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First published online April 18, 2008
Journal of Experimental Biology 211, 1386-1393 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.014688
The effects of acute temperature change on swimming performance in bluegill sunfish Lepomis macrochirus
Department of Biological Sciences, Wellesley College, 106 Central Street, Wellesley, MA 02481, USA
* Author for correspondence (e-mail: dellerby{at}wellesley.edu)
Accepted 26 February 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: gait transition, muscle mechanics, swimming, temperature
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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; Casey,
1980; Herreid et al.,
1981; Rome, 1982;
Hirano and Rome, 1984;
Marsh and Bennett, 1986b).
This is due to a number of interacting factors. Temperature-related changes in
muscle contraction velocity affect mechanical power output
(Josephson, 1984;
Marsh and Bennett, 1986a;
Langfeld et al., 1989;
Stevenson and Josephson, 1990;
Rome and Swank, 1992;
Rome et al., 1992;
Altringham and Block, 1997).
Temperature changes also impact the performance of the respiratory and
cardiovascular systems and their ability to support aerobic metabolism (e.g.
Randall and Brauner, 1991;
Driedzic and Guesser, 1994;
Farrell, 2002;
Farrell, 2007;
Stecyk et al., 2007). In fish,
the effects of seasonal temperature changes on locomotor performance can
largely be offset by acclimation of the muscular, respiratory and
cardiovascular systems (Rome et al.,
1985; Rome and Swank,
1992; Rome et al.,
1992; Keen and Farrell,
1994; Beddow and Johnston,
1995; Egginton and Cordiner,
1996; Taylor et al.,
1996; Johnston and Temple, 2002;
Rome, 2007). Some species,
however, must cope with more acute temperature shifts. Fish in temperate
freshwater lakes are exposed to a wide range of temperatures, particularly
after the establishment of thermoclines in the spring
(Shuter et al., 1983;
Snucins and Gunn, 1995;
Fee et al., 1996). Movement
between the warm shallows and cooler, deeper water related to foraging,
breeding or predator avoidance can expose fish to rapid temperature changes,
which probably affect locomotor performance.
The bluegill sunfish Lepomis machrochirus is a temperate,
freshwater species potentially exposed to a wide range of water temperatures.
In New England lakes, bluegill breed in shallow water where the temperature
can approach 30°C, but even in the summer can also be exposed to
temperatures below the thermocline as low as 10°C (P. Zakova and M. V.
Moore, personal communication). This species swims in the labriform mode at
low speeds, generating lift and thrust by beating the pectoral fins
(Gibb et al., 1994;
Drucker and Lauder, 1999;
Drucker and Lauder, 2000). As
swimming speed increases, bluegill change gait from labriform swimming to
combined use of their pectoral fins and undulations of the body axis
(Gibb et al., 1994;
Jones et al., 2007;
Kendall et al., 2007). Gait
changes may maximize locomotor economy and/or be driven by mechanical factors
such as the limits to muscle power or the need to minimize mechanical stresses
(Alexander, 1989). When
swimming at their acclimation temperature (Ta), the
labriform–undulatory gait change in bluegill is primarily driven by the
need to recruit additional muscle mass to meet the power requirements of
higher speed swimming (Kendall et al.,
2007). In ectotherms, environmental temperature is an additional
factor determining gait transition speed. An early recruitment of anaerobic
muscle at low temperatures has been identified during undulatory fish swimming
(Rome et al., 1992), but the
effects of temperature on transitions between different styles of aerobically
supported swimming have not been quantified. Understanding how temperature
affects gait transitions of this type is important because the speeds at or
around the gait transition appear to coincide with the minimum total cost of
transport in a number of species, including bluegill
(Brett and Sutherland, 1965;
Korsmeyer et al., 2002;
Kendall et al., 2007).
Temperature-related changes in gait transition speed are therefore likely to
be significant for the energy budgets of gait transitioning species.
Previous work has largely focused on maximal swimming performance, which
typically plateaus, and ultimately declines as temperature increases above
Ta (Fry and Hart,
1948; Randall and Brauner,
1991; Myrick and Cech,
2000; Ojanguren and
Braña, 2000; Lee et
al., 2003; Claireaux et al.,
2006), likely due to limitations on cardiovascular performance at
high temperatures (Randall and Daxboeck,
1982; Jain and Farrell,
2003; Farrell,
2002; Farrell,
2007). Similar constraints are unlikely to apply to the
labriform–undulatory gait transition in bluegill as this occurs at less
than one third of their maximal aerobic capacity
(Kendall et al., 2007). We
therefore hypothesized that the relationships of labriform–undulatory
gait transition speed (Utrans) and maximum aerobic
swimming speed (Umax) to water temperature would be
different from one another, particularly at high temperatures.
Utrans was expected to increase relative to the
acclimation level at temperatures above Ta because of
enhanced muscle mechanical performance in the absence of central or external
limits to oxygen and substrate delivery. By contrast, Umax
was not expected to increase at temperatures above the acclimation temperature
because of central or external limitations on the capacity of the
cardiovascular system to support increased aerobic metabolism. We also
hypothesized that as in previous studies carried out at Ta
in this species (Kendall et al.,
2007), the availability of muscle power from the pectoral girdle
muscles would be the primary factor determining Utrans at
all temperatures. In order to test these hypotheses we determined
Utrans, Umax and pectoral girdle
muscle power output at a range of water temperatures.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Data were collected at the same temperatures used in the
swimming experiments in physiological saline saturated with oxygen.
Animals
Bluegill sunfish (Lepomis macrochirus Rafinesque) were collected
from Lake Waban, MA, USA using hook and line. Kinematic, maximal swimming
performance, and muscle power output data were obtained from six fish [mass
152.3±12.8 g, fork length (L) 19.1±0.5 cm, mean
± s.e.m.]. The fish were kept at 22°C under a 12 h:12 h light:dark
cycle and fed chopped earthworms twice a week. All procedures were approved by
the Institutional Animal Care and Use Committee.
Swimming flume
Swimming experiments were carried out at 14, 18, 22, 26 and 30°C in a
sealable, recirculating flume (Model 90, Loligo Systems, Hobro, Denmark)
capable of generating flow velocities ranging from 5 to 150 cm
s–1. The flume consisted of an inner chamber 88.6 l in volume
with a working section of 20x20x70 cm and an outer tank, which
buffered temperature changes and served as a reservoir of oxygenated water.
Ambient temperature in the room housing the flume was 22°C. For
experimental temperatures below 22°C, water temperature was reduced using
a thermostatically controlled aquarium chiller (Arctica, 1/10 Horsepower,
Transworld Aquatics, Inglewood, CA, USA) through which water was circulated
with a submersible pump. Two 300 W thermostatically controlled aquarium
heaters (Hydor, Vicenza, Italy) were used to raise the temperature above
22°C. Swimming experiments were carried out at all temperatures in air
saturated water, and additionally at 30°C with the dissolved oxygen
content elevated to 12.0 mg l–1 by bubbling 100% oxygen into
the water via an air stone. Oxygen concentration was monitored using
a polarographic oxygen probe inserted through a port in the lid of the flume
(Accumet XL40, Fisher Scientific, Pittsburgh, USA). The order in which fish
were exposed to the different experimental conditions was randomized.
The large volume of water in the flume meant that rapid temperature changes
could not be applied using the heaters or chiller. Rates of temperature change
were limited to approximately 1°C per hour. Consequently fish could not be
exposed to an instantaneous temperature change while in the flume. Exposure to
slow temperature changes was undesirable, as this had the potential to allow
for at least partial acclimation to temperatures other than
Ta. Netting fish to allow transfer between the holding
tanks and flume can induce escape responses and struggling behaviors leading
to the buildup of lactic acid due to intense contractions of the anaerobic
myotomal muscle (Lackner et al.,
1988). To avoid this, fish were removed from holding tanks by
gently scooping them into a 5 l plastic container of water. This was immersed
in the working section of the flume and slowly rotated to release the fish.
This approach allowed the transfer of fish with a minimum of disturbance,
reducing the need for lengthy recovery periods after transfer to the flume,
while still enabling exposure to acute temperature changes. If a fish became
startled and exhibited escape responses or struggling during transfer it was
returned to the holding tank and another individual selected for swimming
kinematics or performance measurements.
Swimming kinematics
Video sequences were recorded using a Sony HDR HC-3 camcorder at a frame
rate of 120 Hz at speeds ranging from 8.4 to a maximum of 51.1 cm
s–1 (0.44–2.68 l s–1), the upper limit
varying with water temperature. Under each set of conditions speed was
increased from 8.4 cm s–1 (0.44 l s–1) in
approximately 4 cm s–1 (0.21 l s–1)
increments. At each speed the fish was allowed to swim for 5 min before video
recording was started. A mirror mounted above the flume at a 45° angle
allowed simultaneous recording of lateral and dorsal views of the fish. Video
sequences were captured on a Macintosh iMac computer and analyzed using
VideoPoint software (Lenox Softworks, Lenox, MA, USA) to determine pectoral
and caudal fin beat frequencies during sequences of steady swimming (mean
sequence length 25 fin beats). Utrans was defined as the
first speed at which there was detectable lateral movement of the caudal fin.
The same group of fish was used for measurements of maximal swimming
performance.
Maximal swimming performance
A protocol involving incremental changes in swimming speed was used to
establish Umax using the same group of fish for which
kinematic data were obtained. Starting at 8.4 cm s–1, speed
was increased in 4 cm s–1 increments and maintained at a
given level for 10 min between increments. Speed increases continued until the
fish could no longer maintain position in the flume. This coincided with the
onset of burst and coast swimming behavior and high amplitude lateral body
undulation, probably indicative of the recruitment of anaerobic muscle. The
time maintained at the final speed interval (T, in min) was recorded.
Umax (in cm
s–1)=Ufin+4(T/Tint),
where Ufin (in cm s–1) was the speed of
the final interval at which steady swimming could be maintained and
TInt was the time interval between speed increments. This
test was not equivalent to a critical swimming speed
(Ucrit) test, as these typically involve exercising the
fish until complete exhaustion, indicated by an inability to move from the
mesh at the rear of the flume working section
(Brett, 1964). Our aim was to
determine maximal aerobically supported performance in a similar manner to
Claireaux et al. (Claireaux et al.,
2006). Speeds approaching Ucrit involve the
recruitment of anaerobic muscle (Burgetz
et al., 1998; Lurman et al.,
2007), elevating performance above sustainable, aerobic levels. A
standard Ucrit protocol was therefore not compatible with
our experimental goals.
Muscle power measurements
The maximum mechanical power output of the largest muscle powering the
pectoral fin downstroke (abductor superficialis) was measured in
vitro using the work loop technique
(Josephson, 1985). This
technique measures the mechanical power output of cyclically operating muscles
under conditions that mimic those experienced by the muscle in vivo.
Experimental protocols were similar to those previously used to measure
pectoral girdle muscle power output in this species
(Jones et al., 2007;
Kendall et al., 2007). Fish
were anesthetized using buffered MS-222 solution at a concentration of 100 mg
l–1, and then an L-shaped incision was made in the skin
overlying the pectoral girdle muscles, and the skin blunt dissected from the
underlying musculature to expose the abductor superficialis. A loop of silk
suture was tied to the distal tendon of a muscle fascicle and the tendon cut
distal to the knot. The fascicle was gently freed from the surrounding muscle
tissue, the section of the cleithrum around the origin of the fascicle was cut
and the intact fascicle removed to a dish of chilled, oxygenated physiological
saline at 5°C. The saline contained (in mmol l–1) 109
NaCl, 2.7 KCl, 1.8 CaCl2, 0.47 MgCl2, 2.5
NaHCO3, 5.3 sodium pyruvate and 10.0 Hepes, pH 7.4 at 22°C.
Muscle power measurements were made using a muscle ergometer (300B-LR,
Aurora Scientific, Aurora, Ontario, Canada). This controlled muscle length and
measured force while the muscle was stimulated electrically (701B, Bi-Phase
Current Stimulator, Aurora Scientific). Sinusoidal length change cycles were
applied to the fascicle. A sinusoid is a reasonable approximation of the
strain patterns experienced by the muscle fascicles in vivo
(Jones et al., 2007;
Kendall et al., 2007). The
frequency, amplitude and relative timing and duration of stimulation were
controlled using Dynamic Muscle Control software (Version 4.0, Solwood
Enterprises Inc., Blacksburg, VA, USA). The force and position data were
captured to a PC via a 604A A to D interface, (Aurora Scientific) and
a PCI A to D card (PCI-6503, National Instruments, Austin, TX, USA). The net
work done per cycle was calculated using Dynamic Muscle Analysis software
(Version 3.12, Solwood Enterprises Inc., Blacksburg, VA, USA).
The temperature of the tissue chamber was controlled by circulating water from a Neslab RTE7 thermostatically controlled water bath (Thermo Electric, Chicago, IL, USA) through the water jacket and it was monitored with a thermocouple thermometer (EasyView 10, Extech, Waltham, MA, USA). Power measurements were made at the same temperatures for which kinematic data were obtained in the flume (14, 18, 22, 26 and 30°C). For a given fascicle the order of progression through the temperatures was randomized. On switching to a new temperature the fascicle was allowed 5 min rest to ensure that the temperature within the chamber had stabilized. At each temperature an initial set of control work loops was applied to the fascicle. Subsequently, at the fin beat cycle frequency used during maximal labriform swimming at that temperature, muscle strain and relative timing and duration of activation were systematically changed until the maximum power output was measured. Power was then measured at progressively higher cycle frequencies (increased at 0.4 Hz intervals) until a decline in power output was measured. Muscle strain and relative timing and duration of activation were again systematically changed to maximize power output. Optimal strain and stimulus parameters were similar to those previously established for this muscle (Jones et al., 1997). Finally, the control work loops were repeated. Before switching to the next experimental temperature the chamber was brought to the same temperature as was used for the initial set of control work loops at the start of the experiment, and the control loops repeated. This allowed us to control for changes in performance at a given temperature, and across temperatures. The decline between controls was used to correct the power outputs measured during the intervening work loops, assuming a linear change in work output between controls. Data collection was terminated if power output declined by 10% relative to the initial control. After completion of the power measurements, the connective tissue and bone were removed from the fascicle, and the muscle tissue weighed. Power outputs were measured from six muscle fascicles in total, one from each of the fish used for the collection of swimming performance data.
A number of muscles contribute to powering movements of the pectoral fins
in labriform swimmers (Drucker and Jensen,
1997; Westneat and Walker,
1997; Lauder et al.,
2006; Jones et al.,
2007). The abductor superficialis is the largest fin abductor and
constitutes 36% of the total muscle mass likely supplying positive power
during steady labriform swimming in bluegill
(Jones et al., 2007). Its main
antagonist, powering the upstroke, is the adductor profundus, constituting
another 38% of the power supplying muscle mass. We have not obtained work loop
data in relation to changing temperature for this muscle. However, the basic
contractile properties, power outputs, and range of operating frequencies are
similar in both muscles (Jones et al.,
2007). The effects of temperature on the isometric properties of
both muscles are also similar (D.J.E., unpublished data). Given these
similarities it is reasonable to use the changing mechanical performance of
the abductor superficialis in relation to temperature as an indicator of the
likely temperature-related changes in the other major power producing
muscle.
Statistical analyses
All statistical analyses were carried out using SPSS (Version 14.0, SPSS,
Chicago, USA). An individual fish identifier was included in all statistical
models as a random factor. General linear models were used to test for
differences in Utrans and Umax between
different temperature and oxygen treatments, with temperature and oxygen
treatment included in the models as a fixed factor. Similar models, with
pectoral and caudal fin beat frequency as the dependent variables, were used
to test for differences in these variables between different temperature and
oxygen treatments. A general linear model (GLM) was also used to test for
differences in abductor superficialis power output in relation to changing
temperature and cycle frequency. Temperature and cycle frequency were included
in the model as fixed factors. For the muscle power data obtained at a given
temperature, power output at higher strain cycle frequencies was compared to
that at the in vivo cycle frequency using a simple contrasts
procedure. This tested whether there was a significant change in muscle power
output at higher cycle frequencies relative to that used in vivo. All
data are shown as mean ± s.e.m.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Randall and Brauner, 1991;
Myrick and Cech, 2000;
Ojanguren and Braña,
2000; Lee et al.,
2003; Claireaux et al.,
2006). Increasing the water oxygen concentration with 100% oxygen
at 30°C did not result in detectable changes in maximal swimming speed
relative to that measured in air-saturated water at 30°C
(Fig. 2A,B). This is similar to
the pattern observed in salmonids, where Ucrit is the same
in hyperoxic and normoxic water (Davis et
al., 1963; Jones,
1971).
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; Drucker and Lauder,
1999; Jones et al.,
2007). There were significant changes in maximal labriform
swimming speed in relation to changing temperature and oxygen treatment
(Fig. 2A; GLM,
F=59.52, P<0.001). There were also significant changes in
pectoral fin beat frequency at the gait transition speed
(Fig. 4B; GLM,
F=21.00, P<0.001). Initially, both gait transition speed
and fin beat frequency increased with increasing temperature. Raising the
temperature above 22°C did not result in further detectable increases in
either variable relative to their values at that temperature
(Fig. 4A,B). Increasing the
water oxygen concentration with 100% oxygen at 30°C did not result in
detectable changes in either gait transition speed or fin beat frequency
relative to those measured in air saturated water at 30°C
(Fig. 4A,B).
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Muscle mechanical performance
Isometric tetanic stress (175±4.8 kN m–2), and
twitch times at 22°C [twitch rise time (Tr),
40.9±2.2 ms; time from peak force to 90% relaxation
(T90), 118.4±3.6 ms] were similar to those
previously measured in this muscle at the same temperature
(Jones et al., 2007). Peak
tetanic stress did not change significantly in relation to changing
temperature (GLM, F=2.7, P>0.05). Both
Tr and T90 changed significantly with
temperature (GLM, F=50.1, P<0.001,
Tr; GLM, F=44.0, P<0.001,
T90). Tr ranged from 58.0±2.9
to 28.0±2.1 ms, and T90 from 190.1±4.6 and
79.1±2.8 ms between 14 and 30°C. The overall Q10 for
twitch rise times was approximately 1.9 from 14 to 30°C, similar to that
observed in other vertebrate muscles across a similar temperature range (e.g.
Bennett, 1985;
Marsh and Bennett, 1986a;
Langfeld et al., 1989). All
values for isometric properties are means ± s.e.m., N=6.
Representative fascicle stress, strain and work loop traces from an abductor superficialis fascicle are shown in Fig. 5. Work loop shape changed with temperature (Fig. 5B). As relaxation times decreased with increasing temperature the fascicles could be stimulated for a greater proportion of shortening (Fig. 5B). This resulted in more sustained stress production during shortening, and enhancement of positive work output. Mean net mass specific power outputs of the abductor superficialis fascicles are shown in Fig. 6. Overall there were significant changes in power output in relation to changing temperature (GLM, F=56.8, P=0.001) and cycle frequency (GLM, F=17.44, P<0.001). Within the temperature treatments, no change in power output relative to the in vivo cycle frequency with increasing cycle frequency were detected at 14, 18 and 22°C (P>0.05 for all contrasts). At 26°C power output was significantly higher at a cycle frequency of 5.0 Hz, relative to the in vivo frequency of 4.2 Hz (P=0.047). At 30°C power output was significantly higher at all higher cycle frequencies relative to that at the in vivo cycle frequency of 3.8 Hz (P<0.001 for all contrasts).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Altringham and Ellerby, 1999;
Drucker and Lauder, 1999;
Coughlin, 2002). The
availability of muscle power may therefore limit maximum swimming and gait
transition speeds (Korsmeyer et al.,
2002; Kendall et al.,
2007). The capacity to deliver oxygen and substrates to active
muscle, or the muscle to utilize these in the mitochondrial respiratory chain,
may also set performance limits (Weibel et
al., 1996). This can be due to external factors such as oxygen
levels in the surrounding environment, or internal factors such as the rates
at which the respiratory surface and cardiovascular system can take up and
deliver oxygen (Weibel et al.,
1996; Sollid et al.,
2005; Farrell,
2002; Farrell,
2007). Determining which factors limit performance in a given
locomotor system requires an integrated approach, measuring performance at
both the whole organism and tissue levels. By measuring both swimming
performance and pectoral girdle muscle power output at a range of
temperatures, we have determined how temperature affects both maximal aerobic
performance, and a low-speed gait transition in bluegill sunfish. We have also
shown that the physiological and mechanical factors limiting the gait
transition speed change with temperature.
Most previous studies of the effects of temperature on fish swimming have
focused on maximal aerobic performance
(Fry and Hart, 1948;
Griffiths and Alderdice, 1972;
Randall and Brauner, 1991;
Myrick and Cech, 2000;
Ojanguren and Braña,
2000; Lee et al.,
2003; Claireaux et al.,
2006). Bluegill exhibited a typical teleost relationship between
maximal aerobic swimming speed (Umax) and temperature. At
low temperatures, swimming performance was impaired relative to that at the
acclimation temperature (Fig.
1, Fig. 2A,B),
probably because of a reduction in myotomal muscle contraction velocity and
power output (Figs 5 and
6)
(Rome, 1990;
Rome et al., 1992). Raising
the water temperature above the acclimation temperature did not change
Umax or the caudal fin beat frequency used at that speed,
relative to their acclimation levels (Fig.
1, Fig. 2A,B),
despite the potential for enhanced myotomal muscle power output. The dissolved
oxygen levels in air-saturated water at 30°C are approximately 70% of
those at 14°C (Weiss,
1970). It has been suggested that this may constitute an external
limit on oxygen availability at high temperatures, limiting performance
(Brett, 1971). Elevated oxygen
levels did not increase swimming performance at 30°C
(Fig. 1,
Fig. 2A,B) suggesting that this
was not a factor in the present study. In the absence of external limits of
this type, the capacity of the cardiovascular system to maintain systemic
oxygen delivery has been identified as a major factor determining maximal
aerobic performance at high temperatures
(Farrell, 2002;
Farrell, 2007). At high
temperatures, cardiac performance may be limited by the oxygen supply to the
heart. In many fish the venous blood returning to the heart supplies oxygen to
the cardiac muscle in the absence of an extensive coronary circulation.
Increased oxygen extraction by skeletal muscle at high temperatures and the
resulting reduction in the oxygen content of the venous blood may therefore
limit cardiac output (Farrell,
2002). Even if sufficient environmental oxygen is available, the
capacity for oxygen uptake at the gills or oxygen and substrate delivery by
the cardiovascular system may therefore be insufficient to meet the increased
metabolic demands of locomotor muscle at high temperatures
(Randall and Daxboeck, 1982;
Jain and Farrell, 2003;
Farrell, 2002;
Farrell, 2007).
Studies of maximal swimming have provided valuable insight into which
factors limit aerobic performance in fish with respect to changing
temperature. Most locomotor behavior, however, involves sub-maximal energy
expenditure. The extent to which temperature changes affect routine locomotor
behavior in fish is less well understood. Many fish gait transitions fall into
this category of routine behaviors, occurring at relatively low levels of
aerobic activity (Brett and Sutherland,
1965; Parsons and Sylvester,
1992; Korsmeyer et al.,
2002; Cannas et al.,
2006; Kendall et al.,
2007). This means that the factors relating to oxygen uptake and
delivery that limit Umax are unlikely to apply to
Utrans. Peripheral factors, such as oxygen and substrate
delivery at the muscle level and the relationship between muscle mechanical
performance and temperature, rather than systemic maxima for blood flow and
respiratory exchange rates, are likely to be significant in determining
performance. This led us to hypothesize that, because of the potentially
different constraints that applied, the effects of temperature on
Umax and Utrans would be
different.
Contrary to our expectation, the relationship between
Utrans and temperature was similar to that for
Umax (Fig.
3, Fig. 4A,B). At
low temperatures this was expected, because of the reduction in pectoral
girdle muscle contraction velocity and power output at temperatures lower than
the acclimation temperature (Figs
5 and
6). The plateau in
Utrans at temperatures above the acclimation temperature
did not fit with our initial predictions. In bluegill, aerobic activity can be
sustained at a level three times greater than that used during maximal
labriform swimming (Kendall et al.,
2007), so at Utrans there is additional
capacity to deliver and utilize oxygen, at least at the whole-organism level.
Factors other than systemic respiratory and cardiovascular performance must
limit Utrans at high temperatures.
If the limits to muscle mechanical performance were driving the gait
transition, then the power available from the pectoral girdle musculature
would be approximately maximal at the fin beat frequency used at
Utrans. This has previously been observed in bluegill
acclimated to, and swimming at 22°C
(Kendall et al., 2007). A
similar pattern was observed in the present study at 14, 18 and 22°C
(Fig. 4B,
Fig. 6). At these temperatures,
the strain cycle frequency that maximized muscle mechanical power output
approximated that used in vivo at Utrans
(Fig. 4B,
Fig. 6). By contrast, at
temperatures above Ta, there was a mismatch between the
in vivo cycle frequency, and the optimal cycle frequency for
maximizing mechanical power output (Fig.
4B, Fig. 6). At
both 26 and 30°C there was considerable scope in vitro for
increasing operating frequency and power output beyond the in vivo
maxima (Figs 5 and
6). Something other than the
intrinsic mechanical properties of the muscle must therefore be determining
Utrans and driving the gait transition at higher
temperatures.
A similar mismatch between in vitro and in vivo muscle
mechanical performance has been observed in running lizards [Sceloporus
occidentalis (Marsh and Bennett,
1986b)]. In this species the maximum shortening velocity of the
iliofibularis muscle, a hip extensor, increased with increasing temperature
(Marsh and Bennett, 1986a;
Marsh and Bennett, 1986b).
Despite this, both stride frequency and maximal speed plateaued at high
temperatures in a similar way to pectoral fin beat frequency and
Utrans in bluegill
(Marsh and Bennett, 1986b). In
Sceloporus this was attributed to passive mechanical constraints that
were not temperature sensitive (Marsh and
Bennett, 1986b). Similar factors are also likely to be important
in bluegill. Detailed analyses of fin kinematics have revealed the complex
twisting and curvature of the fin surface throughout the fin beat cycle
(Lauder et al., 2006;
Standen and Lauder, 2006;
Lauder et al., 2007). Although
powered and controlled by muscles, the movement patterns are also caused by
the passive mechanical properties of the fin rays, fin membrane and tendons
(Lauder et al., 2006;
Lauder et al., 2007). The
properties of these passive components, which are largely fixed with respect
to temperature, may limit fin beat frequency. An additional, external
mechanical factor is the interaction of the pectoral fins with the water to
generate lift and thrust. In bluegill, as labriform swimming speed increases,
the jet flow associated with the pectoral fin down-stroke becomes increasingly
laterally oriented (Drucker and Lauder,
2000). This means that as speed, and therefore drag, increase, the
capacity to develop thrust as a component of the total momentum transferred to
the water decreases, potentially imposing a hydrodynamic limit on labriform
swimming that is independent of the available muscle power.
Physiological factors may also limit pectoral girdle muscle performance at
high temperatures. Blood flow rates to specific muscles can reach maximum
levels at sub-maximal levels of organismal aerobic metabolism
(Armstrong et al., 1987;
Ellerby et al., 2005). Even
though central limits to oxygen uptake and delivery have not been reached at
Utrans, peripheral limits to blood flow rate, and
consequently oxygen and substrate delivery, may prevent the pectoral girdle
muscle from reaching its maximum potential power output in vivo.
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Alexander, R. M. (1989). Optimization and gaits
in the locomotion of vertebrates. Physiol. Rev.
69,1199
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