Take-off mechanics in hummingbirds (Trochilidae)
1 Department of Biology, University of Portland, 5000 North Willamette
Boulevard, Portland, OR 97203, USA
2 Bioengineering 138-78, California Institute of Technology, 1200 East
California Boulevard, Pasadena, CA 91125, USA
3 Biology Department, George Fox University, 414 N. Meridian Street,
Newberg, OR 97132, USA
* Author for correspondence (e-mail: tobalske{at}up.edu)
Accepted 21 January 2004
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Summary |
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Key words: rufous hummingbird, Selasphorus rufus, force, perch, velocity, kinematics, flight
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Introduction |
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The velocity (v) of the center of mass as an animal takes to the
air is determined by mass-specific impulse:
![]() | (1) |
Among the bird species studied to date, take-off appears to be
`hindlimb-driven' in that acceleration to an initial flight velocity is
produced largely by leg thrust during jumping rather than lift from the wings
(Heppner and Anderson, 1985;
Bonser and Rayner, 1996
;
Earls, 2000
).
We hypothesized that hummingbirds would depart from this pattern of
dominant hindlimb contribution and use slower initial flight velocities than
other birds because of their hindlimb morphology. Using what appears to
represent an active upstroke during hovering, hummingbirds move their wings in
a different manner compared with all other flying birds
(Greenewalt, 1960;
Weis-Fogh, 1972
;
Stolpe and Zimmer, 1939
;
Chai and Dudley, 1996
). Lift
production during upstroke may enhance take-off impulse relative to other
birds. However, as members of the Apodiformes, hummingbirds have
proportionally tiny hindlimbs compared with other birds
(Cohn, 1968
), and their
tarsometatarsi make up a smaller proportion of total leg length (19%) compared
with those of passerines (31%; Gatesy and
Middleton, 1997
). During jumping, their morphology should provide
decreased relative hindlimb contribution to F and t
(Bennett-Clark, 1977
;
Johnston, 1991
). Some insects
enhance jump performance using morphological specializations that permit
elastic energy storage in their limbs
(Alexander, 1995
;
Burrows and Wolf, 2002
), but
hummingbirds do not appear to share this design feature
(Zusi and Bentz, 1984
).
We test the effects of motivational state upon take-off mechanics because
these effects are largely unknown. Most studies of animal locomotion assume an
animal is exhibiting either `typical' or `maximal' performance without testing
this assumption or describing the observed behavior within the range of
motivational states available to the animal. In previous investigations of leg
thrust during take-off in birds (Fisher,
1956; Heppner and Anderson,
1985
; Bonser and Rayner,
1996
; Bonser et al.,
1999
; Earls,
2000
), birds initiated flight of their own volition or in response
to hand signals that were intended to stimulate or startle the birds. Earls
(2000
) reports that patterns
of force development in the European starling, Sturnus vulgaris, do
not vary according to flight-initiating stimulus but did not explicitly test
for an effect. Seemingly in contrast, Kullberg et al.
(1998
) and Lind et al.
(2002
,
2003
) report that a mock
predator's attack angle, approach speed and the distance at which the predator
is detected all affect take-off trajectory in tits (Parus spp.).
The high metabolic rate of hummingbirds
(Berger, 1985) and their
competitive aggression when food resources are potentially limited
(Carpenter et al., 1993
)
allowed us to vary hummingbird motivation for initiating flight. We report on
leg forces and kinematics measured during take-off in rufous hummingbirds
(Selasphorus rufus Gmelin) as the birds initiated flight in three
motivational states: autonomously to feed, startled to escape a hand movement,
and aggressively to chase a conspecific from a feeder.
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Materials and methods |
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We measured morphology of the hummingbirds using standard techniques
(Pennycuick, 1989;
Tobalske et al., 1999
);
differences between genders were not significant, so all birds were pooled in
our sample (Table 1). For a
given bird, body mass (g) was an average of all measurements obtained during
experiments as the bird sat motionless on our force perch. Wing measurements
were made with the wings spread as during mid-downstroke. Linear measurements
(mm) were obtained using digital calipers, and areas (mm2) were
measured using digitized photographs with a known scale for pixel-to-metric
conversion.
During experiments, we marked the birds using removable strips of 1-mm-wide tape applied at the shoulder and base of tail to assist us in identifying these anatomical landmarks during later kinematic analysis.
Experimental protocol
The experiments took place within a flight cage, 1 m wide x 2 m long
x 2 m high, constructed of 2.5 cm plastic pipes and covered with 1.36-cm
nylon mesh. Four halogen lights were distributed around the cage to
continuously illuminate the field for video recording. Perches and feeders
were 1 m above the floor and centered within the flight cage except for the
subdominant perch present only during aggressive take-off. This perch was
placed laterally and 25 cm away from the feeder. Feeders were filled with
Nektar-Plus (NEKTON®; Günter Enderle, Pforzheim,
Baden-Württemberg, Germany) and suspended from the ceiling of the cage.
In aggressive experiments, we exercised the option of blocking the
hummingbirds' access to the food by lowering the feeder(s) into a container on
a platform under the feeder.
Birds took to flight in one of three motivational states: to feed on their own volition (hereafter referred to as `autonomous'), to respond to a startling human motion (hereafter `escape') or to chase a conspecific away from a feeder (hereafter `aggressive'). We obtained two take-offs per bird for each motivational state sampled, although only four out of six birds were sufficiently dominant to provide aggressive take-off.
Autonomous and escape take-off occurred with one bird, two freely available feeders at either end of the flight chamber, 1 m above the ground, and a force perch 1 m high and located in the center of the flight chamber. During autonomous take-off, the bird voluntarily initiated flight from the perch to a feeder, flew directly to a feeder and immediately began feeding. During escape take-off, the bird on the perch was startled by a single hand elevation performed by one of the experimenters seated a distance of 6 m from the cage. The bird initiated flight from the perch and flew around the cage without feeding.
Aggressive take-off involved a dominant bird as the test subject chasing a subdominant bird away from a single feeder in the cage. The pair of birds remained in the cage together, with free access to food, for 324 h before the recording of aggressive take-off. During the experiment, we would periodically block access to the feeder. Because the dominant bird always preferred the perch in the center of the flight chamber, the subordinate bird was relegated to a non-instrumented perch located laterally and 25 cm away from the feeder. When the feeder was raised to permit access, the subdominant immediately took off and flew to the feeder to begin feeding. The dominant bird would then take off and chase the sub-dominant bird away from the feeder before returning to feed itself.
Data acquisition
We used a custom-made perch instrumented with strain gauges (120 ,
type EA-06-125ad-120; Micro-Measurement, Vishay Measurements Group, Rayleigh,
NC, USA) to measure leg thrust. Our single-beam design was adapted from
Biewener and Full (1992
). It
had an 11-cm steel rod 1.5 mm in diameter in the center. On both ends of this
rod, two twin-bladed force transducers were constructed as half-bridge
circuits to yield horizontal and vertical forces; signals were amplified
2000x using separate channels of a strain gauge amplifier (2120B; Vishay
Measurements Group). We used known masses (g) to calibrate the strain-gauge
amplifier output from volts into Newtons. Resonant frequency of the perch was
75 Hz. Ideally, all bending in this perch would occur at the force transducers
but, due to the small diameter of the central rod, necessary to accommodate
tiny hummingbird feet, the central rod flexed slightly during experiments.
This flexure caused the transducers to be most sensitive to force when a bird
was centered on the rod. Thus, we calibrated horizontal and vertical forces
along the central rod and, for each take-off, used a location-specific
calibration appropriate for the bird's position on the perch as verified using
high-speed video (250 Hz; Motionscope 250; Redlake, San Diego, CA, USA).
Analog output from the strain-gauge amplifiers was sampled at 5000 Hz using a
16-bit data acquisition system (Digidata 1320A; Axon Instruments, Union City,
CA, USA) and subsequently stored for analysis on a computer. Force recordings
were synchronized with our Motionscope camera and an additional high-speed
video camera (1000 Hz; PCI-2000; Redlake) using a Transistor-Transistor Logic
(TTL) pulse that triggered our video cameras.
Flight kinematics were obtained from digital video. The Redlake PCI-2000 provided a lateral view (1000 Hz; stored using PCI-R v2.18 software) to digitize wing and body motion. The Redlake Motionscope 250 (250 Hz) provided a cranial or caudal view for perch calibration and correction of lateral-view parallax. Analog output from the Motionscope was imported to computer and stored using Quicktime v. 3.5 software (Apple, Cupertino, CA, USA). For both cameras, we used a shutter speed of 1/4000 s.
Data analysis
To facilitate comparison with other species, we adapted methods in Earls
(2000) in our definition of
take-off and its components. In brief, take-off started (relative timing=0%)
when horizontal force production, as recorded using the force perch, reached
5% of body weight (henceforth called `begin leg thrust'). The end of take-off
(relative timing=100%) was the first upstrokedownstroke transition
after the feet broke contact with the force perch. The end of foot contact,
when horizontal and vertical forces reached 5% of body weight, represented
`end leg thrust'. Wing movements were classified as upstroke or downstroke
based on movement of the wrist relative to the midline of the body. Body angle
was the acute angle between the midline of the body and horizontal, with the
midline described as a line connecting the shoulder and middle base of the
tail. We assumed that the center of mass of the body was halfway between the
shoulder and the base of the tail. Counter-movement was identified using
vertical movement of the center of mass; because this movement was sometimes
minimal, we used vertical head movement to help verify its timing.
We sampled take-off from 10 ms (10 frames at 1000 Hz) before the start of any change in body angle or position of the center of mass to 10 ms after end of take-off. For each frame of video in the sample, we digitized the wing tip, base of the shoulder and base of the tail using Didge software (v. 2.1; Alistair Cullum, Creighton University, Omaha, NE, USA). During experiments, we marked the birds using removable strips of 1-mm-wide tape applied at the shoulder and base of tail to assist us in identifying these anatomical landmarks during later kinematic analysis. Digitized points were converted to metric coordinates using a known scale, and subsequent analysis was performed using Igor Pro software (v. 3.5; Wavemetrics, Inc., Lake Oswego, OR, USA).
We plotted position of the center of mass as a function of time and fitted the data with a polynomial curve. The degree of the polynomial curve was selected using the constraint that residuals must be <0.5 mm. We calculated body velocity and acceleration using differentiation of this fitted curve. Total velocity represents the time history of total accelerations derived from the combined forces produced by the legs and the wings.
To evaluate accuracy of our digitizing and kinematic analysis, we conducted a ball-drop acceleration test. The second derivative of position of the ball as a function of time yielded a value for g of 9.79 m s2, a 0.14% error.
Measurements from our force perch were used to calculate the relative
contribution of the legs to velocity of the center of mass
(Earls, 2000). Body weight was
subtracted from vertical force. Horizontal and vertical velocities were then
integrated from acceleration after the measured force was divided by the
bird's body mass. We used our video measurements of horizontal and vertical
velocity at the start of leg thrust to define our horizontal and vertical
integration constants for the force data.
After analyzing 33 take-offs, we tested for statistically significant differences among treatment means using repeated-measures analysis of variance (ANOVA; StatView v. 5.0.1; SAS Institute, Cary, NC, USA). We report means±S.D. for N=6 birds for autonomous and escape take-off and N=4 birds for aggressive take-off, so d.f.=3,2 for all repeated-measures ANOVA.
Comparative analysis
We compared hummingbird take-off performance with that of other species
using previously published accounts (Bonser
and Rayner, 1996; Earls,
2000
; Tobalske et al.,
2000
). Additionally, we obtained unpublished data collected in
association with Tobalske
(1996
), Tobalske and Dial
(2000
), Tobalske et al.
(2000
), Zimmerman and Tobalske
(2000
) and a new empirical
study in the field (B. Brandsma, unpublished data). In cases where body mass
was not measured, we used average mass for the species, specific to gender if
known (Dunning, 1993
).
Kinematic and force data for one zebra finch (Taeniopygia guttata;
15.2 g) engaged in autonomous take-off in our flight chamber at a flight
distance of 10 m were recorded in the same manner as for hummingbirds. We also
incorporated data on velocity at end of take-off in 15 other species up to the
mean body mass of wild turkey (6.5 kg).
We tested for an effect of body mass on velocity at end of take-off using
reduced-major axis (RMA) regression of independent contrasts [Phenotypic
Diversity Analysis Program (PDAP) v. 5.0; J. A. Jones, P. E. Midford and T.
Garland, Jr, University of Wisconsin, Madison, WI, USA]. Independent contrasts
account for the non-independence of species due to phylogenetic relationships
(Garland et al., 1992). Our
hypothesized phylogeny was based on DNADNA hybridization data and
average linkage (UPGMA) data in Sibley and Ahlquist
(1990
); we assumed uniform
branch lengths. With 16 contrasts and all nodes resolved, d.f.=15 for the RMA
regression. Velocity and body mass were log-transformed prior to this
analysis. As take-off data from birds in the field probably included birds
with varying motivation, for the hummingbird velocity we used a mean velocity
among all three motivational states.
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Results |
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Mean duration from start of body movement to the end of take-off was 120.8±26.0 ms during autonomous take-off (Figs 1, 2). Within this time interval, mean take-off duration, from the start of leg thrust to the start of the first downstroke after the end of leg thrust, was 81.3±8.7 ms. Hummingbirds used their legs to apply thrust to the perch for 71.0±10.8 ms. After the start of leg thrust, vertical force on the perch varied about a mean value representing weight support, while horizontal force increased until reaching a peak of 25.4±5.2 mN (0.8x body weight) after the first downstroke. Peak vertical ground-reaction force averaged 47.3±5.5 mN (1.6x body weight) and occurred 6.9±5.7 ms after peak horizontal force (Fig. 2). Peak horizontal acceleration due to leg thrust averaged 8.3±1.8 m s2, and peak vertical acceleration (including g) was 14.8±2.0 m s2. Peak acceleration due to the hindlimbs was 5075% of peak acceleration due to the legs and wings combined (Fig. 3A); the peak acceleration due to legs and wings averaged 27.0±7.6 m s2.
|
Velocity increased between the end of leg thrust (0.56±0.08 m s1) and the end of take-off (0.06±0.08 m s1; Figs 1, 3B). The percent contribution of leg forces to total velocity at the end of leg thrust was 62.5±18.6%; by the end of take-off, this percent contribution declined to 50.5±11.4%.
Hummingbirds completed 2.4±0.4 wingbeats (range 25) before
ending leg thrust. This is different from other bird species
(Earls, 2000), including the
zebra finch (Fig. 2), which are
only partially through one downstroke before ending leg thrust. Also, in
comparison with other bird species, hummingbirds took off more slowly
(Bonser and Rayner, 1996
;
Earls, 2000
;
Tobalske et al., 2000
;
Zimmerman and Tobalske, 2000
;
Fig. 4). Our regression of
species data and independent contrasts illustrated that velocity at the end of
take-off increased as body mass increased (P<0.01;
Fig. 4B). Velocity varied from
0.7 m s1 to 4.1 m s1 over a size range
from the 3.5 g hummingbird to the 6.5 kg wild turkey
(Fig. 4A). Although the slope
of the independent contrasts regression, proportional to
Mb0.26, was significantly different from zero,
only 42.3% of the variation in take-off velocity was explained by variation in
mass. This suggests that other unmeasured variables, including morphology and
motivation, will help account for variation in performance.
|
Effects of motivational state
Hummingbirds altered certain aspects of their take-off performance
according to their motivational state. Mean duration from start of body
movement to the end of take-off was shorter for escape and aggressive take-off
compared with autonomous take-off (P=0.02;
Fig. 2). Percent leg
contribution to total velocity was less during escape (46.2±18.5%) and
aggressive (47.0±9.9%) compared with autonomous take-off
(59.1±12.2%), but the differences were not statistically significant
(P>0.3). Peak acceleration, due to combined hindlimb and wing
forces, varied significantly with motivational state (P=0.008;
Fig. 3A); a maximum of
37.4±10.1 m s2 was exhibited during chase take-off.
There was a significant effect of motivation on the magnitude of peak vertical
force from the legs (P=0.02), which was lower during autonomous
take-off than during escape and aggressive take-off. Although peak horizontal
force from the legs was greater during escape take-off than during autonomous
or aggressive take-off, differences were marginally non-significant
(P=0.09). Likewise, peak resultant hindlimb force and direction
varied according to motivational state, but the differences were marginally
non-significant (P=0.11 and P=0.14, respectively). Peak
resultant force, measured using the force perch, varied from 46.7±4.4
mN (1.5x body weight) during autonomous take-off to approximately 55 mN
(1.8x body weight) during chase and aggressive take-off
(Fig. 3A). The angle of this
resultant, relative to horizontal, was greater during startle
(77.9±12.0°) than during autonomous (65.8±9.4°) and
aggressive (65.1±6.5°) take-off.
Velocities were lower during autonomous take-off compared with escape and aggressive take-off. Among motivational states, there was a significant difference in velocity at the end of leg thrust (P=0.04), but the observed differences were marginally non-significant for velocity at the end of take-off (P=0.08).
Compared with autonomous and aggressive take-off, escape take-offs featured earlier start of wing movement and more wingbeats before the end of leg thrust. There was a significant effect of motivational state upon wingbeat frequency (inverse of wingbeat duration) in the first wingbeat (P<0.05) but not the second wingbeat (Fig. 3C). There was also a significant difference among motivational states in the relative timing of wing kinematics, including start of wing unfolding (P=0.04), start of first downstroke (P=0.02), start of first upstroke (P=0.01) and start of second downstroke (P<0.01).
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Discussion |
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As take-off velocity is proportional to impulse (equation 1), our results indicate that hummingbirds exhibited proportionally lower F or t relative to other birds. Given that the upstroke is presumed to be active in hummingbirds, and lift from the wings should contribute to F, it is significant that their unique wingbeat style did not result in a comparatively faster take-off velocity (Fig. 4).
Positive scaling of take-off velocity with body mass among species
(Mb0.26;
Fig. 4) suggests that species
in our sample were not geometrically or dynamically similar
(Hill, 1950;
Pennycuick, 1992
;
Marsh, 1994
). Inferring from
data available on functional morphology and jump mechanics in anuran
amphibians (Marsh, 1994
), we
anticipate that relatively small hindlimb muscles in hummingbirds limit
F, whereas relatively short limb length, proportionally small
tarsometatarsi and high intrinsic rates of muscle shortening limit t.
However, regardless of hindlimb proportions, take-off velocity was relatively
slower in smaller birds. As the hummingbirds were the smallest species in our
sample, small body mass and unique hindlimb morphology are confounded. Further
comparative study is, therefore, warranted before it may be accepted that
hindlimb morphology limits take-off velocity in the hummingbird.
Evidence of a de-emphasis of leg contribution to take-off in hummingbirds
includes early onset of wing beating (Figs
1,
2), hindlimb forces
contributing only half of the total velocity at the end of take-off, and small
accelerations due to hindlimb forces (Fig.
3A). In comparison, other species are only halfway through their
first downstroke, when their feet end contact with the ground
(Earls, 2000;
Fig. 2), and hindlimb
contribution to take-off velocity is greater than 80% in other species
(Earls, 2000
;
Tobalske et al., 2000
;
Zimmerman and Tobalske, 2000
).
Peak accelerations due to hindlimb force are also greater in other species,
ranging from a reported low of 15.6 m s2 in pigeons
(Heppner and Anderson, 1985
)
to 2540 m s2 in starlings
(Bonser and Rayner, 1996
;
Earls, 2000
) and to 76.5 m
s2 in quail (Coturnix coturnix;
Earls, 2000
).
Motivation had an effect upon wingbeat kinematics and mechanics including peak resultant acceleration due to leg and wing forces, peak vertical force from the hindlimbs, and velocity at the end of leg thrust (Fig. 3). Using velocity as a measure of performance, escape and aggressive take-off were similar and, therefore, may both potentially represent maximal effort in hummingbirds. However, these types of take-off were not equivalent. Compared with aggressive take-off, during escape hummingbirds started wing motion relatively earlier and used wingbeats of higher frequency. Also, during escape take-off, hindlimb forces tended to be greater, resultant peak force from the hindlimb was oriented more vertically, total peak acceleration was greater, and the duration of leg thrust was shorter (Fig. 3A,C).
Our results provide new insight into the role of motivational state upon
locomotor performance, particularly with regard to wing kinematics and leg
thrust (Fig. 2). Ecologically
relevant motivational states should be incorporated into experimental design
in much the same way that morphological or physiological characteristics often
have been (e.g. Witter et al.,
1994; Swaddle et al.,
1999
; Veasey et al.,
2001
; Burns and Ydenberg,
2002
). The importance of animal motivation may be broadly
underestimated in lab and field studies of locomotion. Among the range of
possible behavioral motivations for taking into the air, perceived risk of
predation is the only factor that has received extensive study
(Kullberg et al., 1998
; Lind
et al., 2002
,
2003
). Kullberg et al.
(1998
) show that attack
avoidance has an effect on take-off performance, whereas daily variation in
body mass does not. When escaping models of predators, small birds tend to
vary flight trajectory rather than velocity
(Kullberg et al., 1998
; Lind
et al., 2002
,
2003
); this may hint that
velocity at the end of leg thrust is always maximal when a bird perceives a
threat.
As many investigations into animal take-off focus on the flight path of a
bird after it has left the ground, data are often lacking regarding what are
likely to be significant leg contributions to take-off performance
(Earls, 2000;
Fig. 1). Comparative
experiments that couple behavioral manipulations with mechanical measurements
should, therefore, improve our understanding of the ecological and
evolutionary implications of take-off flight.
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Acknowledgments |
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