). Physiol. Zool. 60,310 -320.
Swain, D. P. (1992). The functional basis of natural selection for vertebral traits of larvae in the stickleback Gasterosteus aculeatus. Evolution 46,987 -997.
Swank, D. M. and Rome, L. C. (2001). The
influence of thermal acclimation on power production during swimming. II.
Mechanics of scup red muscle under in vivo conditions. J.
Exp. Biol. 204,419
-430.
Tåning, A. V. (1952). Experimental study of meristic characters in fishes. Biol. Rev. 27,169 -193.
Temple, G. K. (1998). The phenotypic plasticity of whole animal and muscle performance during fast-starts in Cottidae. PhD thesis, University of St Andrews, Scotland.129pp .
Temple, G. K. and Johnston, I. A. (1998).
Testing hypotheses concerning the phenotypic plasticity of escape performance
in fish of the family Cottidae. J. Exp. Biol.
201,317
-331.
Temple, G. K., Wakeling, J. M. and Johnston, I. A. (2000). Seasonal changes in fast-starts in the short-horn sculpin: integration of swimming behaviour and muscle performance. J. Fish Biol. 56,1435 -1449.
Tiiska, A. J. and Lagerspetz, K. Y. H. (1999). Effects of thermal acclimation on nervous conduction and muscle contraction in the frog Rana temporaria. Comp. Biochem. Physiol. A 124,335 -342.
van Leeuwen, J. L. (1999). A mechanical
analysis of myomere shape in fish. J. Exp. Biol.
202,3405
-3414.
van Leeuwen, J. L., Lankheet, M. J. M., Akster, H. A. and Osse, J. W. M. (1990). Function of red axial muscles of carp (Cyprinus carpio): recruitment and normalised power output during swimming in different modes. J. Zool., Lond. 220,123 -145.
Vornanen, M., Tiitu, V., KaKela, R., and Aho, E. (1999). Effects of thermal acclimation on the relaxation system of crucian carp white myotomal muscle. J. Exp. Zool. 284,241 -251.[Medline]
Wakeling, J. M., Cole, N. J., Kemp, K. M. and Johnston, I.
A. (2000). The biomechanics and evolutionary significance of
thermal acclimation in the common carp Cyprinus carpio. Am. J.
Physiol. 279,R657
-R665.
Wakeling, J. M. and Johnston, I. A. (1998).
Muscle power output limits fast-start performance in fish. J. Exp.
Biol. 201,1505
-1526.
Wakeling, J. M., Kemp, K. M. and Johnston, I. A.
(1999). The biomechanics of fast-starts during ontogeny in the
common carp Cyprinus carpio. J. Exp. Biol.
202,3057
-3067.
Watabe, S., Imai, J., Nakaya, M., Hirayama, Y., Okamoto, Y., Masaki, H., Uozumi, T., Hirono, I. and Aoki, T. (1995). Temperature acclimation induces light meromyosin isoforms with different primary structures in carp fast skeletal muscle. Biochem. Biophys. Res. Commun. 208,118 -125.[Medline]
Watkins, T. B. (1996). Predator-mediated selection on burst swimming performance in tadpoles of the Pacific tree frog, Pseudacris regilla. Physiol. Zool. 69,154 -167.
Wilson, R. S. and Franklin, C. E. (1999). Thermal acclimation of locomotor performance in tadpoles of the frog Limnodynastes peronii. J. Comp. Physiol. B 169,445 -451.[Medline]
Wilson, R. S. and Franklin, C. E. (2000). Inability of adult Limnodynastes peronii (Amphibia: Anura) to thermally acclimate locomotor performance. Comp. Biochem. Physiol. A 127,21 -28.
Wilson, R. S. and Franklin, C. E. (2001). Testing the beneficial acclimation hypothesis. Trends Ecol. Evol. 17,66 -70.
Wilson, R. S., James, R. S. and Johnston, I. A. (2000). Thermal acclimation of locomotor performance in tadpoles and adults of the aquatic frog Xenopus laevis. J Comp. Physiol. B 170,117 -124.[Medline]
Zamudio, K. R., Huey, R. B. and Crill, W. D. (1995). Bigger isn't always better: boy size, developmental and parental temperature and territorial success in Drosophila melanogaster.Anim. Behav. 49,671 -677.
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