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First published online September 14, 2007
Journal of Experimental Biology 210, 3422-3429 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.005744
Efficiency of labriform swimming in the 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 27 July 2001
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gross=Pmech/Ptotal),
0.16–0.22; muscle efficiency
(muscle=Pmech/Pmuscle),
0.26–0.37; and propeller efficiency
(prop=Pdrag/Pmech),
0.15–0.20. Comparison with other studies suggests that labriform
swimming may be more efficient than swimming powered by undulations of the
body axis.
Key words: fish swimming, mechanical power, efficiency
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) or undertake lengthy migrations
(Block et al., 2005;
van Ginneken et al., 2005).
Few estimates of locomotor efficiency are available. The nature of some forms
of locomotion precludes this type of measurement. For example, during level,
terrestrial locomotion, the net work and power per stride are zero
(Cavagna et al., 1977), and
energy is expended on a wide range of mechanical functions
(Ellerby et al., 2005).
Determining overall efficiency on the basis of power inputs and outputs is
therefore not practicable for walking or running. The situation is more
straightforward in swimmers and fliers where the muscles are primarily used to
generate power, accelerating the fluid surrounding them to generate lift and
thrust (Rayner, 1979;
Biewener et al., 1992;
Drucker and Lauder, 1999;
Altringham and Ellerby, 1999).
In systems of this type, the overall efficiency of locomotion can potentially
be determined by measuring metabolic rate and the mechanical power output from
the active muscle tissue.
No single study has quantified the power inputs and outputs for a given
locomotor system. Metabolic rate measurements in flying birds have been
compared to mechanical power estimates derived from aerodynamic models
(Rayner, 1999;
Ward et al., 2001) or measures
of muscle force based on bone strain
(Biewener et al., 1992;
Hedrick et al., 2003) or
measured in vitro (Askew and
Ellerby, 2007). The mechanical power output of fish muscle has
been measured in vitro (Altringham
and Johnston, 1990; Luiker and
Stevens, 1992; Luiker and
Stevens, 1993; Rome et al.,
1993; Coughlin,
2000; Syme and Shadwick,
2002), but these data have not been integrated with measures of
the energy costs of swimming for three main reasons. First, the segmented,
myotomal muscle that powers undulatory swimming has a complex architecture and
properties that change along the body axis
(Altringham and Ellerby, 1999).
Second, the precise role of myotomal muscle remains controversial, in
particular the role of the caudal musculature in power transmission as well as
a power production (van Leeuwen et al.,
1990; Rome et al.,
1993; Altringham and Ellerby,
1999). Third, the level of motor unit recruitment changes with
swimming speed (Rome et al.,
1984; Jayne and Lauder,
1995), but detailed recruitment data are only available for a few
species. With these uncertainties concerning muscle mechanical function and
recruitment levels, muscle power outputs measured in vitro are
difficult to relate to the actual mechanical power requirements of
swimming.
In view of these problems, we measured swimming muscle power in bluegill
sunfish (Lepomis macrochirus Rafinesque). This species swims in the
labriform mode at low speeds, generating thrust by beating its pectoral fins
rather than by undulating its body axis
(Gibb et al., 1994). In fish
of this type, the pectoral girdle muscles form a discrete, thrust-generating
`motor', the properties of which can be quantified more readily than segmented
myotomal muscle. It has been proposed that the labriform swimming mode may be
more economical and efficient than undulatory swimming
(Webb, 1975;
Gordon et al., 1989;
Lighthill and Blake, 1990).
The thrust required to overcome body drag may be up to five times higher in an
undulating body, relative to a rigid body axis, and undulatory swimmers may
experience greater energy losses due to lateral recoil of the body
(Lighthill, 1971;
Webb, 1998). Labriform
swimmers that maintain a rigid body axis may therefore be more economical and
efficient than undulatory swimmers. We hypothesized that bluegill sunfish
Lepomis macrochirus, a species that uses the labriform gait at low
speeds, would be more economical and efficient than swimmers that only utilize
undulatory swimming. In order to test this hypothesis, we measured the
mechanical power output from the major pectoral fin adductor and abductor
muscles in vitro using the work loop technique
(Josephson, 1985) and used
this as a basis for estimating mechanical power output during maximal
labriform swimming. The metabolic power input into this system during maximal
labriform swimming was determined using respirometry. We also estimated the
propeller efficiency of the system, measuring the power required to overcome
body drag in towed fish and expressing it as a proportion of the total
mechanical power available from the pectoral girdle muscles. Our data are
compared to available data from the literature concerning the economy and
efficiency of undulatory swimming.
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Swimming flume
Swimming experiments were carried out at 22°C in a sealable,
recirculating flume (Model 90; Loligo Systems, Hobro, Denmark) capable of
generating flow velocities from 5 to 150 cm s–1. The flume
was composed of an inner chamber, 88.6 liters in volume, with a working
section of 20 cmx20 cmx70 cm and an outer tank that buffered
temperature changes and served as a reservoir of oxygenated water.
Kinematic analysis
Video sequences of seven fish (mass M=152.3±2.8 g, length
L=19.5±0.4 cm, means ± s.e.m.), swimming at speeds
ranging from 0.46 to 2.16 L s–1, were recorded using
a Sony HDR HC-3 camcorder at a frame rate of 120 Hz. 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 fin beat frequencies and upstroke and downstroke
durations during sequences of steady swimming (mean sequence length, 20 fin
beats).
Respirometry
A self-stirring polarographic oxygen probe connected to an Accumet Excel
XL40 Dissolved Oxygen Meter (Fisher Scientific, Pittsburgh, PA, USA) was
inserted through a port in the lid of the sealed flume. This logged the oxygen
concentration in the flume every 15 s. The rate of oxygen consumption
(
O2) was calculated from
the rate of decline of oxygen concentration in the sealed flume. Initial
oxygen concentration measurements were taken in an empty flume to determine
the rate of oxygen consumption by the oxygen electrode and microorganisms in
the flume. These readings were repeated after obtaining data for each fish,
and the empty rate of oxygen consumption subtracted from all
O2 values. Flume volume was
corrected for the volume of water displaced by the fish (calculated from body
mass assuming an average density equal to water). The mass specific
O2=R[(Vflume–Vfish)/M]
mg kg–1 h–1, where R is the
measured rate of oxygen decline in the sealed flume in mg l–1
h–1, Vflume is the flume volume in
liters, Vfish is the volume displaced by the fish, and
M is the body mass of the fish in kg.
Before respirometry experiments the fish were fasted for 48 h to avoid
rises in O2 associated with
digestion, and were allowed to acclimate to the flume chamber overnight.
Resting O2 measurements
were taken over a period of 2 h in the early morning, before the usual
lights-on period, during which time the fish were left in darkness
undisturbed. After 2 h, the lights were switched on and the oxygen probe
removed. A submersible pump was used to circulate oxygenated water through the
flume chamber to elevate the internal oxygen concentration to pre-measurement
levels.
Swimming O2 measurements
were taken at the maximum labriform speed. To avoid disturbing the fish and
ensure steady swimming, the flume was screened by a dark cloth, except for a
small gap to allow observation of the fish. Data were collected for six fish
(mass 156.9±12.9 g, length 19.3±0.4 cm, means ± s.e.m.),
from which kinematic data had been previously obtained. Fish swam for 40 min
at their maximal labriform speed, over which time the oxygen levels in the
flume fell by less than 10%. Data were excluded from the analysis if the fish
swam consistently within 5 cm of the wall of the working section. A linear
regression line was fitted to the last 30 min of the swimming oxygen trace,
allowing 10 min for the fish to reach steady state. Segments where the
coefficient of determination for the linear regression was less than 0.95 were
excluded from the analysis.
Muscle power measurements
The maximum mechanical power output (Pmech) of the two
largest muscles powering the pectoral fin upstroke (adductor profundus) and
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.
Fish were anesthetized using buffered MS222 solution at a concentration of 100 mg l–1 and placed in a shallow plastic container with aerated anesthetic solution circulating over their gills via a submersible pump. The scales were removed from the area overlying the pectoral fin musculature. An L-shaped skin incision posterior and ventral to the pectoral muscles was made using a scalpel, and the skin covering the muscles lifted away from the underlying tissue by blunt dissection with a surgical probe. This exposed the abductor superficialis, a muscle that originates on the anterolateral cleithrum and inserts via tendons onto the fin rays of the pectoral fin. The muscle consists of a number of discrete muscle fascicles, each terminating on a fin ray tendon. A loop of silk suture was passed under the tendon of one fascicle and knotted securely in place. The tendon was cut distal to the knot and the silk thread used to gently elevate the distal end of the muscle fascicle while freeing it from surrounding tissue with a scalpel. The section of the cleithrum around the insertion of the fascicle was cut with bone shears and the intact fascicle removed.
Fascicles were also removed from the adductor profundus, a muscle originating on the medial coracoid and ventromedial cleithrum and, like the abductor superficialis, inserting via tendons onto fin rays at the base of the pectoral fin. To obtain a fascicle from this muscle, the entire pectoral girdle was removed allowing access to its medial muscles. The procedure for removing a fascicle was as described for the abductor superficialis.
After removal, the fascicle was immediately placed in 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. If necessary, further muscle tissue was removed so that the diameter of the preparation did not exceed 0.5 mm. The tendon was tied to a stiff, steel hook made from an insect pin and hooked to the lever arm of the muscle lever. The bony origin was clamped to a stainless steel arm, suspending the fascicle vertically between the clamp and the lever arm of an ergometer. The muscle tissue was submerged in a water-jacketed tissue chamber containing oxygenated physiological saline. The temperature of the saline was raised from 5°C to 22°C over a period of 20 min.
Muscle power measurements were made using a muscle ergometer (300B-LR, Aurora Scientific, 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. 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). At the fin beat cycle frequency used during maximal labriform swimming (2.8 Hz), muscle strain and relative timing and duration of activation were systematically changed until the maximum power output was measured. 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). After every three work loop measurements a set of control work loops were run to check for any decline in performance by the preparation. The decline between controls was used to correct the power outputs measured during the intervening work loops. 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 12 muscle fascicles in total (six from the abductor superficialis and six from the adductor profundus). These were obtained from 11 fish (mass 154.1±8.2 g, length 19.5±0.2 cm, means ± s.e.m.). In one case, a fascicle was successfully removed from both muscles in a single individual. In all other cases, a fascicle was removed from just one muscle in a given individual.
Drag measurements
Drag measurements were made using fish euthanized by anesthetic overdose
(400 mg l–1 MS222). Data were collected for three fish (mass
155.1±9.9 g, length 19.4±0.4 cm, means ± s.e.m.). In
order to reproduce fish body posture during labriform swimming, the fish were
laid on a recessed foam surface. The recess ensured that the spinal column was
straight. To further maintain this position during the onset of rigor a
20-gauge steel rod was inserted via the mouth and through the body
tissues parallel and ventral to the spinal column. The fins were arranged in
the posture typically maintained during labriform swimming, apart from the
pectoral fins, which were positioned along the lateral body surface. Fish were
only used for drag analysis if this produced a posture that did not create
lateral oscillations when towed behind the force transducer.
Force measurements were made using a Grass FT03 force-displacement transducer (Grass Instruments, West Warwick, RI, USA). The voltage output was amplified by a ETH-200 transducer amplifier (Grass Instruments) and captured to a PC via an A-to-D card. The transducer was mounted vertically above the flume with a 9.5 cm extension made from a stiff 1 mm diameter stainless-steel rod projecting into the water. The unloaded force transducer output was recorded at a flume speed of 0.24 m s–1, equivalent to the mean maximal labriform swimming speed. The fish were then attached to the distal end of the rod by a 2 cm length of fishing line and the force output of the transducer recorded at the same speed. The drag force on the fish was determined by subtracting the drag force acting on the transducer extension and thread from the total drag force.
Statistical analyses
All statistical analyses were carried out using SPSS (Version 14.0, SPSS,
Chicago, USA). The mechanical properties and stimulus parameters for
maximizing power output of the adductor profundus and abductor superficialis
were compared using unpaired t-tests. A general linear model (GLM)
including a fish identifier was used to compare pectoral fin upstroke and
downstroke durations at the maximum labriform swimming speed.
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) detected a slight asymmetry in the relative pectoral fin
upstroke and downstroke durations at the gait transition (approximately
0.43:0.37 upstroke:downstroke). On the basis of our measurements a sinusoidal
strain wave with equal lengthening and shortening durations was used to
approximate in vivo strain trajectories during in vitro
muscle power measurements.
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Muscle mechanical properties
No significant difference was detected between the maximum power output of
the abductor superficialis and adductor profundus (t-test, d.f.=10,
P=0.07). The muscle power data were therefore pooled to calculate a
mean overall power output from the muscles. The maximum power output of these
muscles with a sinusoidal strain trajectory at a cycle frequency of 2.8 Hz was
16.5±2.4 W kg–1 (mean ± s.e.m., N=12,
6 abductor superficialis and 6 adductor profundus,
Fig. 2). Isometric properties
of the two muscles and the strain and stimulus parameters used to obtain
maximum power output at 2.8 Hz strain cycle frequency are shown in
Table 1. Maximum isometric
stress is similar to that previously measured in the pectoral musculature of a
related species, the pumpkinseed sunfish Lepomis gibbosus
(Luiker and Stevens, 1992;
Luiker and Stevens, 1993).
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There are two potential sources of error in our approach for determining the mechanical power required for maximal labriform swimming in this species. First, that the muscles may not be producing their maximum power output in vivo and that our measurements of maximum power in vitro are not representative of performance during maximal labriform swimming, and second, that we have not accounted for the power available from the total pectoral girdle muscle mass.
There are a number of lines of evidence suggesting that peak power output
is reached during maximal labriform swimming. First, the pectoral fin beat
frequency used just prior to the gait transition maximizes pectoral muscle
mechanical power output in this species
(Kendall et al., in press).
Second, the momentum transferred to the wake by the beating pectoral fins is
maximized at the gait transition in this species, and shows no capacity for
increased power transfer to the wake above the transition speed
(Drucker and Lauder, 1999).
Third, the intensity of EMGs in the abductor superficialis muscle does not
change across the gait transition, showing that there is no capacity for
additional recruitment of motor units and increased force production in this
muscle (E.A.J., unpublished data). It is therefore likely that the pectoral
girdle muscles are operating at, or near, their maximum power output at the
gait transition, and our in vitro measurements are a reasonable
measure of in vivo performance during maximal labriform swimming. In
this regard the bluegill pectoralis muscles may be similar to muscles in other
systems that demand high mechanical powers, where the relationship between
strain trajectory and activation recorded in vivo has been shown
in vitro to correspond to that which is optimal for maximizing power
output (Askew and Marsh, 2001;
Girgenrath and Marsh,
1999).
The pectoral girdle muscles were 1.28±0.08% (mean ± s.e.m.,
N=5, Table 2) of the
total body mass of the fish. During maximal labriform swimming in this
species, thrust is generated during both adduction and abduction
(Drucker and Lauder, 1999;
Drucker and Lauder, 2000).
Muscle activity and kinematic data from other perciform species suggest that
the abductors superficialis and profundus are the major sources of mechanical
power during fin abduction (Drucker and
Jensen, 1997; Westneat and
Walker, 1997; Lauder et al.,
2006). The anatomical arrangement of, and the relationship
between, activity and fin movement for these muscles suggests that they are
active while shortening, and therefore doing positive work on the fin and
surrounding water to generate lift and thrust. The role of the arrector
ventralis is less clear. This muscle inserts on the fin ray and could
potentially power abduction. However, its activity largely coincides with the
reversal between adduction and abduction
(Drucker and Jensen, 1997;
Westneat and Walker, 1997). It
may therefore play a role in decelerating the fin at the end of adduction, as
well as powering abduction.
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Activity in the adductor profundus coincides with fin adduction, and like
the large abductors, its anatomical arrangement and relationship between
activity and fin movement suggests activity during shortening, and therefore
the production of positive work (Drucker
and Jensen, 1997; Westneat and
Walker, 1997). The anatomy and activity patterns of the arrector
dorsalis also suggest a role in power production during adduction
(Westneat and Walker, 1997).
The contribution of the abductor superficialis to power production during
abduction is less certain. The posterior, superficial portion of the muscle
inserts on the posterior fin rays and its fascicles run perpendicular to the
fascicles of the abductor profundus. This part of the muscle is likely to be
involved in controlling the orientation of the fin, rather than powering
abduction. The ventral portion of the abductor superficialis inserts on the
anterior fin rays and has fascicles lying parallel to those of the abductor
profundus. This part of the muscle could do positive work when active during
abduction, but is also active during late adduction and pauses between fin
beats (Drucker and Jensen,
1997).
In view of these uncertainties regarding muscle function, a range of
estimates for the mechanical power, Pmech, supplied by the
pectoral girdle muscles during maximal labriform swimming will be used to
calculate efficiency. If the entire pectoral girdle musculature
(Table 2) supplied the maximum
measured power output, the available mechanical power output would be 0.21 W
kg–1 body mass. Given the available data concerning muscle
recruitment (Drucker and Jensen,
1997; Westneat and Walker,
1997) this is unlikely to occur, but it will allow us to set an
upper limit to our efficiency estimates. Based on the anatomy of the muscles
and recruitment data from other labriform swimmers
(Drucker and Jensen, 1997;
Westneat and Walker, 1997) the
mass of muscle likely supplying power in this species is 0.92±0.04%
(mean ± s.e.m., N=5) of the total body mass of the fish. This
is the total mass of the adductors superficialis and profundus, the abductor
profundus and arrector ventralis. The two muscles for which we have power
output measurements constitute 75% of the total mass of this group. If the
mass-specific power output of the smaller muscles is assumed to be equal to
that of the abductor superficialis and adductor profundus, then this mass of
power producing muscle could supply 0.15 W kg–1 body mass.
This Pmech range 0.15–0.21 W kg–1
body mass will be used in subsequent efficiency calculations.
Metabolic rate
Fig. 3 shows representative
flume oxygen content traces at rest and during labriform swimming. Standard
metabolic rate (SMR) was 98.2±15.5 mg O2
kg–1 h–1 (mean ± s.e.m.,
N=6). Swimming O2
at the maximum labriform speed was 250.4±21 mg O2
kg–1 h–1 (mean ± s.e.m.,
N=6). Oxygen consumption was converted to energy units using an
oxycaloric value of 13.54 J mg–1
(Brett and Groves, 1979). The
total metabolic power input during maximal labriform swimming,
Ptotal, was 0.95 W kg–1 body mass. The
net metabolic requirements of swimming were estimated by subtracting resting
O2 from total swimming
O2. This subtracts out the
energy requirements of maintenance processes not directly associated with
swimming and provides an estimate of the energy expenditure of the active
pectoral girdle muscles. The mean net power input for maximal labriform
swimming, Pmuscle, was 0.57 W kg–1 body
mass.
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Body drag
The drag force measured at the maximum labriform swimming speed (0.24 m
s–1) was 18.3±1.6 mN (mean ± s.e.m.,
N=4). The mean power required to overcome body drag
(Pdrag) for the fish used in the drag measurements was
0.028 W kg–1 body mass.
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gross=Pmech/Ptotal)
for bluegill swimming at their maximum labriform speed fell in the range
0.16–0.22 for the lower and upper estimates of
Pmech, respectively. As the present study is the first
integrated attempt to measure both the power outputs and inputs in any fish
species, few data are available for comparison. There are data available from
separate studies of yellowfin tuna (Thunnus albacares) and Pacific
bonito (Sarda chiliensis) swimming metabolism
(Dewar and Graham, 1994;
Sepulveda et al., 2003) and
in vitro muscle power output
(Altringham and Block, 1997),
where both types of data were obtained at the same temperature, allowing
overall efficiency to be estimated for these species. Swimming at a tail beat
frequency of 3 Hz, bonito
O2 was equivalent to a
power input of 3.6 W kg–1 body mass at 18°C
(Sepulveda et al., 2003). The
muscle mass-specific power output of bonito slow muscle at this cycle
frequency and temperature was approximately 8.8 W kg–1
(Altringham and Block, 1997);
no data are available for muscle power at 18°C, but power–frequency
curves constructed at 15°C and 20°C coincide at a 3 Hz cycle
frequency. Slow muscle makes up 4.51% of the bonito body mass
(Graham et al., 1983), so the
body mass-specific mechanical power output potentially available to the 1.191
kg bonito in the energetics study was approximately 0.40 W
kg–1. Based on these data, the overall efficiency of a bonito
is therefore 0.11. A similar calculation for yellowfin tuna [power input of
4.11 W kg–1 body mass at 4 Hz tailbeat frequency
(Dewar and Graham, 1994);
muscle mass specific power output 7.5 W kg–1 at 4 Hz
(Altringham and Block, 1997);
slow muscle mass 6.51% of body mass
(Graham et al., 1983); body
mass-specific power output 0.49 W kg–1 in a 2.17 kg fish at
25°C] yields an overall efficiency of 0.12.
These efficiency estimates are lower than those obtained for labriform
swimming in bluegill (0.16–0.22). Based on the available data it appears
that labriform swimming in bluegill may be more efficient overall than
undulatory swimming in the bonito and yellowfin tuna. There are, however, a
number of reasons why these estimates of undulatory swimming efficiency should
be viewed with caution. First, the mass specific power output data are from
single muscle preparations, so they may not be representative of muscle
performance in the fish from which metabolic data were obtained. Second, the
muscle power measurements are point measures of performance. Muscle properties
are likely to vary with axial location
(Altringham and Ellerby, 1999),
and these point measures may not be indicative of the properties of the whole
muscle mass. Third, the strains applied to the muscle preparations were not
based on in vivo strains as they preceded direct in vivo
measurements by sonomicrometry (Ellerby et
al., 2000; Katz et al.,
2001), and the measured powers may only approximate in
vivo performance. Finally, the muscle power data were obtained from
supra-maximally stimulated muscle. The mechanical power data are therefore
most meaningfully compared to maximal metabolic rate data where the aerobic
capacity of the animal, and presumably its capacity to generate power from its
aerobic muscles, have been reached. It is not clear that the metabolic rate
data are maximal; therefore comparing maximal muscle powers to sub-maximal
metabolism may have overestimated efficiency. In view of these uncertainties,
further data concerning muscle performance and metabolism in both labriform
and undulatory swimmers are required before this difference in overall
efficiencies can be confirmed. Muscle performance and metabolic cost data are
required from integrated studies of undulatory swimming. Additionally, direct
muscle strain data for the pectoral girdle muscles of labriform swimmers are
required to precisely determine the mechanical functions of all the muscles
inserting on the pectoral fins.
While data concerning swimming efficiency are scarce, several studies have
quantified changes in swimming costs and economy within individual species
that transition from labriform or ballistiform swimming at low speeds to
undulatory swimming at high speeds (Brett
and Sutherland, 1965; Parsons
and Sylvester, 1992; Korsmeyer
et al., 2002). These do not show a consistent pattern concerning
the relative economy of these gaits measured as cost of transport (COT, the
energy required to travel a unit distance). In the pumpkinseed sunfish
Lepomis gibbosus (Brett and
Sutherland, 1965) and triggerfish Rhinecanthus aculeatus
(Korsmeyer et al., 2002) there
was no clear change in COT on the transition from paired-fin based, to
undulatory swimming. An increase in the slope of the metabolic rate
vs speed relationship in triggerfish was detected
(Korsmeyer et al., 2002),
indicating an increase in incremental cost on switching to undulatory
swimming, but the overall COT range measured for each gait was similar. In
contrast, the transition from labriform to undulatory swimming in the white
crappie Pomoxis annularis
(Parsons and Sylvester, 1992)
resulted in a clear decrease in COT. Unfortunately, without data concerning
muscle power output, the relative efficiency of different gaits within these
species cannot be determined.
The only other locomotor system for which estimates of power outputs and
inputs are available is avian flight. This system is similar to labriform
swimming in that the majority of the active muscle mass is concerned with
generating power to accelerate a fluid. Estimates of avian whole organism
efficiency based on aerodynamic estimates of mechanical power range from 0.12
to 0.2 (Rayner, 1999),
comparable to the estimates of whole organism efficiency we have obtained for
bluegill. It may be that this overall efficiency range is common to locomotor
systems in which the acceleration of a fluid is the main function of the
locomotory muscles.
Muscle efficiency estimates
(muscle=Pmech/Pmuscle)
for bluegill swimming at their maximum labriform speed fell into the range of
0.37 to 0.26, based on the upper and lower estimates of available mechanical
power, respectively. The latter figure is probably more realistic as the
entire pectoral girdle muscle mass is unlikely to be supplying mechanical
power. This approach is analogous to that used to determine efficiency during
human cycle ergometer exercise, where resting metabolic costs are subtracted
from total metabolism to estimate energy expenditure by the active muscles.
For this activity, muscle efficiency estimates range from 0.18 to 0.23
(Gaesser and Brooks, 1975;
Luthanan et al., 1987). Our
estimates also fall within the range obtained for vertebrate muscle in
vitro (reviewed by Smith et al.,
2005). The efficiency of skeletal muscle crossbridges in
transducing chemical to mechanical energy is 0.36–0.38
(Reggiani et al., 1997;
He et al., 1999). This
represents an upper limit for possible whole muscle efficiency. Given this
constraint, and the similar efficiency values measured in other muscles, our
efficiency estimate for bluegill pectoralis girdle muscles seems reasonable,
supporting our approach as a means of estimating in vivo mechanical
power in this system.
A portion of the total mechanical power (Pdrag) is used
to generate thrust to overcome body drag. Pdrag is the
product of the drag force acting on the fish's body and swimming velocity.
Based on our measured value for Pdrag (0.028 W
kg–1), and the range of mechanical power output estimates,
propeller efficiency (Pdrag/Pmech)
fell in the range 0.15–0.20. This propeller efficiency range is lower
than that previously calculated for this species using flow visualization as a
means of measuring mechanical power transferred to the wake (0.39)
(Drucker and Lauder, 1999).
This may in part be due to differences in the methods used to measure body
drag between the two studies. Initial attempts to measure drag in anesthetized
fish in a similar way to Drucker and Lauder
(Drucker and Lauder, 1999)
were abandoned due to `flagging' of the body and fins. In the absence of
muscle tone, oscillations of the body axis and fins increased the drag acting
on fish. By measuring drag on dead fish that had gone into rigor these effects
were reduced. This may account for our measured drag powers being a lower
proportion of total mechanical power. An additional factor is that propeller
efficiency in bluegill may change with swimming speed. Our estimates were
obtained at 1.2 L s–1 relative to 0.5 L
s–1 in the previous study
(Drucker and Lauder, 1999).
Power not accounted for as Pthrust is used to impart
lateral momentum to the water for stabilization
(Drucker and Lauder, 1999),
overcome drag on the pectoral fins themselves, and overcome energy losses in
the linkages between the muscles and fin rays.
The potential efficiency and economy of swimming fish is a major factor in
the use of biological designs to inspire swimming robotic vehicles
(Fish, 2006;
Triantafyllou et al., 2000).
Given the interest in developing biomimetic autonomous underwater vehicles
(AUVs), it is important to place our performance data in context with that of
existing AUVs and other fish species. For AUVs, economy may be more important
than efficiency per se. In battery-powered vehicles minimizing the
rate of energy expenditure extends operational duration and range. COT is
therefore an important basis for comparison. In the present study, bluegill
had a COT of 3.9 J kg–1 m–1 during maximal
labriform swimming. This is similar to the COT of robot Madeleine, a flapping
foil powered, biologically inspired, robot [4.0 J kg–1
m–1 (Long et al.,
2006)]. Fish that swim by undulating their body axes have a wide
range of COT values, from 0.4 to 5 J kg–1
(Webb, 1971;
Brett, 1973;
Dewar and Graham, 1994;
Reidy et al., 2000;
van Ginneken et al., 2005;
Claireaux et al., 2006).
Propeller-driven systems appear to be more economical than most swimming fish.
The COT of a typical propeller-driven AUV is approximately 0.4 J
kg–1 m–1
(Allen et al., 1997). Fish and
robots powered by flapping fins appear to fall at the upper end of the COT
range exhibited by swimmers. So while labriform swimmers may be efficient in
terms of the ratio of power input:power output during swimming, they may not
be as economical as undulatory swimmers in turning that power output into
forward velocity. At present, the main advantage in pursuing a biomimetic
approach to AUV design may be improved maneuverability relative to propeller
driven designs (Bandyopadhyay et al.,
1997), rather than improved efficiency or economy.
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Allen, B., Stokey, R., Austin, T., Forrester, N., Goldsborough, R., Purcell, M. and von Alt, C. (1997). REMUS: a small, low cost AUV; system description, field trials and performance results. In OCEANS `97. MTS/IEEE Conference Proceedings, IEEE Oceans Conference, Halifax, NS, Canada, pp.994 -1000, doi:10.1109/OCEANS.1997.624126 .
Altringham, J. D. and Block, B. A. (1997). Why do tuna maintain elevated slow muscle temperatures: power output of muscle isolated from endothermic and ectothermic fish. J. Exp. Biol. 200,2617 -2627.[Abstract]
Altringham, J. D. and Ellerby, D. J. (1999). Fish swimming: patterns in muscle function. J. Exp. Biol. 202,3397 -3403.[Abstract]
Altringham, J. D. and Johnston, I. A. (1990).
Modelling muscle power output in a swimming fish. J. Exp.
Biol. 148,395
-402.
Askew, G. N. and Ellerby, D. J. (2007). The power requirements of avian flight. Biol. Lett. 3, 445-448.[CrossRef][Medline]
Askew, G. N. and Marsh, R. L. (2001). The
mechanical power output of the pectoralis muscle of blue-breasted quail
(Coturnix chinensis): the in vivo length cycle and its
implications for muscle performance. J. Exp. Biol.
204,3587
-3600.
Bandyopadhyay, P. R., Castano, J. M., Rice, J. Q., Philips, R. B., Nedderman, W. H. and Macy, W. K. (1997). Low-speed maneuvering hydrodynamics of fish and small underwater vehicles. J. Fluids Eng. 119,136 -144.
Biewener, A. A., Dial, K. P. and Goslow, G. E., Jr
(1992). Pectoralis muscle force and power output during flight in
the starling. J. Exp. Biol.
164, 1-18.
Block, B. A., Teo, S. L. H., Walli, A., Boustany, A., Stokesbury, M. J. W., Farwell, C. J., Weng, K. C., Dewar, H. and Williams, T. D. (2005). Electronic tagging and population structure of Atlantic bluefin tuna. Nature 434,1121 -1127.[CrossRef][Medline]
Brett, J. R. (1973). Energy expenditure of sockeye salmon, Oncorhynchus nerka, during sustained performance. J. Fish. Res. Board Can. 30,1799 -1809.
Brett, J. R. and Groves, T. D. D. (1979). Physiological energetics. In Fish Physiology. Vol.VIII (ed. W. S. Hoar, D. J. Randall and J. R. Brett), pp. 280-352. New York: Academic Press.
Brett, J. R. and Sutherland, D. B. (1965). Respiratory metabolism of pumpkinseed (Lepomis gibbosus) in relation to swimming speed. J. Fish. Res. Board Can. 22,405 -409.
Cavagna, G. A., Heglund, N. C. and Taylor, C. R. (1977). Mechanical work in terrestrial locomotion. II. Basic mechanisms for minimizing energy expenditure. Am. J. Physiol. 233,R243 -R261.[Medline]
Claireaux, G., Couturier, C. and Groison, A.-L.
(2006). Effect of temperature on swimming speed and cost of
transport in juvenile European sea bass. J. Exp. Biol.
209,3420
-3428.
Coughlin, D. J. (2000). Power production during steady swimming in largemouth bass and rainbow trout. J. Exp. Biol. 203,617 -629.[Abstract]
Dewar, H. and Graham, J. B. (1994). Studies of tropical tuna swimming performance in a large water tunnel. I. Energetics. J. Exp. Biol. 192,13 -31.[Abstract]
Drucker, E. G. and Jensen, J. S. (1997). Kinematic and electromyographic analysis of steady pectoral fin swimming in the surfperches. J. Exp. Biol. 200,1709 -1723.[Abstract]
Drucker, E. G. and Lauder, G. V. (1999). Locomotor forces on a swimming fish: three-dimensional vortex wake dynamics quantified using digital particle image velocimetry. J. Exp. Biol. 202,2392 -2412.
Drucker, E. G. and Lauder, G. V. (2000). A hydrodynamic analysis of fish swimming speed: wake structure and locomotor force in slow and fast labriform swimmers. J. Exp. Biol. 203,2379 -2393.[Abstract]
Ellerby, D. J., Altringham, J. D., Williams, T. and Block, B. A. (2000). Slow muscle function of Pacific bonito (Sarda chiliensis) during steady swimming. J. Exp. Biol. 203,2001 -2013.[Abstract]
Ellerby, D. J., Henry, H. T., Carr, J. A., Buchanan, C. I. and
Marsh, R. L. (2005). Blood flow in guinea fowl Numida
meleagris as an indicator of energy expenditure by individual muscles
during walking and running. J. Physiol. Lond.
564,631
-648.
Fish, F. E. (2006). Limits of nature and advances of technology: what does biomimetics have to offer to aquatic robots? Appl. Bionics Biomech. 3, 49-60.[CrossRef]
Gaesser, G. A. and Brooks, G. A. (1975).
Muscular efficiency during steady rate exercise: effects of speed and work
rate. J. Appl. Physiol.
38,1132
-1139.
Gibb, A. C., Jayne, B. C. and Lauder, G. V. (1994). Kinematics of pectoral fin locomotion in the bluegill sunfish Lepomis macrochirus. J. Exp. Biol. 189,133 -161.[Abstract]
Girgenrath, M. and Marsh, R. L. (1999). Power output of sound-producing muscles in the tree frogs Hyla versicolor and Hyla chrysoscelis. J. Exp. Biol. 202,3225 -3237.[Abstract]
Gordon, M. S., Chin, H. G. and Vojkovich, M. (1989). Energetics of swimming in fish using different modes of locomotion. Fish Physiol. Biochem. 6, 341-352.[CrossRef]
Graham, J. B., Koehrn, F. J. and Dickson, K. A. (1983). Distribution and relative proportions of red muscle in scombrid fishes: consequences of body size and relationships to locomotion. Can. J. Zool. 61,2087 -2096.
He, Z.-H., Chillingworth, R. K., Brune, M., Corrie, J. E. T.,
Webb, M. R. and Ferenczi, M. A. (1999). The efficiency of
contraction in rabbit skeletal muscle fibres, determined from the rate of
release of inorganic phosphate. J. Physiol. Lond.
517,839
-854.
Hedrick, T. L., Tobalske, B. W. and Biewener, A. A.
(2003). How cockatiels (Nymphicus hollandicus) modulate
pectoralis power output across flight speeds. J. Exp.
Biol. 206,1363
-1378.
Jayne, B. C. and Lauder, G. V. (1995). Red muscle motor patterns during steady swimming in largemouth bass: effects of speed and correlations with axial kinematics. J. Exp. Biol. 198,1575 -1587.[Medline]
Josephson, R. K. (1985). Mechanical power
output from striated muscle during cyclic contractions. J. Exp.
Biol. 114,493
-512.
Katz, S. L., Syme, D. A. and Shadwick, R. W. (2001). Enhanced power in yellowfin tuna. Nature 410,770 -771.[CrossRef][Medline]
Kendall, J. L., Lucey, K. S., Jones, E. A., Wang, J. and Ellerby, D. J. (in press). Mechanical and energetic factors driving gait transitions in bluegill sunfish (Lepomis macrochirus). J. Exp. Biol.
Korsmeyer, K. E., Steffensen, J. F. and Herskin, J.
(2002). Energetics of median paired fin swimming, body and caudal
fin swimming, and gait transition in parrotfish (Scarus schegeli) and
triggerfish (Rhinecanthus aculeatus). J. Exp.
Biol. 205,1253
-1263.
Lauder, G. V., Madden, P. G. A., Mittal, R., Dong, H. and Bozkutrttas, M. (2006). Locomotion with flexible propulsors. I. Experimental analysis of pectoral fin swimming in sunfish. Bioinspir. Biomim. 1,S25 -S34.[CrossRef][Medline]
Lighthill, M. J. (1971). Large-amplitude elongated body theory of fish locomotion. Proc. R. Soc. Lond. B Biol. Sci. 179,125 -138.
Lighthill, M. J. and Blake, R. (1990). Biofluid dynamics of balistiform and gymnotiform locomotion. Part 1. Biological background, and analysis by elongated body theory. J. Fluid Mech. 212,183 -207.[CrossRef]
Long, J. H., Jr, Schumacher, J., Livingston, N. and Kemp, M. (2006). Four flippers or two? Tetrapodal swimming with an aquatic robot. Bioinspir. Biomim. 1, 20-29.[CrossRef][Medline]
Luiker, E. A. and Stevens, E. D. (1992). Effects of stimulus frequency and duty cycle on force and work in fish muscle. Can. J. Zool. 70,1135 -1139.
Luiker, E. A. and Stevens, E. D. (1993). Effects of stimulus train duration and cycle frequency on the capacity to do work in the pectoral fin muscle of the pumpkinseed sunfish, Lepomis gibbosus. Can. J. Zool. 71,2185 -2189.
Luthanan, P., Rahkila, P., Rusko, H. and Viitasalo, J. T. (1987). Mechanical work and efficiency in ergometer bicycling at aerobic and anaerobic thresholds. Acta. Physiol. Scand. 131,331 -337.[Medline]
Parsons, G. R. and Sylvester, J. L., Jr (1992). Swimming efficiency of the White Crappie, Pomoxis annularis.Copeia 4,1033 -1038.
Pettersson, L. B. and Hedenstrom, A. (2000). Energetics cost reduction and functional consequences of fish morphology. Proc. R. Soc. Lond. B Biol. Sci. 267, 759.[Medline]
Rayner, J. M. V. (1979). Vortex theory of animal flight. II. Forward flight of birds. J. Fluid Mech. 91,731 -763.[CrossRef]
Rayner, J. M. V. (1999). Estimating power curves of flying vertebrates. J. Exp. Biol. 202,3449 -3461.[Abstract]
Reggiani, C., Potma, E. J., Bottinelli, R., Canepari, M., Pellegrino, M. A. and Stienen, G. J. M. (1997). Chemo-mechanical energy transduction in relation to myosin isoform composition in skeletal muscle fibres of the rat. J. Physiol. Lond. 502,449 -460.[CrossRef][Medline]
Reidy, S. P., Kerr, S. R. and Nelson, J. A. (2000). Aerobic and anaerobic swimming performance of individual atlantic cod. J. Exp. Biol. 203,347 -357.[Abstract]
Rome, L. C., Loughna, P. T. and Goldspink, G. (1984). Muscle fiber activity in carp as a function of swimming speed and muscle temperature. Am. J. Physiol. 247,R272 -R279.[Medline]
Rome, L. C., Swank, D. and Corda, D. (1993).
How fish power swimming. Science
261,340
-343.
Sepulveda, C. A., Dickson, K. A. and Graham, J. B.
(2003). Swimming performance studies on the eastern Pacific
bonito Sarda chiliensis, a close relative of the tunas (family
Scombridae). I. Energetics. J. Exp. Biol.
206,2739
-2748.
Smith, N. P., Barclay, C. J. and Loiselle, D. S. (2005). The efficiency of muscle contraction. Prog. Biophys. Mol. Biol. 88,1 -58.[CrossRef][Medline]
Syme, D. A. and Shadwick, R. E. (2002). Effects
of longitudinal body position and swimming speed on mechanical power of deep
red muscle from skipjack tuna (Katsuwonus pelamis). J.
Exp. Biol. 205,189
-200.
Triantafyllou, M. S., Triantafyllou, G. S. and Yue, D. K. P. (2000). Hydrodynamics of fishlike swimming. Annu. Rev. Fluid Mech. 32,33 -53.[CrossRef]
van Ginneken, V., Antonissen, E., Muller, U. K., Booms, R.,
Eding, E., Verreth, J. and van den Thillart, G. (2005). Eel
migration to the Sargasso; remarkably high swimming efficiency and low energy
costs. J. Exp. Biol.
208,1329
-1335.
van Leeuwen, J. L., Lankheet, M. J. M., Akster, H. A. and Osse, J. W. M. (1990). Function of red axial muscles in carp (Cyprinus carpio L.): recruitment and normalised power output during swimming in different modes. J. Zool. Lond. 220,123 -145.
Ward, S., Moller, U., Rayner, J. M. V., Jackson, D. M., Bilo,
D., Nachtigall, W. and Speakman, J. R. (2001). Metabolic
power, mechanical power and efficiency during wind tunnel flight by the
European starling Sturnus vulgaris. J. Exp. Biol.
204,3311
-3322.
Webb, P. W. (1971). The swimming energetics of
trout. II. Oxygen consumption and swimming efficiency. J. Exp.
Biol. 55,521
-540.
Webb, P. W. (1975). Hydrodynamics and energetics of fish propulsion. Bull. Fish. Res. Board Can. 190,109 -119.
Webb, P. W. (1998). Swimming. In The Physiology of Fishes (ed. D. H. Evans), pp.3 -24. Boca Raton, FL: CRC Press.
Westneat, M. W. and Walker, J. A. (1997). Motor patterns of labriform locomotion: kinematic and electromyographic analysis of pectoral fin swimming in the labrid fish Gomphosus varius. J. Exp. Biol. 200,1881 -1893.[Abstract]
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