Neuromuscular Control and Kinematics of Intermittent Flight in the European Starling (Sturnus Vulgaris)

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The Journal of Experimental Biology 198, 1259Ð1273 (1995) 1259 Printed in Great Britain © The Company of Biologists Limited 1995

NEUROMUSCULAR CONTROL AND KINEMATICS OF INTERMITTENT FLIGHT IN THE EUROPEAN STARLING (STURNUS VULGARIS)

BRET W. TOBALSKE Division of Biological Sciences, University of Montana, Missoula, MT 59812, USA

Accepted 27 February 1995

Summary Electromyographic (EMG) and kinematic data were scapulohumeralis caudalis occasionally showed activity collected from European starlings (Sturnus vulgaris) flying during bounds, which may reflect its role as a humeral at a range of speeds from 8 to 18 m sϪ1 in a variable-speed retractor. The frequency and duration of non-flapping windtunnel. Their flight at all speeds consisted of alternating intervals in starlings were less during EMG experiments flapping and non-flapping phases. Wing postures during than during non-implanted flights. non-flapping phases included glides, partial-bounds and During flapping phases, relative intensity and duration bounds. Glides were performed proportionally more often of EMG signal and wingbeat frequency increased with within each speed and were longer in duration than either flight speed, whereas flapping or non-flapping cycle of the other two non-flapping postures, but the percentage duration, the percentage of a cycle spent flapping and the of bounds increased markedly with increasing flight speed. number of wingbeats in a cycle were all greatest at 8 m sϪ1. The shift from flap-gliding at slow speeds towards flap- Wingbeat amplitude was smaller at intermediate speeds, bounding at fast speeds was consistent with reducing mean but differences among speeds were not significant. These power output relative to continuous flapping. variables allowed indirect estimates of power output and The starlings often combined more than one non- suggested that minimum power speed for starlings was flapping posture within a single non-flapping period. near 12 m sϪ1 and that power output increased at both Transitions between non-flapping postures, as well as slower and faster speeds. Within windtunnel speeds, transitions between bounds and subsequent flapping, were muscle activity changed in relation to wingspan at mid- classified as ‘pull-outs’. Pull-outs consisted of an increase upstroke, wingtip excursion, wingbeat frequency, in wingspan but no change in wingtip elevation. The acceleration, velocity, altitude and horizontal position. pectoralis and supracoracoideus exhibited electrical activity during glides but not during bounds. The scapulohumeralis caudalis was not active during glides, but Key words: European starling, Sturnus vulgaris, intermittent flight, this muscle and the supracoracoideus were typically active flight, electromyography, muscle, kinematics, flap-glide, flap-bound, during partial-bounds and pull-out phases. The partial-bound, power output.

Introduction

Many species of birds exhibit intermittent flight in which greatest at minimum power velocity (Vmp). In contrast, flap- flapping phases are regularly interrupted by phases of gliding gliding should be less costly at slower speeds. Ward-Smith’s (wings extended) or bounding (wings flexed). Flapping flight, (1984b) model for flap-gliding flight predicts that a lower per unit time, has the highest metabolic cost of any form of power output compared with continuous flapping may only be vertebrate locomotion (Tucker, 1968, 1973; Torre-Bueno and achieved during flight at Vmp, whereas Rayner’s (1985) model LaRochelle, 1978; Pennycuick, 1989; Schmidt-Nielsen, 1984). predicts a significant saving at, or slower than, Vmp. Thus, if Is intermittent flight performed in order to reduce energy intermittent flight is a method of reducing energetic costs, birds expenditure during flight? Several mathematical models based should tend to flap-glide when flying at slower speeds and shift upon aerodynamic theory predict that, at fast speeds (generally to flap-bounding at faster speeds (Rayner, 1985). at or faster than maximum range velocity, Vmr), flap-bounding In general, intermittent flight patterns appear stereotypic for should offer a reduction in power output in comparison with bird species and frequently serve as a characteristic for field continuous flapping flight (Lighthill, 1977; Rayner, 1977, identification. The ‘heavy’ flap-bounding flight style of 1985; Alexander, 1982; Ward-Smith, 1984a,b), whereas the woodpeckers (Picidae) is an example of this (Tobalske model of DeJong (1983) predicts that savings should be 1994a,b), as is the flap-gliding of falcons (Falconidae). 1260 B. W. TOBALSKE

Moreover, most of the published mathematical models that chamber in which the starlings flew was walled with clear pertain to intermittent flight behavior treat the two forms acrylic and measured 76 cmϫ76 cmϫ91 cm. Air was drawn independently (Lighthill, 1977; Rayner, 1977, 1985; through the flight chamber by a Buffalo 36-b-vanaxial- Alexander, 1982; Ward-Smith, 1984a,b). These models either asymmetric fan, coupled with a 15 000 W d.c. motor. Airflow imply or explicitly state that a bird species exhibits either flap- was straightened at all airspeeds by a 5 mm honeycomb baffling gliding or flap-bounding, but not both, in order to fly over a (10 cm thick) placed upwind from the flight chamber. Airflow range of speeds. DeJong (1983) developed a model for flap- was laminar in all areas of the flight chamber more than 2.5 cm bounding flight that includes a ‘pull-out’ phase of wing from the walls, and airflow velocity varied by no more than extension that occurs each time flapping resumes after a bound. 4.2 % (Tobalske and Dial, 1994). Wind velocities were The pull-out phase consists of an increase in wingspan without monitored with a pitot tube and an airspeed indicator calibrated wingtip elevation and, according to DeJong (1983), should be with a Davis TurboMeter electronic airspeed indicator. aerodynamically similar to a glide but very brief in duration. From a total of 11 starlings trapped from wild populations Kinematic variation during the pull-out phase dramatically near Missoula, MT, USA, six were willing to fly in the affects flap-bounding efficiency in DeJong’s (1983) model. windtunnel and were therefore used in this study [mean body Empirical evidence regarding what form of intermittent mass 79.2±2.7 g (S.E.M.), mean wingspan 35.4±0.5 cm, N=6]. To flight a bird exhibits across a range of flight speeds is relatively encourage the birds to fly in the windtunnel, I used the methods scarce. Consistent with the hypothesis that intermittent flight of Torre-Bueno and LaRochelle (1978). Over a period of 4Ð6 patterns are fixed for a species, zebra finches (Taenopygia weeks, I trained each starling for approximately 30 min per day guttata) intermittently bound during slow-speed flight when to fly at 8, 10, 12, 14, 16 and 18 m sϪ1. These speeds were intermittent gliding would, according to theory, be less costly selected as they represented the full range of speeds at which all (Rayner, 1985). However, the finches did not fly across a full of the birds would sustain flight for at least 1 min. Various range of flight speeds (Scholey, 1983; Rayner, 1985). By combinations of five starlings were used for each experiment. comparison, budgerigars (Melopsittacus undulatus) flying in a variable-speed windtunnel tend to decrease wing extension Kinematic analysis during non-flapping intervals as flight speed increases, from Starlings (N=5) were filmed and video-taped while flying at glides at slow speeds to partial-bounds at intermediate speeds various speeds in the windtunnel using a Red Lakes 16 mm and to bounds at fast speeds (Tobalske and Dial, 1994). During camera at 200 frames sϪ1, and a Panasonic Hi-8 video recorder flapping phases, wingbeat frequency and patterns of motor-unit at 60 frames sϪ1 with an electronic shutter set at 4000 sϪ1. recruitment in their primary flight muscles also vary Simultaneous lateral and dorsal views of the starlings were considerably, both within and among flight speeds. provided by placing the camera or video recorder lateral to the The conflicting evidence from the studies of finches and flight chamber and using a mirror mounted at 45 û on top of the budgerigars makes it worthwhile to conduct additional flight chamber. Posterior views were obtained by video- experimental studies of intermittent flight in birds. A prediction recording through the fan section behind the flight chamber. that follows from the study of budgerigars is that most birds that All electromyography (EMG) experiments were recorded on use intermittent flight will exhibit flap-gliding at slow speeds and video tape and simultaneous high-speed films were made of flap-bounding at fast speeds (Tobalske and Dial, 1994). In the approximately half of these sequences. An electrical pulse present study, I begin to test this prediction by repeating the synchronized with each frame of film (Kodak 7250 experiments performed upon budgerigars in Tobalske and Dial Ektachrome) was recorded on computer to permit (1994) using European starlings (Sturnus vulgaris) (hereafter synchronization of kinematic data recorded on film (but not referred to as starlings). In addition, I report the effect of airspeed video tape) and EMG data. upon the wing kinematics and muscle activity patterns that Film and video tape were used to study flapping and non- starlings exhibit during flapping and non-flapping phases of flapping intervals. Film was viewed using an L-W motion intermittent flight. Starlings represent a species that commonly analyzer projector (224-S) with a frame counter. Video tapes engages in flap-gliding flight in the wild: Rayner (1985) presents were viewed using a Panasonic AG-1960 video player with a a model for flap-gliding flight based upon this species, and shuttle advance and a television monitor. I identified non- Torre-Bueno and LaRochelle (1978) describe well-trained flapping intervals as phases of no wing movement lasting at starlings to be those that fly in a windtunnel with intermittent, least 15 ms on filmed runs (three frames at 200 Hz) and 33.3 ms ‘brief glides as is typical of starlings in the wild’. There is also on video-taped flights (two frames at 60 Hz). These phases some evidence that starlings flap-bound in nature, at least during were classified into three categories on the basis of my visual migratory flights (Danielson, 1988). estimate of wingspan (glide, wings extended greater than 30 cm; partial-bound, wingspan 5Ð20 cm; bound, wingspan less than 2.5 cm). Intervals during a non-flapping phase in Materials and methods which wingspan increased but wingtip elevation remained Windtunnel and training constant were considered ‘pull-outs’ (DeJong, 1983). I The variable-speed windtunnel used in this study was the categorized wingspan for a total of 1093 non-flapping intervals same as that used by Tobalske and Dial (1994). The flight among five starlings. The percentage of non-flapping phases in Intermittent flight in starlings 1261 each category of wing extension (N=3) was calculated for each 41±0.5 ûC using a heating pad and infrared lamp. Target muscles bird (N=5) at each speed (N=6). Averages among birds were [left side, pectoralis major pars sternobrachialis (PECT), then computed for each speed. supracoracoideus (SUPRA) and scapulo-humeralis caudalis I divided flights into cycles, which began with the onset of (SHC)] were exposed by skin incisions and blunt dissection and flapping following a non-flapping interval and lasted until the then implanted with electrodes (twisted pairs of 100␮m end of the subsequent non-flapping interval(s). Two non- diameter silver wire with 0.5 mm insulation removed at each flapping postures in immediate succession (i.e. without a wing- recording tip and the tips separated by a distance of 1 mm) using flap between them) were considered to be part of the same a 23 gauge hypodermic needle (Basmajian and DeLuca, 1985; cycle, with the portion of time during which wing movement Loeb and Gans, 1986). I used low-voltage electrical stimulation resulting in the transition between postures (pull-out) occurred and visual inspection of wing movements to verify that counting as part of the second non-flapping posture. electrodes were placed in the mid-region of each muscle. Continuous flapping for more than 5 s was considered a Each electrode was sutured to adjacent fascia approximately complete cycle. Using up to ten cycles per bird (N=5) and 5 mm from its exit from the muscle. A short loop of wire was speed (N=6), I recorded the number of wingbeats within the left between the exit point and fascial suture to allow the flapping phase, the duration of the flapping phase (ms) and the electrode tips to move freely with the contracting muscle, thus duration of the non-flapping phase(s) (ms). Average values for reducing low-frequency movement artifacts from the EMG these variables and for the proportion of time spent flapping signals. The electrodes were channeled subcutaneously to a during a flight cycle were calculated for each bird and speed. female miniature connector (Microtech FG-6) which was Kinematics during EMG sequences were examined by sutured to the intervertebral ligaments and opened superficially projecting each frame of high-speed film onto a graphics tablet between the scapulae on the dorsal surface of the bird. (Summagraphics Bit Pad Plus) and digitizing anatomical EMG recordings started the day after an evening surgery. A landmarks (center of head, base of tail and distal tips of wings) lightweight, six-lead cable (Cooner Wire Co.) with a male along with reference points on the flight chamber (Digitizing miniature connector was used for carrying electrical signals and Analysis software, courtesy of Dr Stephen M. Gatesy). from the female connector on the dorsal surface of the bird to Kinematic variables included altitude (relative to the bottom of the recording equipment. EMG signals were amplified and the flight chamber), horizontal position (relative to the back of filtered (Grass P511J, 1000ϫ gain, bandpass filter the flight chamber), wingspan (distance between wingtips) and 100Ð3000 Hz) and recorded directly onto a computer (Zenith wingtip elevation (perpendicular distance of the wingtip above 386SX) via a Keithley 5000 series analog-to-digital (A/D) 12- or below an imaginary line connecting the eye and the lateral bit converter. Digital sampling rates were 5 kHz. base of the tail). I calculated flight velocity using changes in For analysis of motor patterns of the recorded muscles, the altitude and horizontal position of the starling’s eye during EMG signals were displayed from stored digital data using 50 ms intervals. Acceleration was calculated as the rate of custom-built programs (DMAN and DAD, Dr Garr Updegraff, change in flight velocity within the 50 ms intervals. To reduce Data Crunch Inc., San Clemente, CA, USA). EMG bursts were erratic fluctuations in the data, flight velocity and acceleration identified as spikes with rectified amplitude at least two times values were smoothed as a running average over five points greater than the baseline electrical noise. Timing was measured using the formulae in Alexander (1983). at a resolution of 0.5 ms. For each bird, ten consecutive Wingbeat amplitude was estimated using video tapes of wingbeats within a flight (disregarding intermittent non- posterior-view flight. Hi-8 video master tapes were recorded to flapping intervals) were measured for the three muscles at each Super VHS using a Panasonic AG-1960 video player. Video flight speed. I calculated duration of burst (ms), relative frames were then imported to a Macintosh Quadra 950 intensity (the area of the rectified and integrated EMG burst computer using Macintosh Screenplay software. I digitized the divided by the value for the maximum intensity burst observed dorsal wing near the wrist and shoulder using Image software for that electrode) and wingbeat frequency (the reciprocal of (N.I.H.). Wingbeat amplitude was calculated as the angle the time interval from the onset of pectoralis muscle activity described by the pivoting of the shoulderÐwrist line during the during one wingbeat to the onset of pectoralis activity for the time between the beginning of the downstroke and the subsequent wingbeat; Dial, 1992). beginning of the upstroke. I calculated wingbeat amplitude for both wings and averaged the result per wingbeat. Ten wingbeats were measured for each bird and speed. Statistical analysis Values are presented as means ± S.E.M.(N=5 starlings). For Electromyography each of the variables examined in this study, I computed an EMG data were recorded using surgically implanted bipolar average within each bird at each speed (N=6). The distributions electrodes, as in Tobalske and Dial (1994). Birds were deeply of these mean values did not violate the assumptions associated anesthetized using intramuscular doses of ketamine with parametric statistical analysis; thus, I tested for a significant (25 mg kgϪ1) during all surgical procedures. During surgery, effect of flight speed upon each variable by using univariate body temperature was monitored with a YSI telethermometer repeated-measures analysis of variance (von Ende, 1993; and YSE series 400 probe. Body temperature was maintained at MANOVA procedure, SPSS Inc. 1990). The variables tested 1262 B. W. TOBALSKE

100

Fig. 1. Starlings (Sturnus vulgaris) performed glides (black areas) more frequently than bounds (white 40 areas) or partial-bounds (hatched areas) at any flight speed. As flight speed increased from 8 to 18 m sϪ1, the average percentage of bounds increased while the Non-flapping intervals (%) 20 average percentage of partial-bounds remained relatively constant. The trend of an increasing percentage of bounds and a decreasing percentage of 0 8 1012141618 glides at higher speeds was similar to that observed in Ð1 budgerigars (Tobalske and Dial, 1994). Speed (m s ) were: relative intensity of EMG, EMG duration, wingbeat wingbeats within a cycle both decreased with increasing flight frequency, wingbeat amplitude, cycle duration, the percentage speed to reach a minimum at 16 m sϪ1, where cycles lasted of time spent flapping within a flapping or non-flapping cycle 1451.82±187 ms (Fig. 2A) and the number of wingbeats in a and the number of wingbeats within a cycle. cycle was 14.5±2.0 (Fig. 3). At 18 m sϪ1, cycle duration increased to 1719±307.6 ms and the number of wingbeats in a cycle increased to 17.6±3.9. The percentage of time spent Results 10 100 Starlings exhibited glide and partial-bound postures during A Cycle duration Ϫ1 non-flapping intervals at all flight speeds from 8 to 18 m s , % Flapping whereas bound postures were only observed for speeds from 10 8 90 to 18 m sϪ1 (Fig. 1). At all speeds, glides made up over 50 % of the total non-flapping intervals observed, but starlings 6 80 decreased the percentage of glides and increased the percentage of bounds as flight speed increased from 8 to 18 m sϪ1 (Fig. 1). 4 70 A trend with flight speed was not evident for partial-bounds, Cycle duration (s) 2 60 which were always less than 10 % of the total non-flapping intervals within a speed. Non-flapping phases often consisted Flapping phase of cycle (%) 0 50 of more than one wing posture. Of the 751 glides recorded, 6 8 10 12 14 16 18 20 24.9 % were preceded by a bound or a partial-bound, 51 % of 272 bounds were followed immediately by a partial-bound or 100 B glide, and 61 % of 70 partial-bounds were followed immediately by a glide. Glides were always followed by 90 flapping flight, and bounds were always preceded by flapping flight. Pull-out phases, when wingspan increased but wingtip 80 elevation remained near 0 cm (DeJong, 1983), always occurred between two non-flapping postures within a single non-flapping 70 S2 phase and between a bound and subsequent flapping flight. S5 60 S6 Among five starlings, glides lasted 284.1±16.4 ms (S.E.M.),

Flapping phase of cycle (%) S8 whereas the average duration for partial-bounds was S9 50 66.7±6.6 ms and for bounds was 57.0±3.6 ms. Pull-out phases 6 8 10 12 14 16 18 20 lasted on average 43.8±2.4 ms. There was a significant effect Speed (m sÐ1) of flight speed upon the average duration of a flapping or non- flapping cycle (P<0.0005), the percentage of time spent Fig. 2. (A) Flight speed had a significant effect upon the average duration of a flapping or non-flapping cycle (P<0.0005) and the flapping during a cycle (P=0.049) and the number of wingbeats Ϫ1 average percentage of the cycle time spent flapping (P=0.049) for five within a cycle (P<0.0005; Figs 2A, 3). At 8 m s , where the starlings (Sturnus vulgaris) flying at speeds from 8 to 18 m sϪ1 in the values for these variables were highest, cycle duration was windtunnel. Values are means±S.E.M.(B) The percentage of time spent 5806±936 ms, the percentage of the cycle spent flapping was flapping within a cycle for five individual starlings. The pattern 95.3±0.8 % and the number of wingbeats in a cycle was observed for starlings S6 and S9 was considered most likely to 61.2±12.1. Average cycle duration and the number of represent behavior in the wild. Intermittent flight in starlings 1263

90 PECT 80 0.8 SUPRA 70 SHC 60 50 0.7 40 a cycle 30 20 0.6 10 Number of wingbeats within 0 6 8 10 12 14 16 18 20 0.5 Speed (m sÐ1) Relative intensity of EMG signal

Fig. 3. The average number of wingbeats within a flapping or non- 0.4 flapping cycle varied with flight speed (P<0.0005) for five starlings 8 1012141618 (Sturnus vulgaris) flying in a windtunnel. The number of wingbeats Speed (m sÐ1) in a cycle was considerably larger at 8 m sϪ1 than at other speeds. Fig. 5. The average relative intensity of EMG signal in five starlings Values are means±S.E.M. (Sturnus vulgaris) during flapping flight tended to increase with flight speed. Flight speed had a significant effect on the relative intensity of flapping decreased from 8 m sϪ1 to a minimum value at Ϫ1 EMG bursts in the supracoracoideus (SUPRA; P=0.001), a marginally 12ms when the starlings flapped, on average, 78.7±4.9 % of non-significant effect for the relative intensity of the pectoralis (PECT; Ϫ1 the cycle time (Fig. 2A). From 12 to 18 m s , the average P=0.055) and the effect on the relative intensity of the supracoracoideus percentage of the cycle spent flapping was between 82 and (SHC) was not significant (P=0.334). Values are means + S.E.M. 84 %. Trends for all of the variables I examined showed considerable Ϫ1 variation within individuals in comparison to the mean values at 10 m s (92.9±4.1 û) and somewhat greater (between 99.6 Ϫ1 among birds within a speed. For example, in starlings S6 and S9, and 102.5 û) at 8, 16 and 18 m s (Fig. 4). Wingbeat frequency the pattern for the percentage of time spent flapping within a cycle did vary significantly with flight speed (P=0.001), increasing Ϫ1 described an approximately U-shaped curve (i.e. lowest values at from an average of 13.3±0.4 Hz at 8 m s to 16.2±0.2 Hz at Ϫ1 either 10 or 12 m sϪ1 and higher values at slower and faster 18ms (Fig. 4). speeds), whereas the three other starlings I used in this In the PECT and SUPRA muscles, the general trend for both experiment (starlings S2, S5 and S8) decreased the percentage of relative intensity and duration of EMG bursts during flapping Ϫ1 time spent flapping as speed increased from 8 to 18 m sϪ1 was an increase from minimum values at 8 m s through Ϫ1 (Fig. 2B). In general, starlings S6 and S9 appeared more intermediate values at 10 and 12 m s to maximum values at acclimated than the other birds when flying in the windtunnel and they consistently performed longer-duration flights (with less 100 PECT external encouragement) at all flight speeds. SUPRA 90 Flight speed did not have a significant effect upon wingbeat SHC amplitude (P=0.617), although average amplitude was lowest 80

70 17 130 Wingbeat frequency 16 Wingbeat amplitude 60 120 15 50 110 14 Duration of EMG signal (ms) 40 13 100 30 12 8 1012141618 90 Speed (m sÐ1)

Wingbeat frequency (Hz) 11

Wingbeat amplitude (degrees) Fig. 6. The average duration of EMG signal from the pectoralis 10 80 6 8 10 12 14 16 18 20 (PECT), supracoracoideus (SUPRA) and scapulohumeralis caudalis Speed (m sÐ1) (SHC) during flapping flight in five starlings increased with flight speed from a minimum at 8 m sϪ1 to a maximum at 18 m sϪ1. Fig. 4. The average wingbeat frequency increased with flight speed in Differences among speeds were significant for the duration of EMG five starlings (Sturnus vulgaris) (P=0.001). Average wingbeat burst in the pectoralis (PECT; P=0.019) and in the supracoracoideus amplitude was smaller at intermediate speeds but this was not (SUPRA; P=0.008) but marginally non-significant in the significant (P=0.617). Values are means±S.E.M. scapulohumeralis caudalis (SHC; P=0.079). Values are means + S.E.M. 1264 B. W. TOBALSKE higher speeds (Figs 5, 6). An example of this pattern is the was concurrent with changes in wingbeat frequency (Fig. 8) and average relative intensity of the PECT EMG, which was least at wingbeat kinematics, including wingspan at mid-upstroke and 8msϪ1 (0.54±0.06) and greatest at 14 m sϪ1 (0.75±0.03) and wingtip excursion in a parasagittal plane (Fig. 9). During peak 16msϪ1 (0.75±0.05). The duration of the SUPRA EMG was accelerations, generally when a starling was gaining in altitude 44.5±3.0 ms at 8 m sϪ1 and 66.9±5.3 ms at 18 m sϪ1. Differences prior to a non-flapping phase and exceeding the windtunnel among flight speeds were statistically significant for PECT EMG airspeed, wingbeat frequency and the distance the wingtip duration (P=0.019) and for SUPRA EMG relative intensity moved in a lateral plane during a wingbeat were increased, (P=0.001) and duration (P=0.008). Variation with flight speed whereas wingspan at mid-upstroke was decreased (i.e. the was evident but marginally non-significant in PECT relative wingtips were drawn in closer to the midline of the body). Also, intensity (P=0.055) and SHC duration (P=0.079), and variation EMG relative intensity increased and EMG duration decreased in SHC relative intensity (P=0.334) was not significant. for the PECT, SUPRA and SHC muscles. Immediately preceding, or following, non-flapping phases, the starlings Periodic fluctuation in muscle activity and kinematics during tended to decelerate or remain at a constant velocity. Relative flapping phases intensity of EMG, wingtip excursion and wingbeat frequency Within a windtunnel speed, all of the starlings exhibited were decreased, and duration of EMG burst and wingspan at periodic fluctuation in EMG relative intensity and duration, mid-upstroke were increased. Peak negative acceleration of the which was visible in the EMG recordings (Fig. 7). This variation starling usually occurred during the non-flapping phase.

Flapping (1) Non-ﬂapping Flapping (2)

Wingbeat number Wingbeat number 1.25 15 16 17 18 19 20 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17

PECT EMG signal (mV) −1.25

1.25

−1.25 SUPRA EMG signal (mV) 1.25

SHC EMG signal (mV) −1.25 0 200 400 600 800 1000 1200 1400 1600 1800 2000 Time (ms)

Fig. 7. Typical periodic fluctuations in EMG patterns from the pectoralis (PECT), supracoracoideus (SUPRA) and scapulohumeralis caudalis (SHC) during the flapping phases of intermittent flight in starling S9 with windtunnel airspeed at 16 m sϪ1 (corresponds with Figs 8, 9). Similar patterns were seen for all starlings at all speeds. This sequence shows the final six wingbeats from flapping phase 1, a non-flapping phase (a partial-bound followed by a pull-out and then a glide) and then flapping phase 2, consisting of 17 wingbeats. Flapping phase 2 was followed by a partial-bound (not shown). Fluctuations in the peak positive and negative amplitudes of the EMG signals occurred during the flapping phases. In particular, wingbeats 7–14 of flapping phase 2 show increased EMG amplitude for all three muscles. Intermittent flight in starlings 1265

Measurements from 2 s of intermittent flight in starling S9 phase 2, just after the non-flapping phase, to wingbeat 11 of with the windtunnel airspeed at 16 m sϪ1 provide an example flapping phase 2, during the middle of the flapping phase, of the extent of these changes in EMG and kinematic variables wingspan at mid-upstroke decreased from 10 to 2 cm, the (Figs 7Ð9). The sequence consisted of the last six wingbeats difference in wingtip elevation between the start and end of from a flapping phase (1) lasting 410 ms followed by a non- downstroke increased from 25 to 34 cm, the relative intensity flapping phase lasting 310 ms (a partial-bound followed by a of the EMG signal in the PECT increased from 0.28 to 0.36, pull-out and then a glide), and then an entire flapping phase (2) the duration of EMG signal in the PECT decreased from 41 to including 17 wingbeats and lasting 1280 ms. During the two 28 ms, and wingbeat frequency increased from 11.5 to 16.0 Hz. flapping phases, wingspan was always near 35 cm at mid- During the non-flapping phase, wingspan fluctuated slightly downstroke but varied between 2 and 8 cm at mid-upstroke but remained less than 10 cm during the partial-bound, which (Fig. 9). Wingtip elevation varied between 7 and 16 cm at the lasted 115 ms (Fig. 9). The subsequent glide lasted 210 ms, beginning of downstroke and between Ϫ6 and Ϫ17 cm at the during which wingspan first increased to 32.5 cm with a pull- beginning of upstroke. In the PECT, relative intensity of the out, decreased slightly to 30 cm during the next 45 ms and EMG signal ranged from 0.2 to 1.0 and duration of the EMG remained near 30 cm for 120 ms until the end of the glide. The signal ranged from 22 to 41 ms (Fig. 8). Similar variation was wingtip was held approximately 1 cm above the lateral midline observed in the SUPRA and SHC. Wingbeat frequency varied of the body during the partial-bound and first half of the pull- between 11.5 and 16.3 Hz (Fig. 8). out and at 0 cm during the rest of the pull-out and glide. Wingbeats immediately preceding or following the non- During the final six wingbeats of flapping phase 1, the flapping phase were most different from those in the middle of starling’s altitude increased by 26 cm and its horizontal a flapping phase. For example, between wingbeat 1 of flapping position (distance from the back of the flight chamber)

Flapping (1)Non-flapping Flapping (2)

1.0 PECT 0.8 SUPRA SHC 0.6 0.4

Relative intensity of EMG signal 0.2 0

45 PECT 40 SUPRA SHC 35 30 25

Duration of EMG signal (ms) 20 17 16 15 14 13 12

Wingbeat frequency (Hz) 11 14 15 16 17 18 19 (20) 12345678910111213141516(17) Wingbeat number (within flapping phase)

Fig. 8. Relative intensity and duration of EMG bursts and the wingbeat frequency during the flapping phases of intermittent flight in starling S9 with windtunnel airspeed at 16 m sϪ1 (corresponds with Figs 7, 9). Concurrent with maximum accleration (see Fig. 9), the wingbeats in the middle of flapping phase 2 exhibited high relative intensity and short duration of EMG signal and high wingbeat frequency. Wingbeat frequency appeared low, but was not calculated, for wingbeat 20 of flapping phase 1 and wingbeat 17 of flapping phase 2 because these wingbeats were immediately followed by a non-flapping phase. 1266 B. W. TOBALSKE increased by 15 cm (Fig. 9). Also during this time, flight became negative. 20 ms into the non-flapping phase, vertical velocity was approximately 17.2 m sϪ1, 1.2 m sϪ1 faster than position began to decrease and a peak deceleration of the windtunnel airspeed, and acceleration was near 0 m sϪ2. Ϫ7.5msϪ2 occurred. Velocity continued to decline During wingbeat 20, the final wingbeat of flapping phase 1, throughout the non-flapping phase, reaching 15 m sϪ1 by the flight velocity began to decrease and acceleration therefore end of the glide. 200 ms into the non-flapping phase,

Flapping (1) Non-ﬂapping Flapping (2) 40

20 (cm)

Wingspan 10

0 Wingbeat number Wingbeat number 20 1516 17 18 19 20 1 2 3 4 5 6 7 8 9 1011121314151617

0 (cm) −10 Wingtip elevation −20

90 80 70 60 50 Altitude (cm) ÐÐÐÐÐÐÐÐÐÐÐÐÐ

Ð 40 30 Horizontal position (cm)

) 18 1 − 17

Flight velocity (m s 14

5 ) 2 − 0 (m s − Acceleration 5

−10 0 200 400 600 800 1000 1200 1400 1600 1800 2000 Time (ms) Fig. 9. Wingbeat kinematics, body position within the flight chamber, flight velocity and acceleration during intermittent flight in starling S9 with windtunnel airspeed at 16 m sϪ1 (corresponds with Figs 7, 8). During flapping phases, wingspan at mid-upstroke, maximum and minimum wingtip elevation, horizontal position, altitude, flight velocity and acceleration all exhibited periodic fluctuations while wingspan at mid- downstroke remained approximately constant. The starling performed a partial-bound during the first 115 ms of the non-flapping phase. This was followed by a glide lasting 210 ms, the first 45 ms of which was a pull-out during which wingspan increased markedly. Intermittent flight in starlings 1267 horizontal position reached a maximum of 84 cm, whereupon partial-bound), acceleration began to decrease, flight velocity it began to decrease. Acceleration increased from negative reached approximately 17 m sϪ1, and both horizontal and values to 0 m sϪ2 by wingbeat 3 of flapping phase 2. At this vertical positions had increased to values similar to those time, flight velocity reached a minimum of approximately before the previous non-flapping phase. 14.8 m sϪ1, and both horizontal and vertical positions continued to decrease. During wingbeats 9 and 10 of flapping Muscle activity and wing kinematics during non-flapping phase 2, horizontal and vertical positions began to increase, phases flight velocity exceeded 16 m sϪ1 and acceleration reached a I successfully recorded simultaneous EMG and kinematic maximum of 4.5 m sϪ2. During the final wingbeats of flapping data from the PECT, SUPRA and SHC muscles during 84 non- phase 2, prior to the next non-flapping phase (which was a flapping wing postures and 15 pull-outs in four starlings. The

Flapping Non-ﬂapping Flapping 40 Pull-out Glide 30

20 (cm) Partial-bound Wingspan 10

0 (cm) −10 Wingtip elevation −20

1.25

0 (mV) PECT EMG signal −1.25 1.25

0 (mV) SUPRA EMG signal −1.25 Fig. 10. An example of the 1.25 wing kinematics and EMG patterns recorded from starling S9 during a partial- bound followed by a pull-out 0 and then a glide at a (mV) windtunnel speed of 16 m sϪ1. Flapping ended on the SHC EMG signal upstroke before the partial- −1.25 bound and resumed on a 0 100 200 300 400 downstroke after the glide. Time (ms) 1268 B. W. TOBALSKE non-flapping postures included 53 glides, 23 partial-bounds During flight at 16 m sϪ1, starling S9 performed a 200 ms and eight bounds. Eighty-one of these non-flapping postures non-flapping period consisting of a 20 ms partial-bound were from two starlings (starling S6, N=22; starling S9, N=59); followed by a 40 ms pull-out and then a 140 ms glide (Fig. 10). and all 15 of the pull-outs were from these two birds (starling The starling entered the partial-bound during upstroke with S6, N=5; starling S9, N=10). During EMG experiments, very low-amplitude EMG activity present in the SUPRA. partial-bounds were only performed by starlings S6 and S9 and During the partial-bound, the wingspan was approximately bounds were only performed by starling S9. As starling S9 10 cm and wingtip elevation was 0 cm. The PECT and SHC performed all of the non-flapping postures while implanted were inactive and the SUPRA continued to exhibit low-level with EMG electrodes, I will describe the neuromuscular spikes of electrical activity. The partial-bound ended and the control and kinematics of non-flapping intervals in starlings pull-out began as the wingspan began to increase and the PECT using two typical examples of intermittent flight in this bird. exhibited EMG activity. Throughout the pull-out, the PECT

Flapping Non-ﬂapping Flapping 40

20 Pull-out (cm) Bound Wingspan 10

0 20

0 (cm) −10 Wingstip elevation −20 1.25

0 (mV) PECT EMG signal −1.25

1.25

0 (mV)

SUPRA EMG signal −1.25

1.25

Fig. 11. An example of a bound followed by a pull-out phase in 0 starling S9 during flight at a (mV) windtunnel airspeed of 18 m sϪ1. Flapping ended on the upstroke SHC EMG signal before the bound and resumed −1.25 with an upstroke after the pull- 0 50 100 150 200 250 300 out. Time (ms) Intermittent flight in starlings 1269 and SUPRA were active, the SHC inactive and wingtip flapping phases (Figs 7Ð11) probably represent substantial elevation remained close to 0 cm. For most of the glide, the savings in metabolic power output relative to isotonic wingspan was approximately 30 cm, wingtip elevation was contractions during flapping (Goldspink, 1981). near 0 cm, the PECT was continuously active, the SUPRA Models of mechanical power output during level flapping occasionally exhibited spikes of electrical activity and the SHC flight predict a U-shaped curve with a minimum power was inactive. 20 ms before the end of the glide, EMG activity required to fly at an intermediate speed (Vmp) and greater in the SUPRA ceased; 10 ms later the PECT became inactive values at both slower and faster speeds (Pennycuick, 1968b, and 5 ms before the end of the glide the SHC became active. 1975, 1989; Tucker, 1973; Rayner, 1979). Contrary to these Flapping resumed with a 25 ms downstroke as wingspan and models, the rate of metabolic energy expenditure is relatively wingtip elevation decreased. The SHC exhibited electrical constant across measured flight speeds in most of the species activity during the downstroke, and 5 ms after the downstroke of flying animals that have been studied, suggesting a flattened commenced the SUPRA also showed a burst of EMG activity. or J-shaped curve (Ellington, 1991). A flat metabolic power Although the PECT remained inactive during this particular curve is particularly evident in starlings (Torre-Bueno and downstroke, in other instances where flapping resumed with a LaRochelle, 1978), but a classic U-shaped curve is evident in downstroke after a glide, the pectoralis was active (see budgerigars (Tucker, 1968). The trend in the starlings to use Figs 7Ð9). flap-gliding at slow speeds and flap-bounding at fast speeds During a 15 ms bound in starling S9 flying with the (Fig. 1) may explain some of the discrepancies between the windtunnel set at 18 m sϪ1, wingspan was less than 2 cm, predictions of mechanical power models and observations of wingtip elevation was approximately 0 cm and the PECT, relatively constant metabolic power output for birds that use SUPRA and SHC were inactive (Fig. 11). The starling entered intermittent flight, if the birds on which metabolic power was the bound from an upstroke as the PECT and SUPRA were measured exhibited such intermittent flight behaviors during inactive but while the SHC was exhibiting EMG activity. the experiments. During the bound, wingspan and wingtip elevation were The U-shaped metabolic power curve exhibited by constant. The bound was followed by a pull-out phase which budgerigars (Tucker, 1968) seems at first to undermine this lasted 25 ms. During the pull-out, the PECT remained inactive, argument, but it is probable that the additional payload of a the SUPRA and SHC exhibited bursts of EMG activity, mask and a sampling tube used in measuring oxygen wingspan increased and wingtip elevation remained near 0 cm. consumption (Tucker, 1968) would severely limit their use of Activity in the SHC ceased after 15 ms of the pull-out, whereas non-flapping phases. The presence of trailing EMG wires activity in the SUPRA continued for 10 ms into the subsequent appeared to constrain the performance of non-flapping phases flapping phase. Flapping resumed during this period of SUPRA in starlings in the present study, and in previous experiments activity on an upstroke as wingspan increased and wingtip with budgerigars, which have approximately half the body elevation increased. mass of starlings, using trailing EMG wires much greater than 1 g in mass has eliminated their performance of non-flapping phases altogether (Tobalske and Dial, 1994). Significantly, the Discussion flat metabolic curve for starlings was obtained using a closed- Starlings, representing a typical flap-gliding species, tended circuit windtunnel so that the starlings had no increased to flap-glide at slow speeds and flap-bound at fast speeds payload or drag (Torre-Bueno and LaRochelle, 1978). (Fig. 1). Compared with continuous flapping at all flight Intermittent flight is unlikely to result in a flat power curve, speeds, average mechanical power output should be lower if a however, because flight speed had a significant effect upon bird flap-glides at slower speeds and flap-bounds at faster other kinematic and EMG variables in starlings, suggesting, at speeds (Lighthill, 1977; Rayner, 1977, 1985; Alexander, 1982; least qualitatively, that mechanical power output should Ward-Smith, 1984a,b). Thus, starlings, like budgerigars describe a concave curve in approximate agreement with a U- (Tobalske and Dial, 1994), used intermittent flight in a manner or J-shape. The average percentage of time spent flapping in a that was consistent with reducing average mechanical power cycle was least at 12 m sϪ1 (Fig. 2A), which probably reflects output during flight across a full range of speeds. DeJong Vmp for starlings. Average cycle duration, the percentage of (1983) suggests that the use of pull-out phases after bounds cycle time spent flapping and the number of wingbeats in a would make flap-bounding flight less costly than continuous cycle were all greater at 8 m sϪ1 than at other flight speeds flapping at most flight speeds, rather than only at fast speeds. (Figs 2, 3). Thus, average power output is likely to be Thus, the use of pull-outs after bounds in starlings (Fig. 11) relatively large at the slowest speed for which the starlings may explain why I observed some intermittent bounds at all would sustain flight. During flapping phases, however, the speeds except 8 m sϪ1. relative intensity and duration of EMG signals in the PECT, Mechanical power output was obviously higher during SUPRA and SHC muscles along with wingbeat frequency flapping than during glides, partial-bounds and bounds because generally increased with flight speed (Figs 4Ð6), which is periods of no wing movement (Figs 7Ð11) represent no power similar to the pattern seen in budgerigars (Tobalske and Dial, output (i.e. distance of muscle contraction = 0 cm). Periods of 1994). The changes in relative intensity and duration of EMG muscle inactivity and isometric contractions during non- signals directly represent changes in the spatial and/or temporal 1270 B. W. TOBALSKE recruitment of motor units in the muscles (Hagiwara et al. performed proportionally more often than either partial-bounds 1968; Burke, 1981; Basmajian and DeLuca, 1985) and also are or bounds, whereas in budgerigars the durations of all three correlated with force production in muscle (Dial and Biewener, phases are similar and bounds are performed more often than 1993). These trends therefore suggest an increase in power glides at faster speeds (Tobalske and Dial, 1994). This may output per wingbeat as flight speed increases because the explain why starlings are generally recognized as a typical flap- starlings were likely to be using more forceful contractions gliding species (Rayner, 1985), especially if commonly seen with each wingbeat (Dial and Biewener, 1993), the muscles flying at slower speeds (i.e. 8–12 m sϪ1), where over 75 % of were active for a greater percentage of the wingbeat cycle (Dial the non-flapping intervals they performed in the windtunnel et al. 1991; Dial, 1992) and there were more wingbeats per unit were glides (Fig. 1). During migratory flight, starlings flap- time within a flapping phase. Although wingbeat amplitude did bound (Danielson, 1988), which is consistent with my not change significantly with flight speed, the average observations of starling behavior during flight at faster speeds wingbeat amplitude was smaller at intermediate speeds in the windtunnel. Although Danielson (1988) did not measure (Fig. 4). This was approximately similar to the pattern Torre- flight speed, migratory flight speed would probably be Bueno and LaRochelle (1978) report for starlings, and relatively fast and near Vmr (Pennycuick, 1989). indicated slightly less contractile range in the muscle fibers, Danielson’s (1988) observations of starlings during and thus lower power output, during the flapping phases at migratory flight suggest that some differences exist between intermediate speeds (Dial and Biewener, 1993). starling flight in nature and in a windtunnel. For three starlings Across the full range of flight speeds, it was clear that there in migratory flight (speed unknown; Danielson, 1988), average was a general increase in relative intensity and duration of cycle time was 618.3 ms, the percentage of the cycle spent EMG signals with flight speed (Figs 5, 6), but the large flapping was 67.7 %, the number of wingbeats in a cycle was standard errors and, in certain cases, the lack of statistical 4.2 and the wingbeat frequency was 10.1 Hz. By comparison, significance, make detailed comparisons between close speeds the average values among five starlings flying in the rather tenuous. For example, there was a decrease in the mean windtunnel were higher for all these variables at all flight relative intensity of EMG signal in the PECT between 16 and speeds, particularly at 8 m sϪ1 (Figs 2Ð4). Multiplying average 18msϪ1 (Fig. 5), which may have represented a reduction in cycle time during migratory flights by the average percentage recruitment of motor units and a reduction in peak force of the cycle spent non-flapping gives an average duration of production in the muscle (Hagiwara et al. 1968; Burke, 1981; 200.6 ms for bound phases (Danielson, 1988), whereas the Basmajian and DeLuca, 1985; Dial and Biewener, 1993). Two average duration of bounds for starlings in the windtunnel was factors suggest that this was more likely to represent random only 57.0 ms. fluctuation about the mean: between 16 and 18 m sϪ1, the mean Thus, the starlings were probably affected to some extent by relative intensity of EMG signal in the SUPRA and SHC the artificial nature of flight in the windtunnel. This is not a increased (Fig. 5) and there was an increase in the mean surprising result and shows the importance of field studies for duration of EMG signal in all three of the primary flight evaluating the results of laboratory experiments. Power output muscles, which was likely to represent an increase in the time during flight can be reduced for animals flying in confined course of force production during a wingbeat (Fig. 6). spaces or above smooth surfaces, such as in a flight chamber, Regardless of the change occurring between 16 and 18 m sϪ1, because of recirculation of lift vortices (Rayner, 1991; Rayner the mean value for the relative intensity of the EMG signal in and Thomas, 1991). With decreased power costs, the starlings the PECT was greater at speeds between 14 and 18 m sϪ1 than presumably would have flapped less during a cycle in the at speeds slower than 14 m sϪ1 (Fig. 5). windtunnel in comparison with migratory flight, but this was Glide speed in many bird species, including pigeons not the case. Some of the discrepancy between my windtunnel (Columbidae) and raptors (Falconiformes) (Pennycuick, data and Danielson’s (1988) migratory flight data may 1968a; Tucker and Parrott, 1970; Tucker and Heine, 1990), is therefore be explained by the stress that the starlings correlated with a continuum of wing flexion from maximum experienced under experimental conditions in the laboratory or extension at slow speeds to a swept-back, high-speed wing the restriction in changes of altitude caused by the ceiling and posture at fast speeds. In comparison with the behavior of these floor of the flight chamber. The effect of airspeed upon the birds, the glides, partial-bounds and bounds that I observed average percentage of the cycle spent flapping differed in during non-flapping intervals in starlings appeared to represent relation to the apparent willingness with which individual distinct categories of wingspan, just as was observed in starlings flew (Fig. 2B). For the two starlings (S6 and S9) that budgerigars (Tobalske and Dial, 1994). Each posture could I judged to be the most acclimated in the flight chamber, the readily be distinguished from the other two postures on the average percentage of time spent flapping during flight at basis of wingspan (Figs 1, 9Ð11). Furthermore, the starlings 12msϪ1 was near Danielson’s (1988) reported value of 67.7 % performed glides at all speeds and the proportion of partial- and, in starling 9, this value decreased to 61 % during flight at bounds, which appeared to be kinematically similar to the 10msϪ1. high-speed wing posture of pigeons and raptors, did not vary As mentioned previously, obtaining EMG recordings also with flight speed (Fig. 1). affected intermittent flight behavior in the starlings. Cycle Glides in starlings lasted considerably longer and were duration and the percentage of time spent flapping in a cycle Intermittent flight in starlings 1271 both increased, and both the frequency and duration of non- kinematic pattern, with the wings more extended during the flapping intervals decreased. Virtually all of the non-flapping upstroke, is more similar to a continuous-vortex gait with lift phases recorded during EMG experiments were from the two production during the upstroke, whereas the decreased most able fliers (starlings S6 and S9), and only starling S9 wingspan at mid-upstroke that the starlings exhibited during performed bounds while implanted with EMG electrodes. peak positive accelerations was more similar to the vortex-ring Also, the average duration of a bound during non-implanted gait with no lift production during the upstroke (Rayner, 1988). flight was 57 ms, whereas bounds during EMG experiments Wingspan in starlings did not vary as much among mid- generally lasted less than 20 ms (Fig. 11). Rayner (1985) downstrokes as among mid-upstrokes, and starlings always predicts that the percentage of time spent flapping in a cycle entered non-flapping phases during the upstroke and resumed should be greater when the fat load of a bird, and thus body flapping with an upstroke after partial-bounds and pull-outs mass, is greater. My observations support this prediction if the (following a bound; Fig. 11). This behavior is generally added payload of EMG recording equipment can be substituted consistent with the variable nature of upstroke in lift for an increase in mass due to body fat. However, because I production (Rayner, 1985, 1988). However, brief downstrokes lacked control treatments in this study, it was not possible to usually occurred after glides (Figs 9, 10). discriminate between the effects of surgery, EMG electrode The patterns of muscle activity during glides in starlings implantation and added weight or drag due to EMG electrodes (Figs 7, 10) closely resembled those of American kestrels Falco and electrode connections. sparverius (Meyers, 1993), in which the sternobrachialis The periodic changes in relative intensity and duration of portion of the PECT and the SUPRA exhibits EMG bursts. The EMG signals in the PECT, SUPRA and SHC, which starlings EMG activity in the PECT, with no change in wing movement, exhibited during flapping phases at all flight speeds (Figs 7, 8), indicated an isometric contraction functioning to support the are also evident in budgerigars (Aulie, 1970; Tobalske and Dial, body relative to the wing during the glide (Meyers, 1993), and 1994) and black-billed magpies (Pica pica; Olson, 1993). They the SUPRA was presumably functioning as an antagonist to the may represent a common pattern of motor-unit recruitment PECT in order to resist wing depression (Meyers, 1992a, 1993). (Hagiwara et al. 1968; Burke, 1981; Basmajian and DeLuca, Herring gulls (Larus argentatus) and budgerigars also exhibit 1985) during the flapping phases of intermittent flight. EMG isometric contractions in the PECT during glides (Goldspink et bursts of higher relative intensity and of shorter duration were al. 1978; Tobalske and Dial, 1994), but during glides in coincident with peak positive acceleration, increasing altitude budgerigars, the SUPRA does not exhibit EMG activity. and flight velocity exceeding the airspeed in the windtunnel It is unlikely that starlings were generating lift with their (Figs 7Ð9). Wingbeat frequency was higher at these times, as wings during bounds, because the wings were flexed against was the difference between wingtip elevation at the beginning the body and wingspan was minimal (Figs 1, 11), but it is not of the downstroke and the beginning of the upstroke (wingtip obvious whether lift was produced from the wings during excursion), which Scholey (1983) showed to be related to partial-bounds and pull-out phases. Vortex visualization wingbeat amplitude. The changes in relative intensity of EMG techniques would help to clarify whether these phases were signal, wingbeat frequency and wingbeat amplitude indicate more aerodynamically similar to bounds or to glides (e.g. that mechanical power output was greater during the peak Spedding, 1987), but some insight is nonetheless available positive acceleration phases (Dial and Biewener, 1993). from the EMG results (Figs 7, 9Ð11). According to Rayner (1985), if a starling fluctuates between Because the PECT was inactive during some partial-bounds high-speed flapping and slow-speed glides, it should obtain (Fig. 10) and pull-out phases (Fig. 11), it is unlikely that lift increased savings in mechanical power output in comparison was always being produced. If lift were being produced, the with maintaining a constant airspeed during the entire flapping PECT should have been resisting upward wing movement and or non-flapping cycle. Starlings typically performed exhibiting an isometric contraction similar to that recorded intermittent glides in this manner (Fig. 9). Flight velocity during glides (Figs 7, 9, 10) (Goldspink et al. 1978; Meyers, varied around the average incurrent airspeed in the windtunnel, 1993; Tobalske and Dial, 1994). An alternative explanation is with slower speeds recorded during and shortly after a non- that, in the regionally complex PECT, distant motor units were flapping phase and faster flight speeds recorded prior to a non- active but occasionally went unrecorded (Boggs and Dial, flapping phase. 1993; Meyers, 1992a, 1993). During the relatively brief Wingbeat gait is a function of whether the wings produce partial-bounds, pull-out phases and bounds, the functions of lift during the upstroke, and increased wingspan during the the flight muscles may also have been masked by a delay upstroke is a correlate of lift production (Scholey, 1983; between the timing of EMG activity and force production on Rayner, 1988). My observations indicate that starlings the proximal humerus and subsequent kinematic changes at the gradually changed gait within the flapping phases of wingtip (Biewener et al. 1992; Dial and Biewener, 1993). Any intermittent flight. Immediately before, and for some time of these alternatives may also explain why the PECT exhibited after, a non-flapping phase, wingspan at mid-upstroke was EMG activity during the initiation of the downstroke after higher than that observed during peak positive accelerations certain glides (Figs 7, 9) and not others (Fig. 10). (Fig. 9), when the starlings were gaining in altitude and During partial-bounds and pull-out phases, the SUPRA and exceeding the incurrent airspeed in the windtunnel. This the SHC usually exhibited EMG activity (Figs 7, 9, 11; 1272 B. W. TOBALSKE compare with Fig. 10 where the SHC was inactive), which may BIEWENER, A. A., DIAL, K. P. AND GOSLOW, G. E., JR (1992). have represented isometric contractions functioning to Pectoralis muscle force and power output during flight in the maintain the posture of the wing (Salt, 1963) or, especially in starling. J. exp. Biol. 164, 1Ð18. the case of pull-outs when wingspan increased, isotonic BOGGS, D. F. AND DIAL, K. P. (1993). Neuromuscular organization contractions involved in humeral movement. It is difficult to and regional EMG activity of the pectoralis in the pigeon. J. Morph. assess precisely the function of these muscles without more 218, 43Ð57. detailed data on the kinematics of the humerus (e.g. Jenkins et BURKE, R. E. (1981). Motor units: anatomy, physiology and functional organization. In Handbook of Physiology (ed. V. B. Brooks), al. 1988), the electrical activity in more distal wing muscles section 1, The Nervous System (ed. J. M. Brookhart and V. B. (e.g. Dial et al. 1991; Dial, 1992) and the aerodynamics of the Mountcastle), vol. 2, Motor Control, pp. 345Ð422. Bethesda, MD: wing (e.g. Spedding, 1987). American Physiological Society. During bounds in starlings, as in budgerigars (Tobalske and DANIELSON, R. (1988). Parametre for fritflyvende småfugles flugt. Dial, 1994), both the PECT and the SUPRA were inactive (Fig. Dansk. Ornith. For. Tidssk. 82, 1Ð2. 11). These two muscles constitute up to 35 % of the body mass DEJONG, M. J. (1983). Bounding flight in birds. PhD thesis, University of flying birds (George and Berger, 1966); thus, their lack of of Wisconsin, Madison. activity during bounds could represent significant savings in DIAL, K. P. (1992). Activity patterns of the wing muscles of the pigeon metabolic energy during migratory flights, when bounds in (Columba livia). J. exp. Zool. 262, 357Ð373. starlings last approximately 200 ms (Danielson, 1988). The DIAL, K. P. AND BIEWENER, A. A. (1993). Pectoralis muscle force and lack of EMG activity in the SUPRA during bound phases was power output during different modes of flight in pigeons (Columba different from the sporadic EMG activity exhibited during livia). J. exp. Biol. 176, 31Ð54. partial-bounds and pull-outs (Figs 7, 9Ð11). Salt (1963), on the DIAL, K. P., GOSLOW, G. E. AND JENKINS, F. A., JR (1991). The basis of histological study, suggested that the SUPRA functional anatomy of the shoulder in the European starling (Sturnus vulgaris). J. Morph. 207, 327Ð344. functions in wing-fixation during bounds, but my results do not ELLINGTON, C. P. (1991). Limitations on animal flight performance. support this hypothesis. The SHC did not exhibit EMG activity J. exp. Biol. 160, 71Ð91. during the bound shown in Fig. 11, but in other bounds I GEORGE, J. C. AND BERGER, A. J. (1966). Avian Myology. London: recorded bursts of activity similar to the burst observed during Academic Press. the subsequent pull-out in Fig. 11. These occasional bursts are GOLDSPINK, G. (1981). The use of muscles during flying, swimming likely to represent isometric contractions functioning to retract and running from the point of view of energy saving. Symp. zool. the humerus and to keep the wing flexed against the body, Soc., Lond. 48, 219Ð238. because the SHC is a humeral retractor during flapping flight GOLDSPINK, G., MILLS, C. AND SCHMIDT-NIELSEN, K. (1978). in starlings and pigeons (Dial et al. 1991; Dial, 1992). It is also Electrical activity of the pectoral muscles during gliding and likely that muscles besides the SHC, such as the latissimus flapping flight in the herring gull (Larus argentatus). Experientia dorsi and biceps brachii, were active in maintaining a flexed- 34, 862Ð865. wing posture, as they are during perching (Meyers, 1992b). HAGIWARA, S., CHICHUBU, S. AND SIMPSON, N. (1968). Neuromuscular mechanisms of wing beat in hummingbirds. Z. vergl. Physiol. 60, 209Ð218. I sincerely thank Dr Ken Dial for research support and JENKINS, F. A., JR, DIAL, K. P. AND GOSLOW, G. E., JR (1988). A scientific guidance throughout this project. Nate Olson was of cineradiographic analysis of bird flight: the wishbone in starlings great assistance during the experiments and Doug Warrick is a spring. Science 241, 1495Ð1498. provided insights and discussion during analysis and writing. LIGHTHILL, M. J. (1977). Introduction to the scaling of aerial Dr John Hermanson and Dr Alison Cooper provided helpful locomotion. In Scale Effects in Animal Locomotion (ed. T. J. comments and editorial corrections on the manuscript and Dr Pedley), pp. 365Ð404. New York: Academic Press. 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