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First published online October 7, 2004
Journal of Experimental Biology 207, 3969-3976 (2004)
Published by The Company of Biologists 2004
doi: 10.1242/jeb.01234

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The energy cost of loaded flight is substantially lower than expected due to alterations in flight kinematics

C. Hambly^1,*, E. J. Harper² and J. R. Speakman^1,3

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

View larger version (15K): [in a new window]   Fig. 1. The time after injection that the peak or plateau of isotope enrichment (delta) occurs varies with different individuals. The longer the isotope was within the body before the peak was reached, the lower the isotope enrichment value. This relationship was significant (regression; y=4746.3–188.36x, r2=0.4, F1,95=65.10, P<0.001).

View larger version (16K): [in a new window]   Fig. 2. The calibration if the 13C-labelled bicarbonate technique in cockatiels 20–30 min after injection. (A) There was no significant relationship if isotope elimination rate (kc) alone is used for the comparison with the metabolism (O2) measured simultaneously by indirect calorimetry (regression; y=10.6x+3.8, r2=0.11, F1,20=2.35, P=0.14) with a low r2 of 10.99%. (B) The relationship of oxygen consumption to the product of elimination rate and bicarbonate pool size was significant (regression; y=5.12x+0.3, r2=0.72, F1,20=49.54, P<0.001) with a high r2 of 72.3%.

View larger version (9K): [in a new window]   Fig. 3. Relationship between the equilibrium of 13C-labelled bicarbonate with varying amounts of CO2. The enrichment values have been log-converted and plotted against the log-converted volume of CO2 added in moles. The relationship was linear and significant (Regression; y=0.72–1.25x, F1,31=7367.5, P<0.001). The equation for the relationship was used to calculate the size of the body bicarbonate pool (Nc) in moles and subsequently ml of CO2 given a known isotope enrichment for each bird. See text for details.

View larger version (13K): [in a new window]   Fig. 4. Raw isotope enrichment data from one individual, which was used to calculate its flight cost. Before flight (diamonds) the isotope enrichment data conforms to a linear regression, while after flight (squares) a polynomial regression provided the best fit. The regression equations were extrapolated to the time when flight began and ended and the gradient between these two values is the isotope elimination rate during the flight period. In this example kc was 0.73 min–1.

View larger version (11K): [in a new window]   Fig. 5. Mean flight cost increases linearly with increased wing loading (diamonds); however, there were large variations in flight cost between flights in the same and different individuals and therefore the increase was not significant (GLM; F4,65=0.11, P=0.98). The relationship for the mean flight cost was described by y=0.43x+16.63, r2=0.93. Adding a 10% body mass ventrally (square) had a lower flight cost than adding the same mass dorsally, but this was not significant (paired t-test; T=0.4, P=0.7).

View larger version (17K): [in a new window]   Fig. 6. Changes in (A) flight speed and (B) wing beat frequency (Fb) with increasing body mass due to the artificially added mass. *Significant difference from the same parameter in the pre-manipulated birds (Pre). Values are means ± S.E.M. (N=70 flights across 5 individuals).

View larger version (18K): [in a new window]   Fig. 7. Mean up- (A) and downstroke (B) duration in relation to added payload mass. Upstroke duration was always significantly higher than downstroke duration (asterisks; P<0.05). When masses were added, both wing upstroke and wing downstroke significantly decreased as wing loading increased (one-way ANOVA; upstroke F5,85=7.22, P<0.001; downstroke F5,85=6.56, P<0.001). Values are means ± S.E.M. (N=70 flights across 5 individuals). Control, pre-manipulation.

View larger version (13K): [in a new window]   Fig. 8. Mean wing amplitude in relation to payload mass added. There were no significant differences with increasing weight added, compared to the controls (pre-manipulation). Values are means ± S.E.M. (N=70 flights across 5 individuals).

View larger version (18K): [in a new window]   Fig. 9. Neither the Pennycuick (one-way ANOVA; F4,24=2.58, P=0.07) nor Rayner (one-way ANOVA; F4,24=1.60, P=0.21) aerodynamic models predicted a significant increase in flight cost with increasing extent of wing loading when calculated using all the measured parameters for these birds. Values are means ± S.E.M. Control, pre-manipulation.