Comparison of the cost of short flights in a nectarivorous and a non-nectarivorous bird
1 Aberdeen Centre for Energy Regulation and Obesity, School of Biological
Sciences, University of Aberdeen, Aberdeen, AB24 2TZ, Scotland, UK
2 Mitrani Department of Desert Ecology, Jacob Blaustein Institute for Desert
Research, Ben Gurion University of the Negev, Sede Boqer Campus, 84990
Midreshet Ben-Gurion, Israel
3 Zoological Laboratory, University of Groningen, PO Box 14, 9750AA Haren,
The Netherlands
4 NERC Molecular Genetics in Ecology Initiative, School of Biological
Sciences, University of Aberdeen, Aberdeen, AB24 2TZ, Scotland, UK
5 The Waltham Centre for Pet Nutrition, Waltham-on-the-Wolds,
Leicestershire, LE14 4RT, England, UK
6 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: energy expenditure, flight cost, labelled bicarbonate technique, Palestine sunbird, Nectarinia osea, starling, Sturnus vulgaris
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Introduction |
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Both metabolic and mechanical approaches to flight energetics have almost
exclusively considered the energy costs of relatively long and steady state
flight, where the animals fly or hover for periods of at least minutes and
often several hours (e.g. Tucker,
1968,
1973
;
Rothe et al., 1987
;
Ward et al., 2001
). Most wild
birds, however, fly for much shorter periods, particularly when foraging. The
energy demands of these short flights are less easily studied because the
behaviour includes a large dynamic component where elevation and speed may be
changing rapidly, and include ballistic phases where the major power is
provided by the legs to generate the initial lift for take-off, rather than
the power being generated by the wings. Aerodynamic modelling of this
situation is consequently more complex than steady state flight mechanics. The
short duration of the behaviour also makes the use of more direct methods of
quantification problematical. Nudds and Bryant
(2000
) measured the energy
demand of short flights in zebra finches and concluded that the costs of this
behaviour might exceed the energy demands of steady state flapping flight by a
factor of three. This enormous discrepancy has obvious serious consequences
when attempting to evaluate the energy costs of such activities in the context
of constructing time and energy budgets for free-living animals. Although
short flights are by definition short in duration, they are performed
frequently and hence their accumulated contribution to the total daily energy
budget may be seriously underestimated if flight times have been uncritically
multiplied by steady state flight costs.
Understanding the factors contributing to the suggested high energy costs of short flights is important because it will allow us to refine our predictions of the energy costs of such activity. Two factors are likely to be of importance in this context. First, when birds fly for short periods they tend to do so at slow speeds. Slow flight is costly because there is little lift generated from the forward movement, thus mechanical costs increase as this lift must be generated by the flapping wings. The second factor is the need to accelerate from standing still to moving at speed in a relatively short time. Different species behave differently during their short-flight behaviour. These differences allow us to explore the factors involved in generating the high-energy demands of short flights. Nectarivorous birds such as hummingbirds and sunbirds often make short flights between flower heads at which they feed. This flight behaviour includes a great deal of slow flight and often periods of hovering. This contrasts with the behaviour of most non-nectarivorous birds that tend to fly more directly between locations and hover little, if at all. Again these differences allow us to explore the relative importance of flight speed versus acceleration costs in the large energy demands of short flight.
We have developed a novel method for measuring the energy cost of flight,
the 13C-labelled bicarbonate technique
(Hambly et al., 2002).
Elimination of 13C-labelled bicarbonate has been used to measure
energy demands of large animals (Young and
Corbett, 1969
; Corbett et al.,
1971
; Benevanga et al., 1992;
Junghans et al., 1997
) and
humans (Irving et al., 1983
;
Armon et al., 1990
;
Elia et al., 1995
), generally
by continuous infusion, which restricts its use to larger species. We have
developed an analogous approach for small species using bolus injection
(Speakman and Thompson, 1997
).
This latter method allows energetic measurements to be made over a much
shorter time scale than with other isotope methods, such as the doubly
labelled water (DLW) technique (e.g.
Gessaman and Nagy, 1988
;
Speakman, 1997
). Elimination
of the 13C label is rapid because CO2 flux is large
relative to the size of the body bicarbonate pool. A calibration on laboratory
mice Mus musculus demonstrated that energy expenditure measurements
on unrestrained animals could be made over periods as short as 15 min using
this technique (Speakman and Thomson,
1997
). An important advantage of the method is that the eliminated
13C can be measured in breath samples, which are much easier to
collect in small birds than the repeated blood samples that are usually
required for the DLW technique.
The 13C-labelled bicarbonate technique was first applied to
birds when the technique was calibrated, and flight costs were measured in
zebra finches Taeniopygia guttata in forward flight
(Hambly et al., 2002). These
flight cost estimates did not differ significantly from allometric predictions
of energy cost compiled from studies using more traditional methods
(Masman and Klaassen, 1987
).
Although promising as a potential method for measuring flight costs, the
method requires further validation. In this study we aimed to assess the value
of this technique for measuring energy expenditure in the Palestine sunbird
Nectarinia osea and starling Sturnus vulgaris, and to
estimate the cost of short flights in these nectarivorous and
non-nectarivorous species.
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Materials and methods |
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Starlings Sturnus vulgaris L. (N=9) were studied at the Zoological Laboratory of the University of Groningen in the Netherlands (53°13'N, 6°35'E; altitude 4 m). The birds were kept individually in one of eight flight cages (5.4 mx0.7 mx0.8 m, lengthxwidthxheight). Water was available ad libitum and the birds were fed fish pellets (Europa Eel, Trouw Nutrition Deutschland, Burgheim, Germany). All birds had previously been trained to fly between two perches at either end of the cage. Both starlings and sunbirds maintained body mass during the study period, and showed no signs of stress or ill health.
13C measurements of energy expenditure
The 13C-labelled bicarbonate technique was used to measure
energy expenditure. In this technique the isotope is injected
intraperitoneally (IP) as NaH13CO3, and the
13C mixes in the bicarbonate pool and is expired as CO2.
The rate of isotope elimination depends on metabolic rate; however, the size
of the bicarbonate pool is small, and therefore the isotope elimination rate
is rapid, allowing energy expenditure to be measured over short periods.
To obtain a standard dilution curve, a fixed volume of 0.2 ml of 0.29 mol
l-1 NaH13CO3 solution was injected, along
with varying volumes (between 5.0 and 0.5 ml) of CO2 gas, into 10
ml vacutainers (Becton Dickinson, Vacutainer Systems Europe, Oxford, UK).
Three replicates were made for each volume of CO2. The vacutainers
were placed in an oven at 60°C for 4 days to equilibrate, after which 0.5
ml of the resulting gas was extracted and injected into a new vacutainer. This
0.5 ml of resulting gas was admitted to an isotope ratio mass spectrometer
(Micromass ISOCHROM µG, Manchester, UK) that uses a gas chromatograph
column to separate nitrogen and CO2 in a stream of helium, before
analysis by isotope ratio mass spectrometry. The enrichment (delta) of
13C:12C was measured as the ratio of the minor to major
beam currents of the samples, compared with a reference gas of known
enrichment (after Lajtha and Michener,
1994), that had previously been characterised relative to the IAEA
(International Atomic Energy Agency) standards 309 a and b.
Calibration
A calibration study was conducted on five individuals of each species to
examine the relationship between the log-converted 13C isotope
elimination rate in breath and both O2 consumption
(O2) and
CO2 production
(
CO2) measured
by indirect calorimetry. The birds were placed in a respirometry chamber with
gas flowing through at a rate of 485 ml min-1 for sunbirds and 1.6
l min-1 for starlings, regulated using a Mass Flow Controller (for
sunbirds, Model 80, McMillan Company, Georgetown, TX, USA; for starlings,
5850S, Brooks, Hatfield, PA, USA). Background 13C enrichment was
measured by collecting gas samples from the outflow of the chamber through a
19 gauge needle directly into 10 ml vacutainers. The birds were then removed
from the chamber and injected intraperitoneally with a weighed volume (to the
nearest 0.0001 g) of approximately 0.1 ml for sunbirds and 0.6 ml for
starlings of 0.29 mol l-1 sodium bicarbonate
(NaH13CO3) and immediately returned to the chamber. Over
the following 60 min,
O2 was measured
using an oxygen analyser (for sunbirds, Applied Electrochemistry Model S-3A,
Naperville, IL, USA; for starlings, Servomex Xentra 4110, Crowborough, UK) and
CO2 was measured
using a CO2 analyser (for sunbirds, OEM Model SBA-1, PP systems,
Hitchin, UK; for starlings, Servomex 1440). Air was dried before and after the
chamber and gas samples were collected from the outflow of the chamber into
vacutainers each minute as previously described. The birds underwent this
procedure on three separate occasions while the chamber was maintained at
different temperatures ranging between 1 and 35°C, to increase the range
of metabolic rates observed. Gas samples were shipped immediately to Aberdeen
University, where they were analysed using isotope ratio mass spectrometry
within 5 days of collection. For each measurement session we determined the
isotope elimination rate (kc), which was the gradient of
the log-converted isotope enrichment with time. Metabolic rate and
kc were initially calculated for all the data after the
isotope had become equilibrated within the bicarbonate pool. We found no
significant relationship between isotope elimination rate and metabolism over
the whole period that the bird was in the chamber, and therefore both
kc and metabolic rates were recalculated over sequential
10 or 15 min intervals to locate the time when the closest relationship
between kc and metabolic rate occurred. This indicated the
optimal time interval over which flight measurements should be taken.
Flight costs
For sunbirds, eight birds were flown (four individuals were flown twice)
for periods of approximately 2 min, commencing 15 min after a 0.1 ml injection
of the same NaH13CO3 solution that was used in the
calibration.
For starlings, flight cost was measured in nine individuals for periods of approximately 10 min, commencing 15 min after a 0.6 ml injection of the same NaH13CO3 solution that was used in the calibration.
Prior to each initial flight the birds were weighed, and their wingspan measured (Table 1). Graph paper was taped to the edge of a table and the bird's body was aligned with the table so that the wing lay flat along the graph paper. The wing was carefully outstretched to the same degree in all birds to maintain a comparable estimate of area across individuals. Total wing area was calculated by counting the enclosed squares on the graph paper and multiplying by 2, 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 isotope injection by briefly placing the bird in the same chamber that was used in the calibration experiment with the same rate of dry airflow. The labelled isotope solution (±0.0001 g) was then injected IP and the bird was immediately returned to the chamber. Based on times indicated by the calibration experiment, breath samples were collected each minute from 10 to 14 min after injection in the sunbirds, and between 1 and 14 min after injection in the starlings, to obtain resting isotope elimination values. 15 min after injection, the bird was removed from the chamber and placed in the flight cage (6 m for sunbirds and 5 m for starlings) where it was encouraged to fly back and forth between perches by approaching the bird after it had landed. The sunbirds' flight cage had natural light, while the starlings flew under artificial lights. However, the birds were acclimated to these flight environments and would not have suffered from stress-induced elevation of their metabolic rates during flight. The majority of birds, once trained, landed repeatedly on the perches, although on a few occasion starlings would land and take off from the floor. The flight was carefully filmed on videotape using a Panasonic AG-455MB VHS video camera and subsequently timed to the nearest second. After flight, the bird was recaptured as quickly as possible and then placed back in the chamber, where breath samples were collected for 5 min in sunbirds and 10 min in starlings. Each starling underwent two or three separate flight measurements while the sunbirds were flown on either one or two occasions.
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Comparison between different types of flight
We examined the relationships between flight costs for different types of
flight in nectarivorous and non-nectarivorous birds using the data generated
here and additional data from the literature. Simple comparisons of this type
are confused, individual species not being independent because of their shared
evolutionary history. We therefore determined the relationship between body
mass and flight cost in the absence of any phylogenetic bias using the
independent comparison method of Felsenstein
(1985), with independent
contrasts identified using CAIC software
(Purvis and Rambaut, 1995
).
The relationship between flight cost and body mass was then tested by
correlating the standardised linear contrasts for the two variables, using
regression through the origin. The phylogeny was derived from Sibley and
Ahlquist (1990
), and assumed
equal rates of evolutionary change per unit branch length in all branches.
Data analysis
Values are means ± standard error (S.E.M.) unless
otherwise stated. Minitab (versions 11 and 13) and SPSS statistical software
were used for data analysis. Non-linear regression, linear least-squares
regression, t-tests and one-way analysis of variance (ANOVA) were
applied to our data. For statistical comparisons we chose P=0.05 as
the minimum acceptable level of significance.
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Results |
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In sunbirds the
O2 varied
between 0.33 and 1.48 ml O2 min-1 and
CO2 varied
between 0.38 and 1.35 ml CO2 min-1 over the measured
temperature range. The respiratory quotient (RQ) at thermoneutral for resting
sunbirds averaged 1.14±0.06 (N=5). A RQ higher than 1 suggests
that the birds were synthesizing fat from their high carbohydrate diet. In
starlings
O2
ranged from 3.5 to 6.4 ml min-1 while
CO2 ranged from
2.4 to 4.7 ml min-1. The average respiratory quotient at
thermoneutral in these five individuals was 0.70±0.003, indicating that
these individuals were predominantly burning fats.
A least-squares linear regression equation was calculated for the
logarithms of the isotope enrichment values measured following injection and
after the plateau had been reached, for different 10 min time intervals (i.e.
1020 min, 2030 min3040 min etc). The isotope elimination
rate (kc, min-1) was calculated from the slope
of the regression in any particular time interval. kc was
plotted against both
O2 and
CO2 over the
same time interval and such plots were accumulated for different intervals
spanning the whole measurement period. This procedure allowed us to examine
the relationship between the isotope elimination rate and metabolism, and to
identify the most suitable post-injection time interval for subsequent flight
cost measurements. In sunbirds, the closest relationship between
kc and
O2, and between
kc and
CO2, occurred
for the time interval 1020 min after injection (regression;
O2,
F1,13=37.5, P<0.001;
CO2,
F1,13=47.7, P<0.001)
(Fig. 2A). Individual bird was
not a significant factor in the relationship (one-way ANOVA;
O2,
F4,13=1.61, P=0.25;
CO2,
F4,13=2.12, P=0.16).
|
For starlings, we found no significant relationships between
O2,
CO2 and
kc over any of the 10 min time intervals post injection.
Isotope elimination rate (kc) was multiplied by body
bicarbonate pool size (Nc), after conversion of the latter
from mole to ml using the gas constant
(Fig. 3) and the width of each
time interval was extended to 15 min.
kcNc increased linearly with
increasing metabolic rate, and the interval 1530 min after injection
provided the closest relationship for both
O2 and
CO2
(Fig. 2B). Both of these
relationships were highly significant (regression:
O2,
F1,13=62.7, P<0.001;
CO2,
F1,13=67.1, P<0.001). We used them to estimate
O2 and
CO2 during
flight given a known kcNc. Individual
bird was not a significant factor in this analysis (one-way ANOVA;
O2,
F4,13=1.92, P=0.19;
CO2,
F4,13=2.75, P=0.10).
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Flight costs
As observed in our previous study using the labelled bicarbonate technique
(Hambly et al., 2002), the
relationship between time after the plateau and isotope enrichment during the
period before flight conformed to a linear regression. After flight, the
relationship between isotope enrichment and time was not linear
(Fig. 4). In all cases, the
best-fit relationship between the isotope enrichment and time after flight was
expressed by a second-order polynomial regression.
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To account for the time spent resting during the flight period, we measured
the total duration of rest and flight activity. To simplify analysis, we then
treated the data as if all flight activity had taken place in the middle of
the flight phase and was preceded and succeeded by periods of rest of equal
duration (Hambly et al.,
2002). In a previous sensitivity analysis we found the error in
flight cost prediction associated with selecting the middle, compared to the
beginning or end periods, averaged 8% in zebra finches
(Hambly et al., 2002
). The
regression equations in the flight experiments were forward and back
extrapolated to the time when the flight started and ended, thus accounting
for the time spent on the perches. The gradient between these two extrapolated
points, calculated for the beginning and end of flight, was the isotope
elimination rate (kc) during the flight period. In
addition Nc was calculated for each flight in starlings
using the enrichment at the plateau and interpolating it onto the regression
equation in Fig. 3.
O2 and
CO2 were
calculated for the flight period by interpolating kc for
sunbirds or kcNc for starlings onto
the corresponding calibration equations
(Fig. 2), and these values were
converted to energy expenditure in W using the RQ for each flight. In
sunbirds, average
O2 was
5.06±0.50 ml O2 min-1 and average
CO2 was
4.25±0.41 ml CO2 min-1; in starlings,
O2 was
61.48±2.32 ml min-1 and
CO2 was
47.36±1.80 ml min-1
(Table 2). The resulting
average flight cost was 1.64±0.32 W in sunbirds using an RQ of 0.85,
and 20.55±0.78 W instarlings using an RQ of 0.77, where the RQ values
were derived from the estimates of
O2 and
CO2 during
flight. This was equivalent to 12.5 times the BMR estimate for sunbirds (based
on the allometric equation in Reynolds and
Lee, 1996
) or 8.6 times the measured resting metabolic rate (RMR)
and 25.3 times the BMR in starlings (measured in control birds by
Bautista et al., 1998
) or 16.8
times the measured RMR.
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Comparison between different types of flight in nectarivorous and non-nectarivorous birds
Flight cost estimates were collected from the literature for an additional
8 nectarivorous and 12 non-nectarivorous species
(Table 3). The flights were
separated into one of four distinct types, hovering and mixed (hovering and
forward) flights for the nectarivores and slow or fast flight for the
non-nectarivores (Fig. 5). Data
were normalized by log-conversion. There was a significant effect of body mass
on flight cost (F1,22=66.25, P<0.001,
gradient=0.785). Using generalised linear modelling there was no significant
interaction between flight type and body mass (interaction;
F1,22=0.57, P>0.05) but there was a
significant group effect (F1,22=0.08, P>0.05).
Analysis of the residuals using one-way ANOVA and tukey tests indicated that
the costs of slow flight in non-nectarivores significantly
(P<0.05) exceeded the costs of fast forward flight in
non-nectarivores and the mixed flight of nectarivores, but were not
significantly elevated (P>0.05) relative to the costs of hovering
in nectarivores.
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The above analysis is potentially compromised by the lack of phylogenetic
independence in the data. To overcome this problem we established the
phylogenetic inter-relationships of the species for which we had flight cost
data and where DNA:DNA hybridisation distances could be determined (all
species except Stellula calliopte)
(Fig. 6A), and used the nodal
estimates of independent and dependent variables derived from the CAIC
(Purvis and Rambaut, 1995)
program to construct the expected relation between body mass and flight cost
in the absence of any group effects. We then calculated the difference between
these predictions and the actual flight costs. The effect of mass disappears
in this analysis because it is used to reconstruct the expected
phylogenetically independent flight cost. In this analysis there was still a
significant group effect in the data (Fig.
6B) and Tukey tests confirmed that the costs of slow flight in the
non-nectarivores significantly (P<0.05) exceeded the costs of fast
forward flight of the non-nectarivores and mixed flight of the nectarivores,
but did not differ significantly (P>0.05) from the costs of
hovering in the nectarivores.
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Discussion |
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The cost of short flight in starlings, however, was significantly higher
than predicted values from all of the allometric equations
(Table 4: t-test for
all equations T>8.48, P<0.001). Although this is the
first study to measure the flight cost of Palestine sunbirds, several previous
studies have addressed the energy demands specifically of starlings, providing
more direct comparisons to the estimates derived here. The starlings in the
present study had elevated flight costs compared to previous measurements of
forward flight for the same species. Forward flight in starlings has been
estimated to cost between 7.8 and 9.6 W using thermal imaging techniques and
between 10.4 and 14.9 W using respirometry in the same bird flying with a mask
at constant speed in a wind tunnel (Ward
et al., 2001). In a separate study using wind tunnel respirometry,
the average flight cost was estimated at 8.9 W
(Torre-Bueno and La Rochelle,
1978
). These wind-tunnel measurements, however, do not include the
many aerial behaviours associated with free flight.
The cost of flight over short distances in starlings has also been measured
previously using a very similar flight cage to the one we used, but with a
slightly shorter distance between the perches
(Bautista et al., 1998).
Bautista et al. (1998
) examined
how starlings coped with changes of food availability. There were two
treatments, one of which gave food rewards after fewer flights between perches
than the other (hard and easy treatments). DLW and BMR measurements were used
to estimate daily and resting energy expenditure, respectively, which in turn
were used to predict the flight costs. The cost of flight was estimated to be
52.3 and 45.5 W in the easy and hard treatments, respectively, approximating
68.5 and 92.3x BMR. These values are over double the values measured in
our study. Westerterp and Drent
(1985
) also measured energy
expenditure in starlings conducting short flights using DLW, from which they
predicted a flight cost of approximately 34 W (equivalent to 42x BMR).
The most probable reason for these very high estimates of flight cost when
using DLW relative to the previous wind tunnel work is the extent of
extrapolation. The birds in these studies 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 have been
shown previously to introduce enormous error into the derived estimates
(Speakman and Racey, 1991
).
These extrapolation errors are eliminated when using the labelled bicarbonate
method, and we therefore feel that our estimate of 20.55 W is a more realistic
estimate of the energy demands of short flights in these birds.
Nudds and Bryant (2000)
used data from different species of birds, which had been measured during
short flights, to generate an allometric equation to predict the cost of short
flights from body mass. Using this equation the starlings in this study,
average body mass 70.11 g, had an estimated average short flight cost of
24.5±0.22 W, which was closer to our measurement but still
significantly higher than the our measured average flight cost 20.6 W (paired
t-test of individual observed and predicted values; T=5.8,
P<0.001). Our starling flight costs were therefore about 80% of
those estimated by Nudds and Bryant
(2000
). The sunbirds we
studied also had significantly lower flight cost than estimated using the
Nudds and Bryant equation, which gives a flight cost of 2.9±0.06 W for
a bird of this size, compared with the actual measurement of 1.64 W (paired
t-test; T=3.8, P=0.006). The discrepancy for
sunbirds was consequently much greater than for starlings, with sunbirds
flying at only 60% of the expected `short-flight' cost.
By comparing our results with those of previous direct measures for steady
state flight (starlings) and allometric estimates for both steady state and
short flights (both species), the consistent pattern that emerges is that
short flights in sunbirds are relatively much cheaper than short flights in
starlings. During their short flights, sunbirds generally drop downwards from
flowers where they are feeding, often hovering intermittently, before
relanding (C. Hambly, personal observation). In contrast starlings jump
upwards and accelerate rapidly towards their `optimum' flight speed, and then
decelerate rapidly before landing (Bonser
and Rayner, 1996). The comparative flight energy demands of these
two species indicate that these accelerations and decelerations increase the
energy demands of flight substantially above the controlled steady flight
expectations. In contrast, the flights of sunbirds, which do not include the
same level of acceleration and deceleration costs, are not significantly
enhanced at all above what is expected during controlled steady flight. Given,
however, that the sunbirds flew at slow speeds and often hovered, this lack of
elevation of costs relative to steady state flight in a wind tunnel was
unexpected. Moreover, this observation was supported by our review of previous
flight cost estimates in nectarivore and non-nectarivorous species. The
unexpected nature of this result is because all of the aerodynamic models
predict that costs should increase significantly at such slow speeds. Previous
energetic measurements for hovering animals have also reported that hovering
costs are lower than anticipated by the aerodynamic models
(Ellington, 1991
), and that
rather than conforming to a U-shaped curve (power against speed), direct
measures indicate that a J shape is perhaps more appropriate. Our data
partially support this interpretation because the costs of mixed flight in
nectarivores, which have bouts of both hovering and forward flight, were not
elevated much above the costs of fast forward fight of non-nectarivores.
However, the costs of pure hovering flight in nectarivores were still elevated
(Fig. 6B).
The practical consequence of these observations is that the suggested elevation of energy demands during short flights (lasting several seconds), as compared with long, steady state flights (lasting minutes and hours), appears to depend critically on the exact nature of the short flights being performed. This conclusion is supported by a much wider comparison of the costs of flight of nectarivore and non-nectarivore species. Our data suggest that it is the acceleration and deceleration to and from perching that causes these elevated costs and, hence, birds performing short flights that do not include such changes, particularly birds that hover, may not experience such high costs. These possibilities should be kept in mind when choosing an appropriate equation for estimating energy demands for inclusion in time budgets.
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Acknowledgments |
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References |
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---|
Armon, Y., Cooper, D. M., Springer, C., Barstow, T. J., Rahimizadeh, H., Landaw, E. and Epstein, S. (1990). Oral [13C] bicarbonate measurement of CO2 stores and dynamics in children and adults. Am. Physiol. Soc. 161,1754 -1760.
Bautista, L. M., Tinbergen, J., Wiersma, P. and Kacelnik, A. (1998). Optimal foraging and beyond: how starlings cope with changes in food availability. Am. Nat. 152,543 -561.[CrossRef]
Benevenga, N. J., Odle, J. and Asche, G. L. (1992). Comparison of measured carbon dioxide production with that obtained by the isotope dilution technique in neonatal pigs: Observations on site of infusion. Am. Inst. Nutr. 122,2174 -2182.
Berger, M. and Hart, J. S. (1974). Physiology and energetics of flight. In Avian Biology, vol.4 (ed. D. S. Farner and J. R. King), pp.415 -477. New York and London: Academic Press.
Bonser, R. H. and Rayner, J. M. V. (1996).
Measuring leg thrust forces in the common starling. J. Exp.
Biol. 199,435
-439.
Butler, P. J. and Bishop, C. M. (1999). Flight. In Sturkie's Avian Physiology (ed. G. C. Whittow), pp.391 -435.
Carlson, A. and Moreno, J. (1992). Cost of short flights in the willow tit measured by doubly labelled water. Auk 109,389 -393.
Collins, B. G. and Briffa, P. (1983a). Seasonal variations in the energetics of an Australian nectarivorous bird, Lichmera indistincta. Comp. Biochem. Physiol. 74A,731 -738.[CrossRef]
Collins, B. G. and Briffa, P. (1983b). Seasonal and diurnal variations in the energetics and foraging activities of the brown honeyeater, Lichmera indistincta. Aust. J. Ecol. 8, 103-111.
Collins, B. G. and Morellini, P. C. (1979). The influence of nectar concentration and time of day upon energy intake and expenditure by the Singing Honeyeater, Meliphaga virescens.Physiol. Zool. 52,165 -175.
Corbett, J. L., Farrell, D. J., Leng, R. A., McClymont, G. L. and Young, B. A. (1971). Determination of the energy expenditure of penned and grazing sheep from estimates of carbon dioxide entry rates. Br. J. Nutr. 26,277 -291.[Medline]
Dol'nik, V. R. and Gavrilov, V. M. (1971). Energy metabolism during flight of some passerines. In Bird Migrations: Ecological and Physiological Factors (ed. B. E. Bykhovskii), pp. 288-296. New York: Halsted Press.
Elia, M., Jones, M. G., Jennings, G., Poppit, S. D., Fuller, N. J., Murgatroyd, P. R. and Jebb, S. A. (1995). Estimating energy expenditure from specific activity of urine urea during lengthy subcutaneous NaH14CO3 infusion. Am. Physiol. Soc. 193,E174 -E182.
Ellington, C. P. (1991). Limitations on animal flight performance. J. Exp. Biol. 160, 71-91.
Felsenstein, J. (1985). Phylogenies and the comparative method. Am. Nat. 125, 1-15.[CrossRef]
Flint, E. N. and Nagy, K. A. (1984). Flight energetics of free-living sooty terns. Auk 101,288 -294.
Gessaman, J. A. and Nagy, K. A. (1988). Transmitter loads affect the flight speed and metabolism of homing pigeons. Condor 190,662 -668.
Hainsworth, F. R. and Wolf, L. L. (1969). Resting, torpid and flight metabolism of the hummingbird Eulampis jugularis. Amer. Zool. 9,1100 -1101.
Hambly, C., Harper, E. J. and Speakman, J. R. (2002). Cost of flight in the zebra finch (Taenopygia guttata): a novel approach based on elimination of 13C labelled bicarbonate. J. Comp. Physiol. 172,529 -539.[CrossRef]
Hussell, D. J. T. (1969). Weight loss in birds during nocturnal migration. Auk 86, 75-83.
Irving, C. S., Wong, W. W., Shulman, R. J., O'Brian-Smith, E. and Klein, P. D. (1983). [13C] bicarbonate kinetics in humans: Intra- vs. interindividual variations. Am. Physiol. Soc. 363,R190 -R202.
Junghans, P., Derno, M., Gehre, M., Hofling, R., Kowski, P., Strauch, G., Jentsch, W., Voigt, J. and Hennig, U. (1997). Calorimetric validation of 13C bicarbonate and doubly labelled water method for determining the energy expenditure in goats. Z. Ernahrungswiss. 36,268 -272.[Medline]
Lajtha, K. and Michener, R. (1994). Stable Isotopes in Ecology and Environmental Science. Methods in Ecology Series. Oxford: Blackwell Science.
Lasiewski, R. C. (1963). Oxygen consumption of torpid, resting, active and flying hummingbirds. Physiol. Zool. 36,122 -140.
Masman, D. and Klaassen, M. (1987). Energy expenditure during free flight in trained and free-living Eurasian kestrels (Falco tinnunculus). Auk 104,603 -616.
Norberg, U. M. (1996). Energetics of flight. In Avian Energetic and Nutritional Ecology (ed. C Carey), pp. 199-249. New York: Chapman and Hall.
Nudds, R. L. and Bryant, D. M. (2000). The
energetic cost of short flights in birds. J. Exp.
Biol. 203,1561
-1572.
Pearson, O. P. (1950). The metabolism of hummingbirds. Condor 52,145 -152.
Pennycuick, C. J. (1968). Power requirements for horizontal flight in the pigeon Colomba livia. J. Exp. Biol. 49,527 -555.
Pennycuick, C. J. (1969). The mechanics of bird migration. Ibis 111,525 -556.
Pennycuick, C. J. (1975). Mechanics of flight. In Avian Biology (ed. D. S. Farner and J. R. King), pp. 1-75. New York: Academic Press.
Purvis, A. and Rambaut, A. (1995). Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Comp. Appl. Biosci. 11,247 -251.[Medline]
Rayner, J. M. V. (1990). The mechanics of flight and bird migration performance. In Bird Migration (ed. E. Gwinner), pp. 283-299. Heidelberg: Springer-Verlag.
Reynolds, P. S. and Lee, R. M., III (1996). Phylogenetic analysis of avian energetics: passerines and non passerines do not differ. Amer. Nat. 147,735 -759.[CrossRef]
Rothe, H. J., Biesel, W. and Nachtigall, W. (1987). Pigeon flight in a wind tunnel. II Gas exchange and power requirements. J. Comp. Physiol. B 157,99 -109.
Schmidt-Nielsen, K. (1984). Scaling: Why is Animal Size So Important? Cambridge: Cambridge University Press.
Sibley, C. G. and Ahlquist, J. E. (1990). Phylogeny and Classification of Birds A Study in Molecular Evolution. New Haven: Yale University Press.
Speakman, J. R. (1997). Doubly Labelled Water: Theory and Practice, pp.186 -193. Chapman and Hall.
Speakman, J. R. and Racey, P. A. (1991). No cost of echolocation for bats in flight. Nature 350,421 -423.[CrossRef][Medline]
Speakman, J. R. and Thompson, S. C. (1997). Validation of the labelled bicarbonate technique for measurement of short-term energy expenditure in the mouse. Z.. Ernahrungswiss. 36,273 -277.[Medline]
Tatner, P. and Bryant, D. M. (1986). Flight cost of small passerine measured using doubly labelled water: implications for energetic studies. Auk 103,169 -180.
Torre-Bueno, J. R. and LaRochelle, J. (1978). The metabolic cost of flight in unrestrained birds. J. Exp. Biol. 75,223 -229.[Abstract]
Tucker, V. A. (1968). Respiratory exchange and evaporative water loss in the flying budgerigar. J. Exp. Biol. 48,67 -87.
Tucker, V. A. (1973). Bird metabolism during flight: evaluation and theory. J. Exp. Biol. 58,689 -709.
Utter, J. M. and LeFebvre, E. A. (1970). Energy expenditure for free flight by the Purple Martin (Progne subis). Comp. Biochem. Physiol. 35,713 -719.[CrossRef]
Ward, S., Moller, U., Rayner, J. M. V., Jackson, D. M., Bilo,
D., Nachtigall, W. and Speakman, J. R. (2001). Metabolic
power mechanical power and efficiency during wind tunnel flight by European
starlings Sturnus vulgaris. J. Exp. Biol.
204,3311
-3322.
Ward, S., Rayner, J. M. V., Moller, U., Jackson, D. M., Nachtigall, W. and Speakman, J. R. (1999). Heat transfer from starlings Sturnus vulgaris during flight. J. Exp. Biol. 202,1589 -1602.[Abstract]
Westerterp, W. W. and Drent, R. (1985). Energetic cost and energy-saving mechanisms in parental care of free-living passerine birds as determined by the D218O method. Acta XVII Congr. Int. Orn. 1, 392-403.
Westerterp, K. R. and Bryant, D. M. (1984). Energetics of free existence in swallows and martins (Hirundinae) during breeding: a comparative study using doubly labelled water. Oecologia 62,376 -381.
Wolf, L. L., Hainsworth, F. R. and Gill, F. B. (1975). Foraging efficiencies and time budgets in nectar feeding birds. Ecology 56,117 -128.
Young, B. A. and Corbett, J. L. (1969). Energy requirement for maintenance of grazing sheep measured by calorimetric techniques. Proc. Aust. Soc. Anim. Prod. 7, 327-334.