The energy cost of loaded flight is substantially lower than expected due to alterations in flight kinematics
1 Aberdeen Centre for Energy Regulation and Obesity, School of Biological
Sciences, University of Aberdeen, Aberdeen AB24 2TZ, Scotland, UK
2 The Waltham Centre for Pet Nutrition, Waltham-on-the-Wolds,
Leicestershire, LE14 4RT, England, UK
3 Aberdeen Centre for Energy Regulation and Obesity, Division of Energy
Balance and Obesity, Rowett Research Institute, Bucksburn, Aberdeen AB21 9BS,
Scotland, UK
* Author for correspondence (e-mail: c.hambly{at}rowett.ac.uk)
Accepted 10 August 2004
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Summary |
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Key words: cockatiel, Nyphicus hollandicus, flight cost, wing loading, labelled bicarbonate, kinematics
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Introduction |
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Kvist et al. (2001)
confirmed that the consequences of seasonal changes in body mass of red knots
Calidris canutus for flight costs were considerably lower than would
be aerodynamically expected. They attributed this increased efficiency to
alterations in the performance of the flight muscles with increasing mass.
This latter study examined the effect of natural increases in mass, by laying
down fat reserves, for constant forward flight in a wind tunnel. Since wind
tunnel flight is unidirectional it may be a good model for migrational flight
behaviour, but may be a relatively poor reflection of day-to-day flight
activity because it does not include the complex aerial behaviours that occur
in free-flying birds. One previous study has examined the energetic and
behavioural consequences of adding long-term artificial masses during free
flight. Nudds and Bryant
(2002
) added up to 28% of the
unloaded body mass to zebra finches Taeniopygia guttata, which in
theory was predicted to generate an increase in the mechanical power of flight
by 4050% The payload mass remained on the birds at all times during
this study so it was more comparable to seasonal changes because the bird had
time to adjust to the mass increase. The cost of carrying a payload mass was
found to be predominantly behavioural, affecting take-off velocity, rather
than energetic, although the birds responded to the increased payload mass by
reducing their body mass.
Seasonal changes in body mass, however, may affect birds differently than
short-term changes in mass because the birds can build up flight muscle as
well as fat (Brodin, 2001),
whilst also decreasing the contribution of energetically costly components
such as the alimentary tract (Piersma,
1998
). Increases in muscle mass while reducing the masses of other
organs may explain the unanticipated rise in efficiency with increased body
mass observed in knots (Kvist et al.,
2001
), suggesting the low cost-effect may pertain only to seasonal
changes in wing-loading, and not more short-term changes such as daily mass
variations and carrying of prey loads. Videler et al.
(1988
) examined the kinematics
of kestrels Falco tinnunculus, which were trained to fly with lead
masses, of up to 30% of their initial body mass, attached to their feet. These
birds flew at a slower speed, with increased wing beat frequency and wing
amplitude. Microchiropteran bats (Microchiroptera), which are more used to
carrying heavier loads such as foetuses or offspring, exhibited similar
patterns. When carrying up to 46% of their body mass, they also reduced flight
speed and increased wing beat frequency
(Hughes and Rayner, 1991
).
Energy expenditure was not measured directly in these latter studies. Birds
may be able to alter their flight kinematics to reduce the energetic effect of
flying at heavier masses over short periods when they cannot modify their body
composition.
The few measurements of flight costs with variations in body mass rely on
the doubly labelled water (DLW) technique or aerodynamic models (e.g.
Kvist et al., 2001;
Nudds and Bryant, 2002
). In
the study by Nudds and Bryant
(2002
) the birds were only
flying for up to 4% of the total measurement period, which therefore required
substantial extrapolation to estimate flight cost for 100% of the period.
These extrapolations using DLW have been shown previously to introduce
significant error into the derived estimates
(Speakman and Racey, 1991
).
The aim of the present work was therefore to examine the response to flight
cost for short-term increases in mass, using a more direct technique. This was
achieved by measuring energy cost using the 13C-labelled
bicarbonate technique in cockatiels Nyphicus hollandicus, flying
whilst carrying external artificial loads equivalent to up to 20% of the
unloaded body mass. The resulting flight behaviour was then examined using
high-speed video footage to observe changes in flight speed, wing amplitude,
up- and downstroke duration and wing beat frequency
(Fb).
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Materials and methods |
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A standard dilution curve for the NaH13CO3 solution
was obtained to enable calculations to be made on the bicarbonate pool size in
each bird using the same methodology as described in Hambly et al.
(2002).
Responses to artificial loads
Birds were trained, for a period of 2 weeks, to fly between perches 20 m
apart along a corridor. Raising a hand slowly towards the bird gave it the cue
to fly to the perch at the other end of the corridor. Each bird was also
trained to fly while carrying a small flat backpack (approx 1.2 g in mass).
This was either attached dorsally with Velcro® straps in a figure-of-eight
pattern in loops under each wing, or ventrally using the same backpack with
the Velcro® straps around the neck and tail regions. Careful observation
during the initial flights suggested that there was no visible restriction of
flight, or changes in the flight behaviour observed while carrying the
backpack, although detailed analysis could not be performed at this stage due
to absence of the high-speed video equipment.
These five trained birds were then flown for carefully timed periods of 2 min after injection with 0.8 ml of the 13C-labelled sodium bicarbonate solution. Prior to flight, wing span was measured and wing area calculated by drawing round the wing. Graph paper was taped to the edge of a table and the bird's body aligned with the table so that the wing lay flat along the graph paper. The wing was carefully out stretched to the same degree in all birds to maintain a comparable estimate of area across individuals. Total wing area was then multiplied by 2 after counting the enclosed squares on the graph paper, and adding the area across the back, which was assumed to be a rectangle (using the wing span minus the length of the two measured wings as one side, and the distance between the top and bottom of the wing as the other). Background breath samples were collected prior to injection. Birds were placed in the same chamber with the same rate of air flow (2 l min1) as used in the calibration study, and samples were collected each minute between 1 and 20 min after injection. After 20 min, the birds were taken out of the chamber and then released and encouraged to fly back and forth between the two perches. The flight time was carefully timed to the nearest second over the 2 min flight period and was also recorded on a Hi-8 Panasonic video camera to enable accurate measurement of the total time the bird was in flight. In addition, a short period of each flight (19 s) was recorded on a Kodak EM high-speed video camera at 500 frames s1 to examine flight kinematics. The camera was orientated head-on and had an 1175 mm zoom lens. After flight, the birds were quickly recaptured and were then immediately placed back in the chamber where further breath samples were collected for the following 7 min.
After the initial unloaded flights, the birds underwent further experiments in which they flew while carrying a backpack, with the mass experimentally manipulated by adding fisherman's non-toxic heavy putty. The putty was shaped to be thin and rectangular and was moulded over the surface of the bird's back to reduce drag. Masses were initially attached to the dorsal surface, and the amount added was calculated to within 0.1 g as a percentage of each individual bird's body mass, including the mass of the harness. Masses of 5, 10, 15 and 20% of the bird's body mass, measured prior to flight, were added, with a cross-sectional area of 0.251 cm2, depending on the mass added. The same flight procedure as previously described was carried out and breath samples were collected prior to and after flight using the same methodology. One final manipulation involved adding 10% of the body mass to the ventral surface of each bird. Flights by each bird were conducted on three separate occasions at each mass manipulation and the masses were removed directly after the flight. Each bird therefore made a total of 18 flights during this study.
Data analysis
All statistical analyses were conducted using Minitab 11 software. Values
are means are ± standard error (S.E.M.). Linear regression,
multiple linear regression, general linear model (GLM) and paired
t-tests were used for our analysis.
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Results |
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To calculate the pool size, the isotope enrichment values (delta) of the
bicarbonate solution, injected directly into vacutainers with varying
quantities of CO2, were log-converted and plotted against the
log-converted volume of CO2 gas added (moles). The relationship was
linear and significant (regression; F1,31=7367.5,
P<0.001; Fig. 3).
The equation from the least-squares linear regression on these data was used
to calculate the body bicarbonate pool size (Nc) by
interpolating the enrichment of 13C at the plateau onto this
relationship. The closest relationship between
kcNc and metabolism occurred
2030 min after injection (Fig.
2B), with a strong significant relationship (linear regression;
F1,20=49.54, P<0.001). There was no
significant difference between individuals (one-way ANOVA;
F7,20=2.43, P=0.08), indicating that the repeated
measurements did not significantly influence the relationship between
kcNc and
O2. The equation
for this regression was subsequently used to predict the oxygen consumption
during flight from a measured isotope elimination rate multiplied by
bicarbonate pool size, during this time interval.
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Flight costs
The elimination rate for the time the bird was flying was calculated as
described in Hambly et al.
(2002)
(Fig. 4).Timings for the total
flight period were corrected for the time that the bird spent on the perch at
either end of the flight corridor. The body bicarbonate pool size was
calculated as described in the calibration, using the isotope enrichment at
the plateau, and this was again multiplied by the elimination rate to
calculate kcNc.
kcNc was interpolated onto the
calibration equation and the corresponding
O2 was
predicted.
O2
was in turn converted to flight cost (in W) using the RQ measured in a subset
of these birds as performed in the accompanying paper
(Hambly et al., 2004
).
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Mean flight cost including all aerial behaviours (horizontal forward flapping flight, ascent, descent, take-off and landing) in the pre-manipulated birds was 16.7±1.8 W and pre-manipulation flight parameters are listed in Table 1. The relationship between the mean pre-manipulated flight cost and changes in the main flight parameters (body mass, wing span, wing area, wing loading, flight speed, amplitude, up- and downstroke duration and Fb) were examined to locate factors that affected flight cost in these non-manipulated individuals using a multiple linear regression. Upstroke duration (regression; T=3.45, P=0.004), the ratio between up- and downstroke duration (regression; T=3.85, P=0.002), flight speed (regression; R=6.35 P<0.001) and wing beat frequency (regression; T=2.24, P=0.04) all had significant relationships with flight cost.
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Changes in flight costs with increasing body mass were examined by adding masses only to the bird's back. The mean flight cost increased linearly with increasing percentage of body mass added (Fig. 5). The r2 for this linear relationship was extremely high at 93%; however, the difference between the mean flight cost in the pre-manipulated birds and that of the birds carrying a 20% increase in body mass was only 1 W, an increase of 5.4% (between 16.7 and 17.7 W) (Table 2).Since there was a high degree of variation within each manipulation there was no significant increase in the individual flight costs when masses were added (GLM; F4,65=0.11, P=0.98). There was, however, a significant difference in flight cost between individuals, with some birds consistently flying with a higher flight cost than others (GLM; F4,74=24.53, P=0.001). The mean flight cost when the 10% mass was added ventrally was not significantly different from when the weight was added dorsally (paired t-test; T=0.4, P=0.7).
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Flight kinematics
Flight speeds and Fb were calculated from the high- and
low-speed video recordings. The Hi-8 videotape was recorded at 25 frames
s1. Individual frames were used to calculate accurately the
time taken for each individual to fly between the two perches 20 m apart for a
minimum of 20 flights spread throughout each flight period. The start and end
of each flight occurred when the birds' feet left the first perch and touched
the next perch, respectively. In addition, Fb, up- and
downstroke duration and amplitude were calculated using the high-speed video
footage, recorded at 500 frames s1. Individual wing beat
cycles were carefully timed throughout the 19 s of recorded footage to the
nearest 0.002 s, for complete cycles only. Wing amplitude was measured by
freezing the frame at the top of the wing beat and tracing the wing angle on
acetate. The point at the tip of the beak was also marked. The film was then
forwarded to the point when the wing was at the bottom of the wing beat and
the acetate was placed over the bird with the beak in the same location and
the wing retraced. The angle between the up- and downstroke was calculated.
The mean kinematic data prior to manipulation are shown in
Table 1. Flight speed averaged
7.2±0.17 m s1 and Fb averaged
9.21±0.08 beats s1 in the control measurements. These
values were compared to the mean values measured when the payload weights were
added. Flight speed decreased when heavier payload weights were added, with
the exception of the weight amounting to 20% of body mass
(Fig. 6A). The decrease was
only significantly lower than pre-manipulated measurements when weights
equivalent to 15% of body mass were added (one-way ANOVA;
F4,64=3.6, P=0.01). Fb showed
a trend to increase with increasing payload weights, which only became
significantly different from the control when payload weights were equal to a
20% increase in body mass (one-way ANOVA; F4,65=7.6,
P>0.01; Fig. 6B).
There was also no significant difference in flight speed or
Fb depending on whether the weight was added dorsally or
ventrally (paired t-test; speed, T=0.3, P=0.8;
Fb, T=0.7, P=0.5). For changes in wing
beat frequency, there was a change in the duration of wing upstroke, which
significantly decreased as the wing loading increased (one-way ANOVA;
F5,85=7.22, P<0.001). The same was also true
of wing downstroke (one-way ANOVA; F5,85=6.56,
P<0.001; Fig. 7).
Mean wing amplitude in the control birds was 122.5±2.8° and this
value did not change significantly when any of the payload weights were added
(one-way ANOVA; F5,90=0.59, P=0.71;
Fig. 8).
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Discussion |
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Loaded flight cost was lower than predicted from aerodynamic models,
assuming a fixed efficiency, which strongly suggests that the efficiency was
not fixed. The mechanical efficiency measured in unloaded birds was 10.9%
using the Pennycuick model (Pennycuick, 1996) and 9.3% using Rayner's model
(Rayner, 1999), which was
comparable to the efficiency estimates for birds of the same mass from Kvist
et al. (2001
) conducting
long-duration flights in a wind tunnel. In our study efficiency increased to
13.9% and 11.1% with a 20% mass increase (calculated using the Pennycuick and
Rayner models, respectively), which was again comparable to the observed
efficiency change in Kvist et al.
(2001
) for the same mass
change.
Tobalske et al. (2003)
directly measured power curves in cockatiels flying in a wind tunnel over a
range of speeds. The speed at which the minimum power output occurred was 5 m
s1, although the curve was fairly flat between 5 and 8 m
s1, and so the pre-manipulated birds in this study were
flying close to the minimum. When carrying all but the highest payload, flight
speed was reduced and therefore was closer to the minimum power output,
reducing the effect of the payload. Our data contradicts previous studies that
suggest that there is an energetic cost for increased mass loading
(Gessaman and Nagy, 1988
;
Kvist et al., 2001
) although
the Kvist study states that it is much cheaper than expected, but confirmed
the findings of Nudds and Bryant
(2002
) who stated that the
effect of artificially loaded flight was primarily behavioural and not
energetic. The main behavioural response exhibited by the artificially loaded
finches in the Nudds and Bryants
(2002
) study was a reduced
take-off velocity. This impact of loading was also observed in birds
responding to natural fluctuations in body mass. During incubation pied
flycatchers Ficedula hypoleuca had a 7% greater mass and take-off
velocity was reduced by 10%, even although they had a greater flight muscle
index compared to that measured after the chicks had hatched
(Kullberg et al., 2002
).
In the present study we were able to pinpoint other responses to the added
payload mass that contribute to minimising the energetic impact that payloads
have. Similar to the studies by Videler et al.
(1988) and Hughes and Rayner
(1991
), our loaded birds flew
at slower speeds when carrying all but the greatest loads. The previous
studies also found a corresponding increasing trend in wing beat frequency,
which paralleled that observed in our study and became significant at the
highest loading. In contrast to these previous studies, however, wing
amplitude was unaffected in our birds by the increase in loading. When a
payload equal to 20% of body mass was added there was a shift in the
behavioural responses whereby wing beat frequency was at its highest and the
birds flew at a faster speed. It appears that the birds adopted different
strategies depending on the extent of the loading.
Our study shows that even when birds had no opportunity to modify their flight muscles or body composition in response to carrying increased loads they made behavioural responses that elevated their flight muscle efficiency and thus reduced the energetic impact of the payload mass.
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Acknowledgments |
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References |
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