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First published online November 14, 2008
Journal of Experimental Biology 211, 3671-3676 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.019869
Low metabolic cost of locomotion in ornate box turtles, Terrapene ornata
Department of Integrative Physiology, University of Colorado, Boulder, CO 80309, USA
* Author for correspondence at present address: Department of Biology, Lafayette College, Easton, PA 18042, USA (e-mail: zanip{at}lafayette.edu)
Accepted 25 September 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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0.1 m s–1. Ornate box turtles consume only half the
energy predicted by the allometric relationship for all terrestrial animals
(15.9±0.35 J kg–1 m–1), and, thus,
appear to be very economical walkers. When walking up a 24 deg. incline
turtles moved significantly slower (0.04±0.004 m s–1),
but performed the extra work required to walk uphill with very high
efficiencies (>49%). It appears that the co-evolution of a protective
shell, the associated shoulder morphology, and very slow, efficient muscles
produce both economical level walking and efficient uphill walking.
Key words: biomechanics, locomotion, energetic cost of transport, muscular efficiency, Terrapene
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Taylor et al., 1982;
Bennett, 1985;
Full, 1989). Previous research
has suggested that the energetic COT largely depends on (1) the proficiency of
minimizing the mechanical work performed
(Cavagna et al., 1977), (2) the
efficiency of performing that mechanical work
(Taylor, 1994), and (3) the
cost of generating force to support body weight
(Kram and Taylor, 1990;
Griffin et al., 2003).
Long-term evolutionary processes have resulted in a wide range of body plans,
yet for a given body mass, metabolic COT converges to a relatively narrow
range. New insights have come from studies of `outliers' from the
allometrically predicted COT (i.e. animals with unusual morphology and/or
gaits) such as kangaroos (Dawson and
Taylor, 1973), penguins
(Pinshow et al., 1977;
Griffin and Kram, 2000),
platypuses (Fish et al., 2001)
and turtles (Baudinette et al.,
2000).
Chelonians (turtles and tortoises) have unique anatomical and physiological
traits and obviously are slow moving. All chelonians have a protective shell
and a specialized articulation between the dorsal prong of the endoskeletal
girdle (scapula) and the carapace (top shell)
(Walker, 1986). This
articulation along with the presence of a plastron (bottom shell) may
eliminate the need for the `muscular sling' that is required by other
quadrupeds (e.g. Carrier et al.,
2006), thus possibly saving energy. In addition, Woledge
(Woledge, 1968) demonstrated
experimentally that tortoise muscle (in vitro) is much slower and
much more efficient (35%) than the muscles of other vertebrates (e.g. frog,
20%). Nwoye and Goldspink have shown that the biochemical efficiency of muscle
is inversely related to its shortening speed
(Nwoye and Goldspink, 1981)
and slow-twitch oxidative fibers also require less energy to generate
isometric force than fast-twitch muscle fibers
(Heglund and Cavagna, 1985).
At the whole-organism level, Baudinette and colleagues showed that Murray
short-necked turtles (Emydura macquarii) use roughly half as much
metabolic energy to walk on the level as other animals of similar size
(Baudinette et al., 2000).
Thus, the extremely slow rate of movement and high muscular efficiency of
chelonians appears to save metabolic energy during terrestrial locomotion.
However, of the over 250 turtle species, this relationship has been studied in
only one (Baudinette et al.,
2000). Furthermore, that species, Emydura macquarii, is a
semi-aquatic turtle and not a terrestrial specialist. These facts led us to
investigate further the energetics of turtle locomotion.
Although slow locomotion with efficient muscles can lead to low COT, slow
walking may conversely increase the COT by confounding mechanical-energy
conservation via the inverted-pendulum mechanism. Cavagna and
colleagues (Cavagna et al.,
1977) demonstrated in many species that the inverted-pendulum
mechanism of mechanical-energy conservation during walking is greatest at
intermediate speeds. In addition, several recent studies have revealed that
extremely slow animals, such as walking alligators and giant tortoises, have
only low levels of energy conservation utilizing the inverted-pendulum
mechanism (Willey et al.,
2004; Zani et al.,
2005). Thus, the physiological efficiency benefits of using slow
muscle fibers may be offset by poor mechanical-energy conservation that
results in greater mechanical work. In this study, our goal was to quantify
the metabolic energy expenditure during locomotion (i.e. in vivo) and
thus calculate metabolic COT and locomotor efficiency of a terrestrial species
of turtle, the ornate box turtle (Terrapene ornata). We hypothesized
that Terrapene ornata would have a lower COT during level walking
than that predicted based on body mass
(Taylor et al., 1982;
Full, 1989) and a greater
uphill walking efficiency than has been measured for other species.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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From mid-December 2003 to late-January 2004, turtles were maintained in a
refrigerator in a state of cold torpor at 5°C in 1 gallon (3.8 l)
plastic boxes (two per box) partially filled with moist soil. During the last
2 weeks of this 6 week period, the daily fluctuation in thermoperiod was
gradually increased by 5°C to mimic spring-like conditions. Turtles
were then placed back into their bins and provided with heat, food and water.
The light:dark cycle was initially set at 14 h:10 h, and day length was
increased by 15 min per week over the course of data collection to simulate
spring. All turtles survived and only individuals that appeared to be healthy
were included in this study.
We trained turtles to walk on a motorized treadmill with a belt that was
coated with sand to provide traction (bed dimensions 0.15 m widex0.5 m
long). Turtles were encouraged to walk continuously by a researcher tapping on
the shell with a pencil. Turtles wore a loose-fitting cylindrical acetate
open-flow mask (Fig. 1;
attached to the shell with Velcro) from which expired air was dried with
Drierite (W. A. Hammond Drierite Co. Ltd, Xenia, OH, USA) and then drawn
through an oxygen analyzer (S3A Ametek, Paoli, PA, USA). The appropriate flow
rate was determined by calculating oxygen consumption during a sample of
duplicate walking trials at several flow rates (1.0, 0.5, 0.4 and 0.3 l
min–1. For all subsequent walking trials, we used the lowest
flow rate (0.4 l min–1) that resulted in an identical
metabolic rate to that for the faster flows. Data were recorded using LabView
6.1 for Macintosh. Oxygen consumption was calculated using the formulas of
Bartholomew and colleagues (Bartholomew et
al., 1981). Rates of oxygen consumption were converted to rates of
energy consumption (i.e. metabolic rates) by assuming 20.1 J of energy are
released for each milliliter of oxygen consumed. A total of 268 trials were
performed on 18 individual box turtles at room temperature
(22.9±1.99°C) over 3 months. Each trial began with a 5–8 min
accommodation period that allowed animals to reach steady-state metabolism.
During this period, animals were required to walk on the treadmill as normal.
We considered turtles to have reached steady-state metabolism when their rate
of oxygen consumption leveled off for at least 1 min. Following this, we
calculated oxygen consumption over a 4 min period of level walking during
which time the metabolic rate was relatively unchanged. We were able to
collect oxygen consumption data for 4 min of steady walking for up to 10
trials per individual. Following a successful level trial, we raised the front
end of the treadmill so that it was inclined 24 deg. This angle was chosen
because it is near the steepest incline that turtles could still walk. After
an additional 4–6 min accommodation, we measured the average oxygen
consumption over a 4 min period for incline walking. Following each trial, we
graded each part (level, incline) as `excellent', `good' or `poor' based on
turtle cooperativeness during the period of accommodation and data collection.
A trial in which the turtle rarely stopped or stopped only briefly was denoted
as excellent; if a turtle stopped occasionally or stopped for no longer than 5
s at a time, it was rated as good; if during a trial a turtle stopped
frequently for long time periods or turned around on the treadmill, the trial
was deemed poor.
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Cost of transport
To estimate the minimum cost of transport (COTmin), we used
three methods. One standard way to compare the expense of locomotion across
taxa is to represent the metabolic rate for locomotion as a function of speed
(e.g. Taylor et al., 1982).
The slope of the relationship between metabolic rate and speed is known as the
energetic COT (J kg–1 m–1) and represents
the amount of energy required to move a given body mass a given distance.
However, the range of steady speeds obtained during this study was slow and
narrow (0.116 m s–1) and presented a new challenge for
determining COTmin. COT can also be calculated for a single trial
by dividing metabolic rate by speed. COTmin can then be determined
as the minimum of the curvilinear regression of individual data points for COT
versus speed. Since this includes all trials from all individuals
this probably represents a conservative estimate of COTmin. A third
way of calculating COTmin is to select the lowest value of COT for
all trials for each individual and then averaging these values for all
individuals. Because turtles were not able/willing to sustain speeds that
might have further minimized energy consumption, each of these methods may
overestimate COTmin. However, we feel that these methods provide
the best possible options for calculating COTmin.
Locomotor efficiency
To lift and accelerate the center of mass of the body and to move the limbs
relative to the body during each stride, legged animals must perform some
amount of mechanical work. Yet, there is no consensus among biomechanists on
how to measure this work (e.g. Willems et
al., 1995; Schenau,
1998; Zatsiorsky,
1998; Donelan et al.,
2002; Bastien et al.,
2003). However, uphill locomotion involves an unambiguous increase
in the work required to steadily lift the center of mass against the force of
gravity. By comparing level and incline walking, we were able to estimate
locomotor efficiency. Locomotor efficiency was determined by first calculating
the extra mechanical power output required on the incline as
mgvsin
, where m is body mass (kg), g is 9.81
m s–2, v is belt speed (m s–1) and
is incline angle (deg.). For example, at a speed of 0.04 m
s–1 on an incline, for the average mass of our animals (0.31
kg), mechanical power was 0.31x9.81x0.04xsin24=0.049 W.
Following this, the metabolic power was calculated by multiplying the
difference in the mass-specific rates of oxygen consumption (ml O2
kg–1 s–1) for incline and level walking by
20.1 J ml O2–1 and mass (kg). Efficiency was then
calculated as the ratio of mechanical-power output to metabolic-power input.
For example, at 0.04 m s–1, if oxygen consumption on the
level was 0.040 ml O2 kg–1 s–1
and for uphill walking it was 0.054 ml O2 kg–1
s–1 there is a difference of 0.014 ml O2
kg–1 s–1. This, multipled by 20.1 J ml
O2–1 and a mass of 0.31 kg, results in an
increased metabolic power of 0.087 W. Thus, at 0.04 m s–1 the
ratio of mechanical to metabolic power is 0.049 W/0.087 W=0.563 for a
locomotor efficiency of 56.3%.
Resting metabolism
As an additional comparison, we conducted two resting metabolism trials on
each individual. Each turtle was handled as usual and placed on the treadmill
while wearing the open-flow mask and allowed to remain still for 5 min.
Animals were unrestrained during this period, but if they started to move we
would hold a hand in front of their heads or rap once on their shells with a
pencil. This had the effect of startling the turtle's head into its shell
slightly and ceasing its attempt to move. However, excessive startling could
result in the animal completely withdrawing its head into its shell (and out
of the mask). Thus, care was taken to ensure that the animal neither moved
excessively nor withdrew its head from the mask for at least four consecutive
minutes during a 15 min trial.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) as 0.01–0.45 ml O2 kg–1
m–1. Using the upper (most conservative) estimate for slope
would produce a COT of 9.07 J kg–1 m–1.
Second, we calculated the COT of each trial from metabolic rate data
(Fig. 2B). Based on a
repeated-measures ANOVA on the 18 turtles with at least eight trials over 3
months, the COT of turtles walking on the level did not change significantly
with training (F7,77=1.91; P=0.080). If anything,
the trend was toward a slightly increased COT with trial date. When plotted
against speed, it is apparent that the COT decreased as expected. A
second-order polynomial provided the best curve fit to these data, explaining
nearly 23% of the variation in COT (versus only 18% for the linear
regression). By setting the first derivative of the regression equation equal
to zero, we determined that the minimum COT occurred at 0.109 m
s–1. The COT at this speed was estimated to be 9.8 J
kg–1 m–1 with 95% confidence intervals (at
this minimum speed) of 5.1 to 14.5 J kg–1
m–1. However, in only three of 141 included trials did
turtles walk faster than 0.11 m s–1 making it difficult to
verify that this was actually the minimum COT. Third, we determined
COTmin for each of the 18 individuals simply as their lowest COT
trial (Fig. 2C). The average of
the 18 COTmin values was 8.0±0.70 J kg–1
m–1 with 95% confidence intervals of 6.31 to 9.69 J
kg–1 m–1.
When walking up a 24 deg. incline compared with level walking, T. ornata showed a significant decrease in walking speed (level: 0.07±0.005 m s–1; incline: 0.04±0.004 m s–1; repeated-measures ANOVA on average speed for each turtle: F1,17=22.4; P<0.001). By limiting data analysis to the range of speeds common to level and incline locomotion (i.e. 0.018–0.062 m s–1) and pairing trials in which turtles walked at the same speed (±0.005 m s–1), we were able to determine the effects of walking on an incline on metabolic rate and COT (Fig. 3). The metabolic rate of turtles on an incline [Fig. 3A; all trials (N=108): 0.051±0.0223 ml kg–1 s–1] was significantly greater than on the level (repeated-measures ANOVA on turtles with trials matched for speed: F1,17=8.41; P=0.010). Likewise, the COT of turtles on an incline (Fig. 3B,C; all trials: 15.0±1.67 J kg–1 m–1) was significantly greater than on the level (repeated-measures ANOVA on turtles with trials matched for speed: F1,17=4.98; P=0.039). However, because variation in the rate of oxygen consumption was so great (Fig. 2A; Fig. 3A), we calculated whole-animal locomotor efficiency (ratio of mechanical to metabolic powers) for the species as a whole by integrating over the range of speeds in common (0.018–0.062 m s–1) at 0.0001 m s–1 increments. The average locomotor efficiency for ornate box turtles over this range of speeds was 59.6% (range, 49.3% at 0.062 m s–1; 96.7% at 0.018 m s–1).
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The average rate of oxygen consumption of turtles resting on the treadmill, but not moving, was 0.006±0.0009 ml kg–1 s–1.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Even the upper
tail of the 95% confidence interval of our most conservative estimate of
COTmin (14.5 J kg–1 m–1) is below
the estimate for this species based on its size.
This is only the second report of the COT of terrestrial locomotion of a
chelonian and the first report for a terrestrial specialist. Baudinette and
colleagues studied a semi-aquatic species of turtle (walking at near the same
speeds as box turtles) and found that the COT (5.97 J kg–1
m–1) was roughly half that expected (12.55 J
kg–1 m–1) based on mass
(Baudinette et al., 2000). In
addition to calculating the expected COT of box turtles using the allometric
relationship of Full (Full,
1989), we used measurements of COT for lizards reviewed most
recently by Hare and colleagues (Hare et
al., 2007) to compare the COT of chelonians with those of other
reptiles (see also John-Alder et al.,
1986; Autumn et al.,
1999). By including the 23 species reviewed by Hare and colleagues
(Hare et al., 2007), the
estimate for Emydura (Baudinette
et al., 2000), and our best estimate of COT (8.0±0.70 J
kg–1 m–1;
Fig. 4), we determined that
both species of chelonians studied thus far have among the lowest metabolic
COT. These costs are similar to those of many nocturnal lizards (e.g.
Autumn et al., 1999;
Hare et al., 2007). Both
species of turtle fall outside the 95% confidence intervals, which supports
the notion that among reptiles, turtles have a low energetic expenditure
during locomotion.
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) to
support the weight of the front part of the body, potentially providing an
energetic saving during locomotion. The evolutionary changes in
shoulder-girdle articulation appear gradually in the protochelonian fossil
record [see figure 12 of Lee (Lee,
1997)] and are nearly indistinguishable from extant forms even in
the earliest chelonian fossils {e.g. 210 mya Proganochelys quenstedti
[American Museum of Natural History (AMNH) no. 29383]; P.A.Z. unpublished
observation} suggesting that these innovations evolved early in the turtle
lineage and have changed very little since.
A second possible explanation for the low metabolic COT of turtles relates
to their muscle physiology. Woledge
(Woledge, 1968) reported that
turtle muscles are more efficient (35%) in vitro than those of other
vertebrates (e.g. frog, 20%). This suggested that turtles would be more
efficient at moving. When we compared the metabolic cost of level with that of
uphill locomotion we estimated the in vivo efficiency of turtles to
be at least 49% and averaging 59.6% over the entire walking speed range. In
addition to calculating efficiency over the range of speeds common to level
and incline locomotion, we extrapolated our efficiency calculations to the
fastest sustainable speed that we measured for this species (0.134 m
s–1) as well as burst speeds for this species (0.208 m
s–1) reported by Claussen and colleagues
(Claussen et al., 2002) and
found locomotor efficiencies of 44.5% and 43.3%, respectively. We surveyed the
literature for reports of the metabolic cost of level and uphill locomotion to
compute locomotor efficiency in other species (see Materials and methods).
Indeed, turtles appear to be unusually efficient when compared with other
animals (Table 1). This high
efficiency could be due, in part, to the fact that muscular efficiency is
inversely related to the shortening speed of muscles
(Nwoye and Goldspink,
1981).
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When trying to understand the low COT in turtles, it may be useful to
consider further the potential co-evolution of slow speed and a protective
shell. Lovegrove (Lovegrove,
2001) related the evolution of body armor in mammals to basal
metabolic rates and locomotor performance (running speeds). Following the
ideas of Lovegrove (Lovegrove,
2001), we hypothesize that the evolution of effective defenses
(e.g. dermal plates, shells, spines, noxious chemicals) may release animals
from selection on enhanced locomotor speed performance for escape, resulting
in slower walking/running speeds and, hence, energetic savings due to the
inverse relationship between speed and muscular efficiency. In other words, an
animal with an effective defense need not be a fast locomotor and, thus,
defenses and metabolic economy may co-evolve. A test of this hypothesis might
include a comparative study of related species with and without defenses (e.g.
skunks with other mustelids; porcupines with other rodents) to determine
whether species with defenses are slow but economical locomotors in
general.
A third explanation for the low energetic COT could be excellent
conservation of mechanical energy using mechanisms such as inverted-pendulum
energy exchange. Species with lower metabolic COT would be expected to have
more proficient exchange of kinetic and gravitational potential energies
during walking. However, the only completed study of the inverted-pendulum
mechanism in chelonian locomotion found that Galapagos tortoises have much
greater potential energy fluctuations than kinetic energy fluctuations when
they walk and thus their inverted-pendulum energy exchange is poor
(Zani et al., 2005).
Preliminary analysis suggests this pattern is similar in ornate box turtles
(Zani et al., 2004) (P.A.Z.,
R.K., A. R. Biknevicius and S. M. Reilly, unpublished data). Willey and
colleagues reported very little mechanical-energy recovery for alligators,
which are similarly slow (Willey et al.,
2004). Extremely slow locomotion apparently precludes effective
inverted-pendulum exchange during walking because there is too little kinetic
energy available to convert into gravitational potential energy. Thus,
chelonians conform to the definition of `lumbering' (sensu
Reilly et al., 2006) in which
fluctuations in potential energy are much greater than fluctuations in kinetic
energy (see also Reilly et al.,
2007). While evolutionarily correlated with the presence of a
shell, it is unclear whether the shell necessarily caused this transition in
chelonians.
The active and resting oxygen consumption rates we calculated for ornate
box turtles are similar to those of a previous report for this species. At
23°C Gatten (Gatten, 1974)
reported that the average active oxygen consumption rate was 0.083 ml
kg–1 s–1 while the resting rate was
0.003 ml kg–1 s–1. Our active and
resting oxygen consumption rates were 0.044 and 0.006 ml kg–1
s–1, respectively. We ascribe these differences to the fact
that we studied turtles walking on a treadmill at sustainable, aerobic speeds
whereas Gatten (Gatten, 1974)
induced maximal activity by several minutes of electric shock. Similar to the
findings of Gatten (Gatten,
1974), our data exhibit considerable variation in the rate of
oxygen consumption (Fig. 2A).
We considered several possible explanations for this variation. First, turtles
may have relied on anaerobic metabolism during locomotion. To test this
possibility, we conducted several trials in which animals were allowed to rest
after an extended period (15 min) of level walking. In all cases, the
rate of oxygen consumption dropped to near resting within 20–30 s
indicating that the turtles had not relied on anaerobic metabolism while
walking. Second, turtles may have been holding their breath intermittently
during locomotion. Early in this study, we noted this behavior in one
individual that held his breath for 15 min while walking continuously and
only breathed when he stopped. Interestingly, the total energy consumed for
that trial was similar to trials in which animals breathed normally (i.e. when
the turtle stopped and breathed his oxygen consumption spiked, but averaged
over the period of walking metabolic rate was `normal'). After noting this
breath-holding behavior, we carefully monitored trials for signs of breath
holding in other turtles (e.g. dips and spikes in oxygen consumption). All
other individuals appeared to breath normally throughout all trials and that
one individual was excluded from further study. Third, turtles are sometimes
clumsy in their movements and will misstep, landing on their shells before
continuing to walk. This did not appear to impede their locomotion as turtles
were able to recover immediately and is akin to a `stumble' in humans. Yet
this may have made the locomotion of some individuals prone to stumbling
energetically less efficient. However, at best we can note that Gatten
(Gatten, 1974) had a similar
spread in the rate of oxygen consumption at a given temperature for this same
species [see figure 2 of Gatten
(Gatten 1974)] and that
individual variation may lead to variation in rates of oxygen consumption and
the subsequent determination of COT (Fig.
2C). Thus, we have no obvious explanation for the variation in the
rate of oxygen consumption, except that metabolic rate appears to vary from
trial to trial within what we considered to be excellent trials. Rather than
obscure the variation by only reporting average values for each individual, we
elected to plot all data points from all excellent trials.
In summary, ornate box turtles walk extremely slowly, and with very low
metabolic costs relative to their body size. Furthermore, the uphill
locomotion of ornate box turtles appears to be unusually efficient (>49%)
compared with that of most other vertebrates. Since the only other turtle
species studied to date revealed poor mechanical-energy recovery using the
inverted-pendulum mechanism (30%), the low metabolic COT in turtles
appears to be due to the morphological changes that accompanied the evolution
of a protective outer shell, extremely slow locomotor speeds and unusually
efficient muscles. It remains to be seen whether the origins of defense
mechanisms in other vertebrate lineages resulted in convergent evolutionary
changes with respect to locomotor energetics and mechanics.
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Acknowledgments |
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O2 (±1
s.d.) is shown as a filled circle at 0 m s–1.
