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First published online December 28, 2007
Journal of Experimental Biology 211, 170-179 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.007476
Research Article, Motor Systems |
Contractile properties of the pigeon supracoracoideus during different modes of flight
1 Department of Biology, University of Portland, 5000 N. Willamette Boulevard,
Portland, OR 97203, USA
2 Concord Field Station, Harvard University, Old Causeway Road, Bedford, MA
01730, USA
* Author for correspondence (e-mail: tobalske{at}up.edu)
Accepted 15 May 2007
Summary
The supracoracoideus (SUPRA) is the primary upstroke muscle for avian flight and is the antagonist to the downstroke muscle, the pectoralis (PECT). We studied in vivo contractile properties and mechanical power output of both muscles during take-off, level and landing flight. We measured muscle length change and activation using sonomicrometry and electromyography, and muscle force development using strain recordings on the humerus. Our results support a hypothesis that the primary role of the SUPRA is to supinate the humerus. Antagonistic forces exerted by the SUPRA and PECT overlap during portions of the wingbeat cycle, thereby offering a potential mechanism for enhancing control of the wing. Among flight modes, muscle strain was approximately the same in the SUPRA (33–40%) and the PECT (35–42%), whereas peak muscle stress was higher in the SUPRA (85–126 N m–2) than in the PECT (50–58 N m–2). The SUPRA mainly shortened relative to resting length and the PECT mainly lengthened. We estimated that elastic energy storage in the tendon of the SUPRA contributed between 28 and 60% of the net work of the SUPRA and 6–10% of the total net mechanical work of both muscles. Mechanical power output in the SUPRA was congruent with the estimated inertial power required for upstroke, but power output from the PECT was only 42–46% of the estimated aerodynamic power requirements for flight. There was a significant effect of flight mode upon aspects of the contractile behavior of both muscles including strain, strain rate, peak stress, work and power.
Key words: flight, muscle, supracoracoideus, force, work, power, stress, strain
Introduction
The supracoracoideus (SUPRA) is the second largest muscle of the avian
wing. It is the major antagonist to the larger pectoralis (PECT), which is the
primary downstroke muscle for bird flight
(Dial, 1992a
). The SUPRA is
active in all modes and speeds of flight
(Dial 1992a;
Tobalske, 1995), yet, with
practice, birds may take off without use of the muscle
(Degernes and Feduccia, 2001;
Sokoloff et al., 2001).
Electromyographic (EMG) data suggest that the muscle decelerates the wing
during late downstroke and reaccelerates the wing during the beginning of
upstroke (Dial, 1992a).
Regardless of its capacity to elevate the wing, an in situ study of
the function of the SUPRA indicated that the principal role of the muscle is
supination of the humerus during the transition from downstroke to upstroke
(Poore et al., 1997). The need
for supination explains the activation of the SUPRA during faster flight when
lift should presumably function to elevate the wing independent of muscle
activation (Rayner, 1985;
Poore et al., 1997;
Hedrick et al., 2002;
Hedrick et al., 2004).
The mechanical properties of the SUPRA in vivo are, unfortunately,
unknown. The vast majority of the variation observed in avian wingbeat
kinematics occurs during upstroke
(Scholey, 1983;
Tobalske, 2000;
Tobalske et al., 2003a) and
this variation appears to correspond with changes in aerodynamic function
(Rayner, 1995;
Spedding et al., 2003). In
contrast, considerable insight is now available on the contractile behavior of
the PECT in flying birds.
The PECT is largely designed to generate work and power
(Biewener, 1998;
Biewener and Roberts, 2000).
Power output in the PECT varies with flight mode and speed
(Dial and Biewener, 1993;
Hedrick et al., 2003;
Tobalske et al., 2003b;
Tobalske et al., 2005). The
large size and complex architecture of the PECT
(Sokoloff et al., 1998) is
accompanied by significant heterogeneity in regional activation patterns
(Boggs and Dial, 1993) and
muscle strain (Biewener et al.,
1998; Soman et al.,
2005).
The anatomy of the SUPRA differs from that of the PECT
(Baumel et al., 1993;
Poore et al., 1997). Although
both muscles are bipinnate, the SUPRA is narrow, with a long tendon of
insertion. The PECT is broad, with a short tendon of insertion and a
substantial region of parallel fibers in the anterior pars
sternobrachialis. Interpreted in the light of muscle function during
terrestrial locomotion, the anatomy of the SUPRA would suggest that the muscle
is used to produce force rather than work and also to exploit elastic energy
storage and recovery (Biewener and
Baudinette, 1995; Roberts et
al., 1997; Biewener,
1998; Biewener and Roberts,
2000). Release of stored energy reduces the metabolic cost of
terrestrial locomotion (Alexander,
1988; Biewener and Roberts,
2000). Such storage has been identified as a potential function of
the avian furcula (Jenkins et al.,
1988), but it has not been documented for any muscles of the
wing.
As power costs for flight are high
(Harrison and Roberts, 2000),
it is generally assumed that selective pressures in evolution optimized the
avian wing for metabolic efficiency. A competing selective pressure is likely
for wing control, particularly during maneuvers
(Warrick et al., 2002). For
maneuvering, it is thought that distal muscles of the wing are relatively more
important than large proximal muscles such as the PECT and SUPRA
(Dial, 1992a;
Dial, 1992b). However, using
EMG recordings and in situ rates of force development in the PECT and
SUPRA, Poore et al. (Poore et al.,
1997) hypothesized that there should be antagonistic force
development in the PECT and SUPRA to facilitate control.
During slow flight in most birds, weight support and thrust are produced
only during downstroke and upstroke appears to be aerodynamically inactive
(Spedding et al., 1984;
Tobalske, 2000;
Hedrick et al., 2004;
Usherwood et al., 2005).
Therefore, in slow flight, we expect PECT power to match the aerodynamic
requirement for flight while SUPRA power should match the inertial power
required for upstroke. Inertial work produced by the PECT to accelerate the
wing during downstroke is expected to be transformed into aerodynamic work at
the end of downstroke (Van den Berg and
Rayner, 1995; Hedrick et al.,
2004).
Much of the information presently available about PECT function in flying
birds is from the pigeon Columba livia (Gmelin 1789), so we selected
this species for investigating SUPRA function. We began with four predictions
from prior research. Given the expected role of the SUPRA in supination of the
wing (Poore et al., 1997), we
hypothesized (1) that peak force in the muscle would occur at the transition
from downstroke to upstroke rather than at mid-upstroke. Anatomy led us to
predict that (2) it would operate with little length change and store elastic
energy it its tendon (Biewener,
1998; Biewener and Roberts,
2000). A need for control of the wing and joint stability would
result in (3) overlap in force production with the PECT
(Poore et al., 1997). Finally,
given the present evidence that upstroke produces little or no lift during
slow flight (Tobalske, 2000),
we hypothesized that (4) power output in the SUPRA should equal inertial power
in upstroke, whereas power output in the PECT should match aerodynamic power
required for slow flight.
Materials and methods
Birds and experimental design
We obtained pigeons (N=7, including five white carneau and two
king, body mass 561.9±94.9 g, means ± s.d.,
Table 1) from commercial
suppliers. An additional three white carneau pigeons (562.3±8.2 g)
(Soman et al., 2005) were used
for 3-D kinematic analysis and estimation of inertial power
(Piner). The birds were housed in a 2 m x 8 m
x 2 m outdoor aviary at the Concord Field Station, Harvard University
(Bedford, MA, USA) and had access to food and water ad libitum. The
Institutional Animal Care and Use Committee at Harvard University approved all
housing and experimental protocols (accredited by the Association for
Assessment and Accreditation of Laboratory Animal Care International). The
birds were trained to fly between platforms (30 cm x 40 cm) and
horizontal poles (diameter 2.5 cm) to accomplish one of three modes of flight:
level, ascent and descent. Level flights (3.9±0.5 m
s–1) were between platforms supported 1.5 m above the floor
and spaced 7–9 m apart. Ascending (1.4±0.5 m
s–1) and descending (1.8±0.3 m s–1)
flights were from a platform placed on the ground and a horizontal pole placed
1.2 m horizontally and 2 m vertically from the platform to effect flight paths
60° relative to horizontal. Flight speeds varied from 0 m
s–1 (hovering, when the bird was unwilling to ascend) to 2 m
s–1. All training and experiments took place in a hallway 1.9
m x 4.2 m x 12 m.
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Morphometric data (Table 1)
were obtained after the completion of experiments. Mass (M) was
obtained for single muscles, and 10 measurements of fascicle length
(L) and fascicle angle (
) were obtained for each surface,
superficial and deep. Muscle cross-sectional area (A) was calculated
as M/
L assuming a muscle density () of 1060 kg
m–3. Measurements of tendon length and mass from the SUPRA
were used to estimate tendon cross-sectional area assuming a tendon density of
1120 kg m–3 (Ker,
1981).
Additional wing and body measurements were obtained with the wings spread
as in mid-downstroke using standard techniques
(Tobalske and Dial, 1996;
Tobalske et al., 1999).
Video recording and modeling of power requirements
We obtained synchronized 2-D kinematic data during implanted flights
(N=7 birds) to estimate the aerodynamic power requirements of the
PECT during flight. To estimate the inertial power requirements of the SUPRA
during upstroke, we also obtained 3-D kinematic data from unimplanted level
and ascending flights in three birds affiliated with Soman et al.
(Soman et al., 2005).
Mathematical modeling was accomplished using Igor Pro version 4.0.6
(Wavemetrics, Inc., Beaverton, OR, USA) and Matlab version 6.5 (The MathWorks
Inc., Natick, MA, USA).
During implanted flights, we used a Redlake PCI-500 (San Diego, CA, USA) to
obtain a lateral-view video (250 Hz, shutter speed 0.5 ms, stored using PCI-R
version 2.18 software) with a pixel:metric scale corrected for parallax using
a synchronized Panasonic AG-450 S-VHS camera (60 Hz, shutter speed 1000 Hz)
that offered cranio-caudal views of the flight path. We adapted the methods of
Hedrick et al. (Hedrick et al.,
2003) and Tobalske et al.
(Tobalske et al., 2003b) in
which 3-D kinematic data were applied to the aerodynamic models of Rayner
(Rayner, 1979a;
Rayner, 1979b), Pennycuick
(Pennycuick, 1975) and
Wakeling and Ellington (Wakeling and
Ellington, 1997). In the 3-D analysis, fully described in
equations 2–7 in Hedrick et al.
(Hedrick et al., 2003),
separate estimates of induced, profile, parasite and climb power were summed
for each video frame, and the sums were then integrated over an entire
wingbeat cycle. Lacking the resolution of 3-D data, we instead calculated the
component aerodynamic powers for each half of the wingbeat cycle and then
integrated over the full cycle (Paero).
From earlier work (Tobalske and Dial,
1996; Tobalske et al.,
2003a), we assumed that the wings were fully extended throughout
downstroke and that wing span at mid-downstroke was always the same as the
morphological wing span of a given bird
(Table 1). We then scaled
mid-upstroke wing span according to the upstroke:downstroke span ratio within
a given wingbeat. Finally, we assumed that wing length did not change
throughout upstroke.
Our results were sensitive to our assumptions of wing length, particularly for downstroke. For example, during level flight a 10% decrease in wing length at mid-downstroke increased our estimate of Paero by 13% (18% increase for induced power, 17% decrease for profile power), and a 10% increase in wing length decreased Paero by 11% (15% decrease for induced power and 20% increase for profile power). In comparison, 10% changes in wing length during upstroke caused the estimated profile power and Paero to vary by <1%.
We later obtained additional high-speed video cameras, which permitted us
to measure 3-D kinematics and, thereby, estimate Piner
during upstroke (Hedrick et al.,
2004). All video recording, camera calibration, data filtering and
measurements of mass distribution were accomplished as in Hedrick et al.
(Hedrick et al., 2004). We
calculated Piner required for upstroke as the change in
kinetic energy of the wing from the start of the upstroke to its maximum
divided by wingbeat duration.
Surgical procedure
Following training, we surgically implanted EMG electrodes and
sonomicrometry (SONO) transducers into the SUPRA and PECT muscles by adapting
standard methods used for the PECT
(Biewener et al., 1998;
Tobalske et al., 2005). We
also attached two strain gauges (FLE-1, Tokyo Sokki Kenkyujo, Ltd, Tokyo,
Japan) to the dorsal surface of the deltopectoral crest adjacent to, and
parallel with, the insertion of each muscle
(Biewener et al., 1998;
Soman et al., 2005)
(Fig. 1). One pair of 2.0 mm
SONO crystals (Sonometrics, Inc., London, ON, Canada) and a fine-wire bipolar
EMG electrode (0.5 mm bared tips with 2 mm spacing; California Fine Wire,
Inc., Grover Beach, CA, USA) were implanted parallel to the fascicle axis of
the mid-anterior region of the sternobrachial portion of the PECT
(Fig. 1A). Another pair of SONO
crystals and an EMG electrode were implanted through the PECT and into the
mid-anterior SUPRA.
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0.1% for 1%
slippage. After the experiments, the pigeons were killed using an intravenous overdose of sodium pentabarbitol (100 mg kg–1) for verification of electrode placement, calibration of strain gauges and measurement of morphology (Table 1).
In vivo muscle recordings and calibrations
Recordings were made by connecting the bird to a 12 m shielded cable, which
the animal dragged as it flew (the suspended portion of cable weighed 80
g). Qualitatively, there was no apparent effect of these elements upon flight
kinematics in the pigeons, but we did not obtain a sufficient sample of
non-implanted flights to use for a statistical test of this hypothesis. The
cable was connected to strain gauge bridge amplifiers (Vishay 2120,
Micromeasurements, Inc., Raleigh, NC, USA), a sonomicrometry amplifier (Triton
120.2, Triton Technology, Inc., San Diego, CA, USA) and EMG amplifiers (Grass
P5-11, Grass Telefactor, West Warwick, RI, USA). All signals were recorded at
5 kHz onto a Pentium II computer running Windows NT (Microsoft, Inc., Redmond,
WA, USA) using a Digidata 1200 A/D converter (Axon Instruments, Union City,
CA, USA) at 5 kHz. For analysis of SONO and EMG signals, we used the methods
of Hedrick et al. (Hedrick et al.,
2002) and Tobalske et al.
(Tobalske et al., 2005).
Sonomicrometry signals were corrected to represent the instantaneous
average L of the muscle in which the crystals were implanted
(Fig. 1A,
Table 1). To treat analysis for
the PECT and SUPRA equally, we assumed 
L was uniform
throughout the fascicle and throughout the muscle. This assumption merits
caution as evidence from a different vertebrate indicates that heterogeneity
of strain is apparent even within single fascicles
(Ahn et al., 2003). Other
studies in pigeons suggest our method may have caused a slight overestimate of
muscle strain (
) for the PECT as a whole because the region we implanted
includes fibers that exhibit the greatest L within the muscle
(Biewener et al., 1998;
Soman et al., 2005). No
information is available for regional heterogeneity of contractile behavior in
the SUPRA. The measured distance between the sonomicrometry crystals was
increased by 2.7% to account for the velocity of sound in muscle (1540 m
s–1) (Goldman and Heuter,
1956) relative to the value of 1500 m s–1 assumed
by the Triton 120.2 amplifier. This value was then increased by 0.74 mm to
account for the higher velocity of sound through the epoxy lens of the 2 mm
electrodes relative to muscle tissue
(Biewener et al., 1998). We
also corrected for a 5 ms phase delay and a frequency-dependent attenuation in
the amplitude of the sonomicrometry signals, both of which were due to the 100
Hz linear phase filter inherent to the Triton 120.2 amplifiers
(Tobalske and Dial, 2000).
Resting length (Lrest) was measured during perching, with
the wings folded and the PECT inactive, and =L
Lrest–1.
To calibrate strain in the bone of the humerus into units of muscle force,
we performed pull calibrations (Dial and
Biewener, 1993; Biewener et
al., 1998; Soman et al.,
2005). Silk suture (OO) was secured around the anterior portion of
the PECT 2 cm from the insertion on the deltopectoral crest (DPC) or the
emergent tendon of the SUPRA immediately adjacent to the belly of the muscle.
The other end of the suture was attached to a calibrated force transducer
(Kistler 9203, Amherst, NY, USA). The anatomy of the DPC
(Fig. 1B) resulted in
cross-talk between strain-gauge channels arising from principal strains
transmitted when forces were exerted by either muscle on the DPC. Tension
produced by either muscle resulted in a compressive principal strain acting
perpendicular to the tensile strain and, thus, generally in line with the
other muscle's tendon of attachment. In other words, tension in one muscle
artificially inflated tension measured for the other muscle. This cross-talk
was approximately 50% from the PECT channel to the SUPRA channel and 5% from
the SUPRA channel to the PECT channel.
We corrected for cross-talk from the PECT to the SUPRA channel and chose to
ignore cross-talk in the opposite direction because of circularity in the
underlying argument. Corrections were applied to the SUPRA channel at the
stage of raw voltages. Using data obtained during PECT pull calibrations, we
regressed SUPRA force upon PECT force. For in vivo data from a given
bird, the scaling factor from this regression was multiplied by observed PECT
force and added to the uncorrected SUPRA force to provide a corrected SUPRA
force. The correction factor affected measurements throughout the wingbeat
cycle because residual tension was always present in the PECT during flight.
We calculated muscle stress (
m, in kPa) as force (N) divided
by Acos (Alexander,
1983) (Table
1).
We measured work (mJ) and power (W) for each muscle using the work loop
technique (Josephson, 1985;
Biewener et al., 1998). A work
loop `shape factor' (Hedrick et al.,
2003) was calculated as the observed area of a work loop relative
to the area of a rectangle with the same range of stress and strain. Net work
per wingbeat duration yielded muscle power (Pmus), and
mass-specific power (W kg–1) was calculated as
Pmus divided by M
(Table 1).
Tendon elastic energy recovery (Urec, in J) was
calculated following Biewener and Baudinette
(Biewener and Baudinette,
1995):
 |
t is tendon stress (in MPa), E is elastic
modulus and Vt is tendon volume (in m3). We
used an estimate of 1.0 GPa for E and 0.93 for tendon resilience
based on observed ranges of data reported by Bennett et al.
(Bennett et al., 1986), Ker
(Ker, 1981) and Shadwick
(Shadwick, 1990). Our
estimated tendon elasticity could be inaccurate because the data in these
references are from different tendons in mammals; however, tendon properties
are generally similar across the species studied. We analyzed contractile properties and timing for 242 wingbeats using the onset of PECT shortening to identify the start of individual wingbeats and the onset of PECT lengthening to identify the start of upstroke.
Statistical analysis
For each variable, we computed the mean value within each bird for each
flight mode. We then tested for a significant effect of mode upon each
variable using a univariate repeated-measures analysis of variance (StatView
version 5.0.1, SAS Institute, Inc., Cary, NC, USA). Values are presented as
means ± s.d.
Results
During flight, the SUPRA and PECT muscles exhibited contraction cycles that alternated with each other and were relatively uniform during most of the flight sequence (Fig. 2). The first one or two wingbeats during take-off and last several wingbeats prior to landing featured lower amplitude muscle strain, stress and EMG voltage. Wingbeat frequency averaged 8.6±0.2 Hz (wingbeat duration=116 ms) and did not vary significantly (P=0.0926) among flight modes. Likewise, flight mode did not have a significant effect upon the relative timing of most of the contractile events in the wingbeat cycle (Fig. 3). There were two exceptions. First, the SUPRA started shortening earlier during ascending flight (48±8%) relative to level (49±7%) and descending (50±8%) flight (P=0.0313). Second, the relative offset of SUPRA EMG activity occurred later during ascending (77±5%) compared with level (70±7%) and descending (71±11%) flight (P=0.0172).
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m) in the SUPRA occurred at 65±8% of
the wingbeat cycle, immediately after the transition between downstroke and
upstroke (lag time averaged 4% of the wingbeat cycle). Peak
m in the PECT occurred during the middle of downstroke. For
either muscle, a peak m occurred as the muscle was
shortening. Shortening in the SUPRA lasted 54±7% of the wingbeat cycle
and shortening in the PECT lasted 62±4%. Neuromuscular activation
preceded the onset of shortening in both muscles with a relative lead time of
10±7% in the SUPRA and 12±4% in the PECT. The duration of EMG
activity in the SUPRA was shorter than in the pectoralis, at 33±3% and
58±5%, respectively, relative to cycle duration. Consequently, a
considerable fraction of force development by both muscles lasted beyond EMG
offset (SUPRA, 29±9%; PECT, 39±7%). The pigeons consistently
exhibited overlap in force production by the SUPRA and PECT muscles (Figs
2,
3,
4). An interval of
simultaneous, antagonistic force took place during late downstroke, as force
was declining in the PECT, and another occurred during late upstroke, as force
was declining in the SUPRA. When positive m was present in
its antagonist muscle, negative work absorbed by the SUPRA was
–16±16 mJ and by the PECT was –48±7 mJ. These values
were 9% of the net work performed by either muscle
(Table 2). The magnitude of
overlap in antagonistic force was increased by our method of correction of
cross-talk from the PECT for measured by the SUPRA strain gauge;
nevertheless, overlap remained apparent even when uncorrected (raw) signals
from the SUPRA strain gauge were evaluated relative to the strain-gauge signal
from the PECT (Fig. 4).
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Many of the contractile properties that we measured varied significantly
according to flight mode (Table
2). Overall, , m, work and power reached
maximum values during ascending flight, were least during descending flight,
and were intermediate during level flight. The only exception to this pattern
was fractional lengthening in the PECT, which remained nearly the same
(P=0.3016) during ascent (28±7%) and level flight
(28±7%).
Stress (m) was greater in the SUPRA than in the PECT
(Fig. 5A), and there was a
significant effect of flight mode upon the peak m exhibited
by the SUPRA (P=0.0463) and PECT (P=0.0017;
Table 2). In the SUPRA, peak
m varied from 85±30 kPa during descent to
125±65 kPa during ascent. Peak m during descent in
the PECT was 50±12 kPa and it was 58±15 kPa during ascending
flight.
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t in the tendon of the SUPRA
averaged 24±14 MPa, which provided an estimate of recovered energy of
58±27 mJ among flight modes. This represented 33±5% of the net
work performed by the SUPRA and 8±2.2% of the net work performed in sum
by the PECT and SUPRA. Although Urec in the SUPRA tendon
during ascending flight was over twice the amount estimated for descending
flight (88±85% versus 36±29%,
Table 2), substantial variance
among birds resulted in a marginally non-significant effect of flight mode
upon Urec (P=0.0548).
Muscle strain () during wingbeats was generally similar in the two
muscles (SUPRA: 36±3%; PECT: 38±4%). During flight, the SUPRA
tended to operate over a range of L that was less than
Lrest, whereas the PECT operated over lengths greater than
Lrest (Fig.
1 and Fig. 5A).
Flight mode did not have a significant effect upon fractional shortening in
the SUPRA (P=0.0762) or fractional lengthening in the PECT
(P=0.3015). In contrast, the observed variation associated with
flight mode was significant for in the SUPRA (P=0.0039),
fractional lengthening in the SUPRA (P=0.0105), in the PECT
(P=0.008) and fractional shortening in the PECT
(P=0.0452).
The comparatively brief duration of SUPRA shortening (Fig. 3) resulted in the SUPRA having higher average strain rates compared with the PECT (Table 2). Strain rate in the SUPRA varied between 5±2 and 7±2 L s–1, and from 5±1 to 6±1 L s–1 in the PECT. Strain rate also varied significantly among flight modes for both muscles (SUPRA, P=0.0042; PECT, P=0.0023).
Work loops differed in shape factor between the two muscles and among modes
of flight (Fig. 6). For
example, in Fig. 6, the shape
factors of the work loops in the PECT were 18±4% greater than the shape
factors for work loops in the SUPRA. This difference in shape factor is
consistent with the comparatively steeper shoulders of the SUPRA work loops on
either side of peak m.
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SUPRA mass-specific power varied from 106±50 W kg–1 during descent to 194±98 W kg–1 during ascent (P=0.0178; Table 2). Expressed as Pmus and doubled to represent the output from both muscles, the mean among flight modes was 3±1 W (Fig. 7). These measurements of Pmus were 2.5 and 2.3 times greater than our estimates of Piner required from the SUPRA muscles for upstroke during level and ascending flight, respectively. However, the estimated Piner required from the muscles was within 1 s.d. of 2Pmus (Fig. 7).
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Discussion
Most aspects of our four hypotheses pertaining to the comparative function
of the SUPRA and PECT were supported by our results: (1) Peak
m in the SUPRA occurred at the transition between downstroke
and upstroke (Figs 2,
3,
4); (2) the SUPRA stored
substantial elastic energy, ranging from 36 to 88 mJ
(Table 2,
Fig. 5A); (3) there was overlap
of antagonistic force at the end of each half stroke (Figs
2,
3,
4); and (4)
Pmus in the SUPRA was close to the estimated
Piner for upstroke
(Fig. 7). However, two
inconsistencies with our predictions were apparent. Contrary to hypothesis
(2), in the SUPRA was over 30% and only slightly less than in the PECT.
Also, contrary to (4), power output in the PECT was less than half of the
estimated Paero.
These discrepancies with our predictions emphasize the role of proximal muscles as producers of work and indicate that independent methods are needed to further explore Pmus for the pectoralis and Paero in bird flight.
Our in vivo experiments show that a major role of the SUPRA is for
supination of the humerus at the end of downstroke, entirely consistent with
the in situ experiments of Poore et al.
(Poore et al., 1997). Peak
m occurred at wing turnaround
(Fig. 2B, Figs
3 and
4), and the shapes of the work
loops generated by the SUPRA (Fig.
6) revealed that stress declined rapidly during mid- and late
upstroke when wing elevation was occurring
(Tobalske and Dial, 1996;
Tobalske, 2000). Poore et al.
(Poore et al., 1997) argued
that long-axis rotation of the humerus was a critical step during the
evolution of flapping flight. Nevertheless, our data show that the SUPRA also
elevates the wing, as m>0 Pa throughout the upstroke
(Figs 2,
3,
4).
Given the complexity of the musculature of the avian wing
(Dial, 1992a;
Baumel et al., 1993), it is
sobering that our predictions of function from anatomy were only partially
correct. This suggests that in vivo studies are required to
adequately understand muscle function. It would be more convenient if all
muscles could be neatly categorized as either force producers or work
producers; however, such a simple dichotomy is often unlikely to be the case.
Given the morphology of the SUPRA (Fig.
1A) and patterns exhibited by terrestrial animals with leg muscles
featuring long tendons of insertion [e.g. tammar wallabies, Macropus
eugenii (Biewener and Baudinette,
1995)], we expected low in the muscle. Our measurements of
relatively large (Table
2, Fig. 5) are
consistent with a compromise in muscle design that permits the SUPRA to
generate work and power to match Piner for upstroke
(Fig. 7), while at the same
time favoring economical force generation
(Biewener and Roberts, 2000).
As the SUPRA is a proximal muscle, our results are similar to those of
experiments in mammalian terrestrial locomotion in which greater is
exhibited by proximal muscles of the limb compared with distal muscles
(Gregersen et al., 1998;
Gillis and Biewener,
2001).
Elastic energy recovered from the SUPRA tendon is a novel result for
muscles of the avian wing. Aside from the role of the furcula
(Jenkins et al., 1988),
elastic energy storage is not presently recognized as a mechanism available to
flying birds (Harrison and Roberts,
2000). Storage and recovery of energy in tendons saves energy
during terrestrial locomotion (Taylor and
Heglund, 1982; Alexander,
1988; Biewener and Baudinette,
1995; Baudinette and Biewener,
1998; Biewener and Roberts,
2000). Energy recovery (Urec) of the order of
8% relative to the combined work output of the SUPRA and PECT
(Table 2) should be included
when estimating the efficiency of bird flight. At 32% of the net work of the
SUPRA, Urec approached the lower end of the range of
recovery reported for the extensor tendons in the legs of tammar wallabies
(38–52%) (Biewener and Baudinette,
1995). The capacity for energy storage merits further study in
other muscles of the wing that exhibit long tendons of insertion, including
the tensor propatagialis longus and flexors and extensors of the distal wing
(Dial, 1992a;
Baumel et al., 1993).
It is widely recognized that co-activation of antagonist muscles provides
stability about a musculoskeletal joint, such as the knee
(Baratta et al., 1988;
Kellis, 1998), and improves
the accuracy of arm movements (Suzuki et
al., 2001; Gribble et al.,
2003). However, Poore et al.
(Poore et al., 1997) were the
first to suggest that antagonistic forces of the SUPRA and PECT might function
to improve wing control during the rapid wing oscillations that occur during
bird flight. Our results provide the first direct evidence for such a role
(Figs 2,
3,
4). Whereas the two muscles are
activated simultaneously during gliding flight
(Tobalske, 1995;
Tobalske, 2000), neuromuscular
activation of these muscles does not overlap during flapping flight. Instead,
because the decay of force within each muscle substantially lags the offset of
EMG activity (Fig. 3), a
significant overlap of antagonistic force occurs at wing turnaround.
The SUPRA generated work and power sufficient to meet the inertial
requirements of wing upstroke (Fig.
7), which were within 1 s.d. of combined Pmus.
Based on kinematic inferences, there has been some debate over the aerodynamic
function of upstroke during slow flight in pigeons and other birds with wings
of relatively high aspect ratio (Tobalske,
2000). Our experiments provide new evidence that the upstroke is
largely an aerodynamically inactive recovery; additional evidence includes the
wake analysis of Spedding et al. (Spedding
et al., 2003) on a thrush nightingale (Luscinia luscinia)
and pressure measurements made about the wings of pigeons by Usherwood et al.
(Usherwood et al., 2005). The
small discrepancy between observed SUPRA Pmus and
estimated Piner (Fig.
7) suggests that any induced or profile power requirements of
upstroke are <10% of Paero for slow flight.
Our measurements of PECT Pmus, at 44% of estimated
Paero, are enigmatic. We reported similar results
previously (Biewener et al.,
1998), wherein mass-specific power from the PECT was 70.2 W
kg–1 in level flight, slightly less than the 87 W
kg–1 we observed here
(Table 2). In contrast, Soman
et al. (Soman et al., 2005)
recently obtained measurements of 207 W kg–1 for level flight
of pigeons under similar conditions. Their analysis used positive work rather
than net work to calculate Pmus. Calculated in this way,
our measurement of mass-specific power during level flight
(Table 2) would be 105 W
kg–1, and 108 W kg–1 in an earlier study
(Biewener et al., 1998). Mean
PECT during level flight is similar among these studies: 36.2% in the
present study (Table 2), 32% in
Biewener et al. (Biewener et al.,
1998) and 31.9% in Soman et al.
(Soman et al., 2005).
Likewise, morphology, wingbeat frequency and general work loop shapes are
similar among the studies. Thus, differences in Pmus are
due to calibrations of the strain gauges used to calculate PECT force.
Uncertainties over pull calibrations were previously reported for other
experiments (Hedrick et al.,
2003; Tobalske et al.,
2003b), in which pull calibrations were abandoned and aerodynamic
models were instead used to calibrate force. We hypothesize that our
measurements of PECT force in pigeons were low because superficial, cranial
PECT fibers adjacent to the DPC exerted a disproportionately large bending
moment on the crest during our pull calibrations. In contrast, pull
calibrations of the SUPRA appeared less sensitive to the location along the
tendon at which we pulled. The insertion of the SUPRA is restricted in area,
and the tendon passes through a foramen triosseum, which restricts the line of
action upon the humerus (Baumel et al.,
1993). Nevertheless, the potential inaccuracy of the pull
calibrations means that caution is necessary when interpreting our reported
m, work and Pmus for both muscles.
The accuracy of aerodynamic models of slow flapping flight is uncertain
because unsteady effects may dominate the local flow field and make
quasi-steady models inaccurate (Spedding,
1993; Dickson and Dickinson, 2003). Other empirical studies,
independent of sonomicrometry and strain gauge technology, also show deficits
in power output relative to required power. Early flow measurements identified
only 60% of the necessary momentum in the wake to account for weight support
in the pigeon (Spedding et al.,
1984). Higher resolution of the flow field may eliminate this
measurement deficit (Spedding et al.,
2003), but attempts have not yet been undertaken using pigeons.
Differential pressure transducers on the wings and tails of pigeons yield
measurements of power output sufficient to support 82% of body weight, with an
estimated mass-specific power of 273 W kg–1 under similar
level, slow flight conditions (Usherwood
et al., 2005).
It appears promising that in vitro measurements of
Pmus in the PECT of blue-breasted quail (Coturnix
chinensis) exceed Paero predicted using quasi-steady
aerodynamic models (Askew and Marsh,
2001; Askew et al.,
2001). These measurements use an ergometer to measure force in
isolated fascicle bundles that are stimulated and strained according to in
vivo EMG and sonomicrometry data but, even so, neglect large negative
work components measured in situ that are judged to be artifacts of
the technique (Askew and Marsh,
2001). With integration of in vitro work loop techniques
(Askew et al., 2001), higher
resolution analysis of wake dynamics
(Spedding et al., 2003;
Warrick et al., 2005) and
novel measurements of local pressure
(Usherwood et al., 2005),
together with continued development of DPC strain–force recordings, an
improved understanding of the aerodynamics of flight in birds should emerge.
Nevertheless, our combined force, length change and activation recordings of
the PECT and SUPRA reveal novel functions of these two muscles that depend on
in vivo observations of muscle function.
List of symbols and abbreviations
t
m
Acknowledgments
We thank M. Williamson, D. Stark, R. Hicks and G. Gillis for assistance during experimentation, D. Sheridan and A. Daus for assistance during modeling of aerodynamic power, T. Hedrick for analysis of 3-D kinematics and inertial power requirements, and P. Ramirez for animal care. We also thank C. Ellington and J. van Leeuwen for inviting us to participate in the World Congress of Biomechanics conference session on Swimming and Flying. Supported by NSF grants IBN-9723699 to A.A.B. and IOB-0615648 to B.W.T.
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