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First published online November 30, 2007
Journal of Experimental Biology 210, 4265-4271 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.009498
Mechanical and energetic factors underlying gait transitions 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 23 September 2007
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Key words: swimming, power, metabolic rate, cost of transport
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). The underlying reasons for gait changes in swimming animals
are less well understood, although it is likely that similar factors are
important.
Bluegill sunfish (Lepomis macrochirus) swim in the labriform mode
at low speeds, generating lift and thrust by beating their pectoral fins
(Gibb et al., 1994;
Drucker and Lauder, 2000;
Lauder et al., 2007;
Jones et al., 2007). As
swimming speed increases, they change gait from labriform swimming to combined
use of their pectoral fins and undulations of the body axis. Pectoral fin
movements are powered and controlled by a number of pectoral girdle muscles.
Undulations of the body axis are powered by the segmented myotomal
musculature. It is unclear whether mechanical or energetic factors drive this
gait transition. The switch in swimming style may be driven by a need to
recruit additional muscle mass as speed increases, or, at higher speeds,
undulatory swimming may be more economical than the labriform gait.
The energetic costs of swimming have been determined in a number of similar
species that change gait from a median paired fin (MPF) gait at low speeds to
an undulatory gait at higher speeds (Brett
and Sutherland, 1965; Parsons
and Sylvester, 1992; Korsmeyer
et al., 2002). For any given species, however, the factors driving
gait changes can only be fully understood if both the metabolic power inputs
and the available muscle power have been quantified across the gait
transition. By taking an integrated approach to studying the gait change in
bluegill sunfish, we have examined both the energetic and mechanical factors
underlying a fish gait change for the first time.
Using respirometry to measure swimming costs, and in vitro measurements of muscle power output, we have determined the energetic consequences of changing gait and the limits to mechanical power output by the pectoral girdle muscles that power labriform swimming. This has enabled us to test two hypotheses concerning the factors underlying the bluegill gait change. First, that, as swimming speed increases, the power available from the pectoral girdle muscles can no longer meet the increasing power requirements of swimming, necessitating the recruitment of the myotomal musculature. In order to test this hypothesis we measured the mechanical power available from the two largest pectoral girdle muscles that power the pectoral fin upstroke and downstroke across a range of pectoral fin beat frequencies spanning the gait transition. The absence of an increase in the available pectoral mechanical power across the gait transition would support the hypothesis that power constraints drive the gait change. Second, we hypothesized that at the upper end of the labriform speed range, this swimming mode becomes uneconomical relative to undulatory swimming, and that a change in swimming style maximizes swimming economy. In order to test this, we used respirometry to measure the metabolic costs of swimming across the gait transition. A decrease in the cost of transport on switching to undulatory swimming would show that energetic factors drive the gait change.
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Swimming flume
Swimming experiments were carried out 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 comprised an inner
chamber 88.6 liters in volume with a working section of 20x20x70
cm and an outer tank that buffered temperature changes and served as a
reservoir of oxygenated water. Water temperature was maintained at 22°C
for all experiments.
Kinematic analysis
Video sequences of seven fish [mass 134.7±13.4 g; length
(L) 19.5±0.4 cm; mean ± s.e.m.] were recorded using a
Sony HDR HC-3 camcorder at a frame rate of 120 Hz swimming at speeds ranging
from 0.10 to 0.27 m s–1. 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 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 were subsequently subtracted from all fish
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). 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. Standard metabolic rate (SMR) measurements were taken over 2 h in
the early morning, before the usual lights-on period, during which time the
fish were left undisturbed in darkness. During these periods the fish
typically remained motionless, resting on the bottom of the working section.
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 made at a range of speeds spanning the
labriform–undulatory transition. To avoid disturbing the fish and ensure
steady swimming, the flume was screened by a dark cloth with a small gap to
allow observation of the fish. Data were collected for nine fish
(M=127.9±4.2 g, L=19.3±0.4 cm). Fish swam for
up to 40 min at each 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 at each speed. Segments
where the coefficient of determination was less than 0.95 were excluded from
the analysis. Measurements were taken at three to four speeds each day with
flushing to replenish oxygen levels between each speed. The fish were then
left to recover overnight before further measurements were taken.
Muscle power measurements
Fish were anesthetized using buffered MS-222 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. These two muscles were selected as they are the single largest
adductor and abductor muscles, constituting about half of the total pectoral
girdle muscle mass in this species (Jones
et al., 2007). Other muscles, such as the abductor profundus,
adductor superficialis and arrectors are also likely to contribute to power
production (Drucker and Jensen,
1997; Westneat and Walker,
1997; Lauder et al.,
2007).
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 (see below). The muscle tissue was submerged in a water-jacketed tissue chamber containing oxygenated physiological saline. The temperature of the saline was raised from 5 to 22°C over a period of 20 min.
Muscle power measurements were made using the work-loop technique
(Josephson, 1985). Experiments
were carried out 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). The aim of these experiments was to determine the maximum power
available from the pectoral girdle muscles during labriform swimming.
Sinusoidal length change cycles approximating the in vivo muscle
strain 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).
Sinusoidal strain trajectories were applied to the fascicles at a range of
cycle frequencies spanning the in vivo fin beat frequency range. For
each frequency, strain amplitude and the relative timing and duration of
activation were systematically changed until the maximum power output was
measured. The force and position data were captured on a PC via a
604A analog-to-digital interface (Aurora Scientific) and a PCI
analog-to-digital 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.). 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%. 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 (six from the abductor superficialis and six from the
adductor profundus) from 12 fish (M=134.1±9.1 g,
L=19.4±0.2 cm), one fascicle being removed from each fish.
Statistical analysis
A general linear model (GLM) in the statistics package SPSS (version 14.0;
SPSS Inc., Chicago, IL, USA) was used to test for changes in muscle power
output with strain cycle frequency. A fish identifier was included as a random
factor in the model to quantify inter-individual variability. A GLM was also
used to test for speed- and gait-related changes in swimming power output and
cost of transport. A fish identifier was also included as a random factor in
this model. If the GLM detected significant changes in a variable in relation
to cycle frequency or swimming speed, Tukey's HSD post-hoc test was
used to make pair-wise comparisons between mean values.
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). Despite
the onset of body undulations, the mean pectoral fin beat frequency increased
slightly beyond the gait transition point. This upward trend does not continue
at higher speeds. Pectoral fin beat frequency plateaus at approximately the
frequency used at the gait transition (A. Jong and D.J.E., unpublished
data).
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Muscle power outputs
The maximal power output from both the adductor profundus and abductor
superficialis changed significantly with cycle frequency (GLM, adductor
profundus, F=8.3, P<0.001, N=12; abductor
superficialis, F=16.8, P<0.001, N=12). The power
output initially increased with cycle frequency in both muscles but reached a
plateau spanning the gait transition at higher frequencies
(Fig. 2). Stimulus parameters
for maximizing fascicle power output at each cycle frequency are shown in
Table 1.
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Energy metabolism and cost of transport
Standard metabolic rate (SMR) was 0.34±0.02 W kg–1
(mean ± s.e.m., N=9). The metabolic power requirements of
swimming increased with swimming speed during both labriform and undulatory
swimming (Fig. 3). There were
significant changes in total metabolic power (Pgross)
during both labriform (GLM; F=14.8, P<0.001,
N=44) and undulatory swimming (GLM; F=36.5,
P<0.001, N=42). There were also significant changes in
net metabolic power (Pnet = total metabolic power minus
SMR) during both labriform (GLM; F=14.2, P<0.001,
N=44) and undulatory swimming (GLM; F=36.3,
P<0.001, N=42).
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Is economy also a factor driving this gait transition? In many terrestrial
animals, gaits are selected to minimize cost within a particular range of
speeds (Hoyt and Taylor, 1981;
Alexander, 1989). Overall, the
cost of transport is significantly higher during undulatory swimming than
during low-speed labriform swimming (Fig.
4). Where there is overlap in the speed range within the two
gaits, however, there is no clear difference in COT between the gaits
(Fig. 4). The absence of a
decrease in COT on transitioning to undulatory swimming indicates
that the gait shift is not a means of maximizing swimming economy. Energetic
factors are therefore not important in driving the gait transition in this
species. Overall, it is clear that the labriform–undulatory gait change
in bluegill sunfish is driven by a need to supply additional mechanical power
rather than to minimize swimming costs.
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) and triggerfish (Rhinecanthus aculeatus)
(Korsmeyer et al., 2002), the
pattern is similar to that measured in bluegill in that there is no clear
change in COT at the gait transition speed, suggesting that limits to
muscle power also drive the gait changes in these species. This pattern is not
common to all species for which data are available. By contrast, the white
crappie (Pomoxis annularis)
(Parsons and Sylvester, 1992)
shows a clear decrease in COT on switching from labriform to
undulatory swimming. This does not rule out mechanical factors, but maximizing
economy appears to be an important factor driving gait change in this
particular species.
How do bluegill compare to other fish species in terms of swimming economy?
Fig. 5 shows the relationships
of net COT to swimming speed in a number of MPF (one species for
which data are shown uses ballistiform swimming, flapping of dorsal and anal
fins while maintaining a rigid body axis, rather than labriform swimming at
low speeds) and undulatory swimmers. Comparing the economy of different
swimming styles is complicated by a number of factors. Mass-specific metabolic
rate in fish scales with body mass–0.25
(Schmidt-Nielsen, 1972). This
prevents a direct comparison of swimming styles based on metabolic cost,
particularly as many MPF swimmers are relatively small, while specialized
undulatory cruisers like the thunniform scombrids are several orders of
magnitude larger. To allow a fair comparison between species of different body
masses, the data sets have been transformed using this relationship so that
they represent the predicted metabolic power and COT for a standard 1
kg fish such that the standardized cost of transport,
COTstand=COTmeas(1/M)–0.25,
where COTmeas is the measured COT value and
M is the body mass in kg. The data are also presented in relation to
body-length-specific speeds, and COT is expressed as the energy
required to travel a unit body length, minimizing variation due to differences
in absolute speed across a large fish size range. Differences in water
temperature between studies impose additional variability that is not related
to swimming style per se. SMR in ectotherms changes with temperature,
so for a given speed any temperature change will alter the proportion of total
metabolism supporting non-locomotor functions. Total metabolic costs and gross
cost of transport are therefore likely to change with temperature. Changes in
temperature are unlikely to change the net metabolic costs of swimming in
adult fish for two reasons. First, temperature-related changes in viscosity
are only a significant factor for larval fish swimming in viscous, low
Reynolds number flow regimes (Fuiman and
Batty, 1997). Second, muscle efficiency in ectotherms does not
change significantly with temperature
(Smith et al., 2005). The net
metabolic costs of swimming in relation to speed should therefore remain
relatively constant irrespective of changes in temperature. This is confirmed
by direct metabolic measurements of COT across a range of water
temperatures (Claireaux et al.,
2006). The COTnet data presented in
Fig. 5 should therefore allow a
comparison of swimming economy where any variability is primarily due to
differences in swimming style rather than scale or temperature.
It has been proposed that MPF swimming is more economical 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). MPF swimmers that
maintain a rigid body axis may therefore be more economical than undulatory
swimmers. The undulatory specialists exhibit a wide range of COT
values. The European eel, bluefin tunas and coho salmon, species that
undertake lengthy migrations requiring sustained swimming performance, have
the lowest COT within this group. This may represent an adaptation to
minimize energy expenditure during migration. It has previously been suggested
that eels may be four to six times more economical at swimming than other fish
species (van Ginneken et al.,
2005). After accounting for scale effects, however, this appears
not to be the case. It is difficult to draw a clear conclusion about the
relative economy of MPF and undulatory swimmers as there is considerable
overlap between the ranges of COT values for each group
(Fig. 5); however, the two most
economical species are both MPF swimmers.
It has also been hypothesized that specialization for MPF swimming may lead
to reduced undulatory swimming performance
(Webb, 1982). In terms of
economy, the low-speed MPF swimmers do not appear to perform poorly in
comparison with the undulatory specialists once they shift to an undulatory
gait at higher speeds (Fig. 5).
In terms of this gait shift, two distinct MPF strategies are apparent. Some
species utilize MPF gaits only at speeds below approximately 1.3 L
s–1, while others exhibit MPF swimming across a much greater
speed range (Fig. 5). This may
be related to differences in the mechanism of thrust generation. Labriform
swimmers exhibit a continuum of swimming styles
(Walker and Westneat, 2002).
At one extreme are rowers like the stickleback, where there is a distinct
propulsive movement, followed by `feathering' of the fin like an oar during
the recovery stroke (Walker,
2004). At the other extreme are `fliers', with pectoral fin
kinematics analogous to the flapping wing of a bird, exemplified by species
like the parrotfish (Korsmeyer et al.,
2002). Bluegill exhibit pectoral fin kinematics that suggest a
combination of drag- and lift-based mechanisms for generating thrust
(Gibb et al., 1994). The two
species for which energetic data are available and that utilize labriform
swimming across a wide speed range happen to both be fliers
(Fig. 5)
(Webb, 1974;
Korsmeyer et al., 2002). The
alternative strategies cannot entirely be due to kinematic differences,
however, as the stickleback (Gasterosteus aculeatus)
(Walker, 2004) can maintain
speeds of over 5 L s–1 using a rowing stroke.
Differences in muscle mass distribution are an alternative explanation for
the different gait-shift patterns. In Cymatogaster aggregata, the
pectoral girdle muscles are 2.6% of the total body mass
(Webb, 1974), compared with
only 1.3% of total body mass in bluegill and pumpkinseed
(Jones et al., 2007). A
greater relative investment in pectoral girdle muscle mass is likely to enable
a fish to maintain labriform swimming across a greater speed range. Also,
labriform swimmers that exhibit a wide labriform speed range lack significant
numbers of aerobic myotomal muscle fibers
(Webb, 1974;
Korsmeyer et al., 2002). This
limits the ability of these species to switch to sustained undulatory
swimming.
It is not just the availability of muscle power but also the ability of the
fish to transfer this power to the water as thrust that may be an additional
factor in setting the limits to labriform swimming performance. Bluegill
sunfish are one of the few species for which data concerning wake structure
are available (Drucker and Lauder,
1999; Drucker and Lauder,
2000; Lauder et al.,
2007) in addition to metabolic and muscle power measurements. In
bluegill, as labriform swimming speed increases, the jet flow associated with
the pectoral fin downstroke becomes increasingly laterally oriented
(Drucker and Lauder, 2000).
This is in contrast to the surfperch (Embiotoca jacksoni), a species
that can maintain labriform swimming at twice the length-specific speed of
bluegill, where jet flow becomes increasingly oriented downstream as speed
increases (Drucker and Lauder,
2000). These differences in wake structure mean that even if the
bluegill could generate additional pectoral muscle power, this could not be
transferred to the water as additional thrust. Wake structure, in addition to
physiological and morphological factors, is therefore an important factor in
determining the limits of labriform swimming performance
(Drucker and Lauder,
2000).
The structural complexity of the habitats inhabited by the different
species may also be a determinant of swimming style. Differences in wake
structure may reflect a functional trade-off, with more effective thrust
production coming at the expense of decreased maneuverability and stability at
low speeds (Drucker and Lauder,
2000). There are relatively few data available on turning
performance in labriform swimmers, although there is clearly a wide range of
abilities in terms of turning performance. At one extreme, the rowing boxfish
can perform a hovering turn with effectively a zero turning radius
(Walker, 2000), whereas some
fliers cannot hover (Gerstner,
1999; Korsmeyer et al.,
2002), turning primarily by modulating pectoral fin kinematics
during forward motion. Differences in maneuvering performance are likely to
dictate whether a species is restricted to open water or can exploit more
structurally complex habitats.
The wake structure of bluegills suggests specialization for maneuverability
rather than speed during labriform swimming
(Drucker and Lauder, 2000). A
number of studies have investigated bluegill foraging preferences and
efficiency (Mittelbach, 1981;
Werner et al., 1981;
Devries et al., 1989;
Harrell and Dibble, 2001), and
bluegills are attracted to structurally complex habitats such as weed beds
(Johnson, 1993). These are
rich sources of the invertebrates that constitute much of the bluegill's diet
(Beckett et al., 1992). The
labriform gait likely allows bluegill to forage economically in patches of
vegetation while maintaining maneuverability. Gait choice in open water may be
determined by a number of factors. The balance between minimizing either cost
or travel time between food patches will depend on the amount of available
food and the level of predation. If minimizing cost is the primary factor, a
speed close to the gait transition speed is the most economical choice
(Fig. 4), although this may not
maximize energy gain from foraging due to the relatively high travel time
between patches (Pettersson and
Hedenström, 2000). In open water, bluegills are more
vulnerable to predation (Mittelbach,
1981; Chips et al.,
2004). High predation levels may therefore favor the use of the
faster, but less economical, undulatory gait to minimize travel times between
patches of vegetation.
In conclusion, the labriform–undulatory gait transition in bluegill sunfish is primarily driven by a need to recruit additional myotomal muscle mass rather than to maximize swimming economy. When compared to undulatory swimming specialists, labriform swimmers are relatively economical. In bluegill, the labriform gait may enable economical low-speed foraging in structurally complex habitats.
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Acknowledgments |
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