Heart rate and the rate of oxygen consumption of flying and walking barnacle geese (Branta leucopsis) and bar-headed geese (Anser indicus)
1 School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15
2TT, UK
2 School of Biological Sciences, University of Wales Bangor, Bangor,
Gwynedd LL57 2UW, UK
* Present address: School of Biology, Bute Medical Buildings, University of St
Andrews, St Andrews, Fife KY16 9TS, UK
(e-mail: sw29{at}st-andrews.ac.uk)
Accepted 15 July 2002
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Summary |
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Key words: flight, exercise, heart rate, oxygen consumption, bird, goose, metabolic power, Branta leucopsis, Anser indicus, migration
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Introduction |
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There are several approaches to the calculation of the energy expenditure
of free-flying migratory birds. Average data for a population can be obtained
from the difference in body mass before and after migratory flights, although
the difficulty in catching birds immediately before departure and after
arrival (Nisbet et al., 1963;
Butler et al., 1998
;
Battley et al., 2000
) and in
interpretation of mass loss data in terms of energy consumption
(Kvist et al., 1998
) means
that these estimates may be inaccurate. The doubly labelled water (DLW)
technique (Lifson and McClintock,
1966
; Speakman,
1997
) would, in theory, allow the measurement of the cost of
migratory flight by individual birds, but this approach is impractical because
of the difficulty in capturing an individual bird at the appropriate times.
The DLW technique can be used to measure metabolic rate during simulated
migratory flights in a wind tunnel
(Lindström et al., 1999
;
Klaassen et al., 2000
;
Kvist et al., 2001
) or during
free flight in homing pigeons (LeFebvre,
1964
; Gessaman and Nagy,
1988
). Energy expenditure during flight can be estimated for a
given bird mass from an allometric relationship with the rate of oxygen
consumption for birds flying in wind tunnels wearing masks from which expired
gases are collected (e.g. Butler and
Bishop, 2000
). However, this approach cannot currently take into
account morphological variation among species because of the relatively small
number of species that have been trained to fly in wind tunnels.
Flight costs can also be predicted from aerodynamic models, particularly
that described by Pennycuick
(1989). This approach has the
advantage that the effects upon the mechanical power for flight of variation
in mass, flight speed, wing morphology and altitude can be calculated (e.g.
Lindström and Alerstam,
1992
; Klaassen,
1995
,
1996
; Hedenström and
Alerstam, 1995
,
1997
;
Pennycuick, 1998
). However,
aerodynamic models have the disadvantage that they predict mechanical power,
which represents only 10-23% of total metabolic power. Because the efficiency
of the flight muscles is not well known
(Kvist et al., 2001
;
Ward et al., 2001
), it is
currently difficult to make accurate predictions of metabolic flight costs
from aerodynamic models. One of the predictions of most aerodynamic models is
that flight costs should form a U-shaped curve with respect to flight speed
(Rayner, 1979
;
Pennycuick, 1989
), so
examining the shape of the powerspeed curve is one way of testing the
accuracy of the predictions of aerodynamic models (e.g.
Dial et al., 1997
;
Rayner and Ward, 1999
;
Kvist et al., 2001
;
Ward et al., 2001
). The form
of the metabolic powerspeed curve has not previously been examined in
relatively large birds such as geese.
Data on heart rate (fH) have been collected from free-living
barnacle geese (Branta leucopsis) during natural migration
(Butler et al., 1998) and from
captive-bred birds trained to fly behind a truck
(Butler and Woakes, 1980
).
Although there is significant variation in fH during migratory
flights, there was no change in fH, respiratory frequency or wingbeat
frequency over a wide range of airspeed in the geese flying behind the truck.
This raises the possibility that power input (determined by measuring the rate
of oxygen consumption,
O2) may also be
constant over a range of flight speeds in these birds. A preliminary study of
barnacle geese (1.7 kg body mass) flying in front of a wind generator
succeeded in measuring mean fH and mean
O2 of 2-3 birds
flying at a single speed (13 m s-1), demonstrating the feasibility
of training this species to fly in a suitably large wind tunnel
(Butler et al., 2000
). The
relationship between
O2 and
fH has previously been established for walking barnacle geese
(Nolet et al., 1992
), but this
relationship does not predict realistic values of
O2 from
measurements of fH made during natural migratory flights
(Butler et al., 1998
). To
determine whether the relationship between
O2 and
fH differs between walking and flying, or between captive and wild
geese (or both), we measured the fH and
O2 of barnacle
geese during walking on a treadmill and flight in a wind tunnel. We also
studied bar-headed geese (Anser indicus) because the ability of this
species to fly at high altitude during migration (up to 9 km, where the
partial pressure of oxygen is 30% of that at sea level;
Swan, 1961
) and its different
form of haemoglobin (Rollema and Bauer,
1979
; Perutz,
1983
) suggest that this species may have an unusual flight
physiology. These are the first data of which we are aware on the detailed
relationship between fH and
O2 during flight
for any animal.
The aims of the present study were to measure fH and
O2 during
walking and flying in two species of goose, to calibrate the relationship
between fH and
O2 during these
two forms of exercise and to test the hypotheses (i) that the relationship
between fH and
O2 differs
between flying and walking (Nolet et al.,
1992
; Butler et al.,
2000
) and (ii) that fH and
O2 show U-shaped
relationships with flight speed that reflect the changes in mechanical power
predicted from most aerodynamic theories
(Rayner, 1979
;
Pennycuick, 1989
).
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Materials and methods |
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The geese were flown in the wind tunnel during times that approximated to
the migratory periods of their wild conspecifics in the autumn (in September
and October, when the barnacle geese were 12-20 weeks old and the bar-headed
geese were 14-22 weeks old) and in the following spring (in April and May,
when the birds were 9-10 months old). We measured fH and
O2 during
flights by both species in autumn and fH during flights by barnacle
geese in spring. The geese were lifted into the air stream by the trainer at
the start of each flight in the wind tunnel. Initially, the trainer had to
stand in the flight section to stop the goslings from landing, but during
flights in the spring it was possible to do this while standing out of the air
stream at the side of the flight section. The position in which the goose flew
relative to the trainer was categorised as position A (with the tail of the
bird at least 1 m upwind of the trainer), position B (with the tail less than
1 m upwind of the trainer) or position C (with the trainer standing out of the
air stream). Each bird was flown over as wide a range of sustainable flight
speeds as was possible (14-20 m s-1 for barnacle geese and 16-21 m
s-1 for bar-headed geese). The range of flight speed of barnacle
geese in the wind tunnel was similar to that recorded during natural migratory
flight by barnacle geese (M. Green, personal communciation). We measured the
O2 of four
barnacle geese (mean mass 1.98±0.10 kg) and two bar-headed geese (mean
mass 2.66±0.15 kg) and the fH of six barnacle geese (mean mass
2.07±0.10 kg) and two bar-headed geese (mean mass 2.56±0.20 kg)
during flight in the wind tunnel.
Five barnacle geese (mean mass 1.99±0.12 kg) and five bar-headed geese (mean mass 2.75±0.09 kg) (including the individuals that were flown in the wind tunnel) were trained to walk on a treadmill enclosed in a respirometry chamber. The treadmill experiments were conducted when the birds were 7-8 months old. All procedures followed Home Office guidelines for the use of animals in experiments in the UK.
Heart rate
We recorded fH using custom-built loggers implanted into the
abdomen (which logged the mean fH over 30 s intervals in barnacle
geese and over 10 s intervals in bar-headed geese) or radio transmitters
(which transmitted the electrocardiogram from two subcutaneous electrodes)
taped to feathers on the back of the bird
(Woakes et al., 1995). The
procedure for abdominal implantation of heart rate loggers followed that used
by Stephenson et al.
(1986
).
Walking and resting respirometry
Measurements of gas exchange during walking were made by placing the goose
inside a Perspex box (74 cm high x 58 cm long x 47 cm wide) that
rested on a wooden frame on a variable-speed treadmill (Powerjog, Sports
Engineering Ltd). The air in the chamber was mixed by three fans in a side
compartment. Brush-style draught excluders minimised air leaks between the
wooden frame and the treadmill belt. The flow rate that we used should replace
95% of the air in the chamber in 12 min. Data from the training sessions
confirmed that stable levels of gas exchange were reached after 10-13 min of
walking at each speed. Mean fH and gas exchange data from the final 5
min of the 18 min spent walking at each speed (i.e. after 13 min of walking at
that speed) were taken to be representative of that walking speed. The geese
walked in the treadmill respirometer at 8-12 speeds at approximately 0.07 m
s-1 increments between 0.07 and 0.92 m s-1. Only one
bird would walk at the full range of speeds. The order of the speeds at which
each bird walked was determined randomly.
The extent to which the treadmill respirometer leaked when the belt was
moving was determined by supplying oxygen-free dry nitrogen gas (BOC) into the
chamber at 11 min-1 (measured to ±0.0051 min-1
with a 1.21 min-1 KDG 1100 rotameter) while air was pumped through
the chamber at a rate similar to that used during the experiments with the
geese (Fedak et al., 1981).
The calculated values of gas exchange were adjusted to compensate for the loss
of chamber gas.
Measurements of fH and the rates of gas exchange from resting
birds were made overnight in the treadmill respirometer. Chamber air
temperature was 19-21°C, within the thermoneutral zone for geese
(Calder and King, 1974).
Resting rates of gas exchange and fH were calculated from the lowest
values when averaged over 5 min.
Mask respirometry
Flying birds were fitted with a mask made from vacuum-formed polyurethane
(of mass 4.4 g for barnacle geese and 8.1 g for bar-headed geese) that covered
the beak and forehead, but not the eyes, of the bird. The mask was attached by
an elastic or lightweight leather strap round the back of the head that passed
just below the base of the skull. Air was extracted from above the nostrils
through a polyurethane tube (internal diameter 6.5 mm, external diameter 9 mm;
46 g m-1) that ran over the back of the bird from the top of the
head. The mask had four round holes (each 1.5 mm in diameter) at the front and
an oval hole (10 mmx5 mm for barnacle geese and 15 mmx8 mm for
bar-headed geese) underneath to allow air to enter. The trainer supported the
tube 1-1.5 m from the head of the bird during flight to counteract most of the
drag and weight of the tube.
Respirometry equipment
The air flow rate was 48.1±0.4l min-1 STPD (mean ±
S.E.M., N=112) for walking and resting birds, 71.0±0.9l
min-1 STPD (N=30) for flying barnacle geese and
75.9±1.0l min-1 (N=23) for flying bar-headed geese
(KDG 2000 150l min-1 rotameter, B105 Charles Austen pump). The rate
of air extraction from the mask was great enough to prevent loss of exhaled
gases because calculated
O2 did not
change when the flow rate was decreased by 10% during a sample of flights
(paired t-tests, barnacle goose, t=0.29, P=0.8,
N=8; bar-headed goose, t=2.2, P=0.2, N=3).
Electronic sensors were used to measure the barometric pressure (Prosser) and
the temperature and relative humidity (Farnell Electronic Services) of the air
flow. A subsample (1.5l min-1) of air from the mask or chamber was
pumped (Charles Austin Dymax 30) through silica gel to dry the air before
passing through a paramagnetic oxygen analyser and an infrared carbon dioxide
analyser (Servomex 1440). The output signals from the gas analysers, and the
pressure, humidity and temperature sensors were passed through a purpose-built
interface box to an analog-to-digital converter unit (DAQ 500 or AT-MIO-16L
card, National Instruments) and then to a computer (Dell Inspiron 7000 or Dell
Dimension XPS P60). A customised computer program (written for LabVIEW,
National Instruments) sampled the signals from the digital converter unit at
1000 Hz and saved the mean values to a file every 10 s. The gas analysers were
calibrated at the start of each day by drawing oxygen-free dry nitrogen (BOC)
at 11 min-1 through the oxygen analyser or carbon dioxide (BOC) at
11 min-1 through the carbon dioxide analyser (measured to the
nearest 0.005l min-1, 1.2l min-1 rotameter, KDG 1100)
into the system together with the flow of atmospheric air to be used during
the experiment (Fedak et al.,
1981
). The lag between gases leaving the respirometry mask and
reaching the gas analysers was 20 s, at which time there was a step change in
gas concentration because the volume of the mask was so small.
Respirometry calculations
The rate of carbon dioxide production
(CO2) was
calculated from:
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Wind tunnel
The open-circuit wind tunnel in which the geese were flown was powered by a
170 kW ThrigeScott direct-current motor driving a Kiloheat RZR 13-1600
centrifugal fan (diameter 1.6 m, with backward curved impellers). The air from
the fan passed through a 4.5 mx4.5 m settling area, three fine-mesh
screens and a honeycomb before gradual contraction into the octagonal flight
section (cross-sectional area 4.25 m2) at the exhaust opening of
the solid-walled tunnel, 19 m downwind of the fan
(Fig. 1). The flight section
(3.06 m long x 2.10 m high x 2.50 m wide) was enclosed by nylon
mesh to prevent the bird from leaving the air stream. The birds were prevented
from flying upwind from the flight section by a 2 cm square plastic (0.5 mm
diameter) mesh and from leaving the flight section downwind by a 6 cm square
plastic (6 mm diameter) mesh. Air was drawn into the wind tunnel from outside
the building, so air temperature (14.9±2.3°C, mean ± S.D.,
range 10.5-19.0°C, N=187 flights), relative humidity
(62±14%, mean ± S.D., range 42-89%, N=187 flights) and
barometric pressure (100.4±1.0 kPa, mean ± S.D., range
97.2-101.7 kPa, N=187 flights) in the flight section were determined
by prevailing environmental conditions.
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The air speed and root-mean-square longitudinal turbulence in the flight section of the wind tunnel were determined using a hot-wire anemometer (Dantec 55P01) from which the output passed through a signal-conditioning card to an eight-channel 16-bit analog-to-digital converter (Io-tech 488/ADC) and then to a Macintosh G3 computer. Turbulence and mean air speed were sampled for 40 s at 200 Hz during each measurement. The output from the hot-wire anemometer was calibrated between 10 and 19 m s-1 against a propeller anemometer (Schiltnecht) and the pitot tube that was used routinely to set wind tunnel air speed. The discrepancy in the cross-calibration was 0.3% (range 0-0.4%) (N=10 speeds at 1 m s-1 increments between 10 and 19 m s-1), so all three instruments were assumed to provide accurate readings.
Variations in air speed and turbulence in the flight section, but without the upwind mesh in place, were measured with the hot-wire anemometer at points 0.21 m apart horizontally and 0.18 m apart vertically on a grid perpendicular to the direction of air flow. The grid was a maximum of 11 points wide and nine points deep. The centre of the grid was 1.23 m from the floor of the flight section. The longitudinal and lateral centres of the grid were centred on the flight section, 1.53 m from either end and 1.25 m from either side. Air speed and turbulence were also measured in the centre of the grid at 2 m s-1 increments at speeds between 8 m s-1 and 20 m s-1.
Air speed (17.9±0.01 m s-1, mean ± S.D., N=93) did not vary systematically over the cross section of the flight section of the wind tunnel. Root-mean-square longitudinal turbulence at an air speed of 17.9±0.01 m s-1 was 0.82±0.03% (N=35 points) in the central part of the flight section in which the geese flew (Fig. 2). Turbulence increased towards the walls of the flight section to 2.46±0.18% (N=29 points) between 0.5 and 0.3 m from the walls, 7.92±0.60% (N=21 points) between 0.3 and 0.1 m from the walls and 25.89±1.14 (N=8 points) less than 0.1 m from the walls. Turbulence was 0.6-0.9% at air speeds between 8.5 and 21 m s-1 in the centre of the area in which the birds flew.
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The equivalent air speed in the flight section was calculated from dynamic
pressure following Pennycuick et al.
(1996). Dynamic pressure was
measured using a manometer connected to a pitot tube that projected 1.0 m
vertically down into the air flow at the upwind end of the flight section. The
pitot tube and manometer measured air speed with a precision of±0.05 m
s-1 and an accuracy of 0.3±0.1% (see cross-calibration of
instruments described below).
Statistical analyses
Statistical tests were carried out with the assistance of Minitab (version
12.22, Minitab Inc.) following Zar
(1996). The coefficients of
determination (r2) of linear regression relationships and
double-logarithmic regression relationships (equivalent to power curves)
between
O2 and
fH were compared to determine which form better described these
relationships. The coefficients of determination differed by less than 0.02 in
all cases, with neither linear nor power relationships providing consistently
greater coefficients of determination. Either linear or power relationships
could therefore be used to describe the data. We present the linear
relationships calculated by least-squares regression. We used mean fH
and mean
O2
measured during entire 3-45 min flights or mean fH and mean
O2 during the
last 5 min of an 18 min walking period on the treadmill at a given speed as
independent data in our analyses of the relationships between fH and
O2. We obtained
most data on the relationship between fH and
O2 during flight
from one bird for each species. We calculated the 95% prediction intervals of
the relationships between fH and
O2 during flight
and the SE of the predicted
O2 for a given
value of fH during flight following equation 16.29 of Zar
(1996
). We assessed whether
simultaneous measurements of fH and
O2 from four
flights by three additional barnacle geese were consistent with the
relationship between fH and
O2 for the
individual of that species from which we had most data by determining whether
the data from the additional birds fell within the 95% prediction intervals of
the relationship.
We used analysis of covariance (ANCOVA) to test whether the slopes and
intercepts of the relationships between fH and
O2 during
walking on the treadmill varied among birds (sections 17.4 and 17.5 in
Zar, 1996
). Since the slopes
of the relationships did not vary significantly among birds, we used a single
regression equation with a common slope and a common intercept to describe the
relationship (Zar, 1996
).
Analysis of variance (ANOVA) was used to examine the effects of more than one factor upon a dependent variable. Factors that did not contribute significantly to a model were eliminated until only those factors that explained a significant amount of variation in the dependent variable remained in the model. We used t-tests to analyse the effect of two alternative factors upon a dependent variable. Two-tailed tests of statistical significance were applied in all analyses. Differences with P<0.05 were regarded as significant. Values are presented as means ± S.E.M. unless stated otherwise. Mean values across birds are means of the mean values for each bird.
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Results |
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The slopes of the relationships between
O2 and
fH during walking on the treadmill did not vary among individuals of
the same species for barnacle geese or bar-headed geese
(Fig. 3). The relationship
between
O2 and
fH during walking on the treadmill was:
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Influence of the presence of a trainer upon heart rate and the rate
of oxygen consumption during flight in the wind tunnel
The fH of barnacle geese flying in the wind tunnel without a mask
in autumn was lower when the birds flew less than 1 m from the trainer
(position B) than when they flew more than 1 m from the trainer (position A)
(t-test, t48=2.3, P=0.03). The
fH and
O2 of barnacle
geese during flight with a mask in autumn were also greater during flight in
position A than in position B (ANOVA, fH, position,
F1,15=9.3, P=0.01; bird,
F3,15=4.4, P=0.03;
O2, position,
F1,29=37.1, P<0.001; bird,
F4,29=11.2, P<0.001). The data from barnacle
geese during flight in the wind tunnel in spring, when the birds flew while
the trainer stood out of the air flow (position C), demonstrate that
fH did not vary between flight in position C and that in position A
(t-test, t19=0.5, P=0.6). The
fH of bar-headed geese during flight without a mask and the
O2 and the
fH of bar-headed geese during flight with a mask in autumn did not
vary with flight position relative to the trainer (t-tests,
P>0.5).
Only data from flights during which costs were not reduced by flying close
to the trainer (i.e. flights in position A) were used to calculate fH
and gas exchange rates typical of unassisted flight in the wind tunnel in
autumn and to examine the relationship between flight costs and flight speed
in barnacle geese. Data from flights during which barnacle geese flew less
than 1 m from the trainer (position B) were used to provide greater variation
in flight costs for the calibrations of fH against
O2 during
flight. The fH value of two barnacle geese during flight in positions
A or C did not vary among birds (P=0.6) but was greater in the spring
than in the autumn (ANOVA, F1,26=20.5,
P<0.001).
Respiratory exchange ratio
The respiratory exchange ratio (RER) declined steadily during flights by
both species. The mean RER of barnacle geese was 1.01±0.02
(N=34 flights by five birds) during the first minute of flight and
declined steadily to 0.80±0.03 (N=10 flights by three birds)
after 10 min of flight. The mean RER of bar-headed geese was 0.98±0.02
(N=23 flights by two birds) during the first minute of flight,
0.89±0.02 (N=14 flights by two birds) after 10 min of flight
and 0.68±0.01 (N=10) between 50 and 60 min of a flight by one
bird that flew for 61 min.
Relationships between flight speed and heart rate and the rate of
oxygen consumption during flight
There was no significant relationship between flight speed and fH
during flight without a mask or between flight speed and
O2 during flight
with a mask in either species of goose [regression with flight speed as the
independent variable, ANOVA with flight speed as a factor or multiple
regression with (flight speed)-1 and (flight speed)2 as
the independent variables (as might be expected if variation in fH or
O2 paralleled
that in mechanical power; Ward et al.,
2001
), P>0.08, Fig.
4].
|
Relationship between the rate of oxygen consumption and heart rate
during flight
Variation in fH followed that in
O2 within
flights during which the position of the bird relative to the trainer changed
during the flight (Fig. 5). We
used the mean fH and the mean
O2 from each
flight by barnacle goose B-B (1.8 kg) and bar-headed goose BH-O (2.8 kg) to
calculate the relationship between
O2 and
fH during flight for the single bird of each species for which we had
data from sufficient flights to perform this analysis
(Fig. 3). The relationship
between
O2 and
fH during flight was:
![]() | (4) |
![]() | (5) |
|
Rate of oxygen consumption during flight without a mask
We used the difference in fH, measured during flight by the same
bird with and without a mask to account for the effect of carrying the
respirometry mask and associated tubing upon
O2. The mean
fH of barnacle goose B-B during flight with a mask in autumn in
positions in which flight costs were not reduced by proximity to the trainer
was 479±8 beats min-1 (N=6 flights), equivalent to
a mean
O2 of
374±28 ml min-1 (equation 4). The mean fH of the
same bird during flight under the same conditions but without a mask was 12%
lower (423±15 beats min-1, N=12 flights),
equivalent to a mean
O2 of
295±29 ml min-1 (21% lower than that during flight with a
mask). The mean fH of bar-headed goose BH-O during flight without a
mask was 434±9 beats min-1, 6% lower than that during flight
with a mask (461±8 beats min-1). The relationship between
O2 and
fH for bar-headed goose BH-O (equation 5) predicted a mean
O2 during flight
without a mask of 388±21 ml min-1, which is 12% lower than
that during flight with a mask (441±20 ml min-1).
The mean O2
of barnacle goose B-B during flight without a mask is equivalent to
168±12 ml kg-1 min-1, 12±1 times resting
metabolic rate measured at night in the same bird and 18±1 times basal
metabolic rate (calculated on a mass-specific basis from
Nolet et al., 1992
), or
102±7 W (N=12 flights). The mean value of 388±21 ml
min-1 for the
O2 of bar-headed
goose BH-O during flight without a mask is equivalent to 138±6 ml
kg-1 min-1, 12±1 times resting metabolic rate
measured at night in the same bird, or 135±6 W (N=19
flights).
Comparison of the relationship between heart rate and the rate of
oxygen consumption during walking and flying
The relationships between
O2 and
fH had steeper slopes and lower intercepts during flight than during
walking in the barnacle goose and the bar-headed goose for which we had
sufficient data to perform the analysis (ANCOVA, barnacle goose B-B,
intercept, F1,22=9.2, P=0.007; slope,
F1,22=7.9, P=0.01; bar-headed goose BH-O,
intercept, F1,23=42.2, P<0.001; slope,
F1,23=87.3, P<0.001;
Fig. 3).
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Discussion |
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Relationships between heart rate, the rate of oxygen consumption and
flight speed
Neither fH nor
O2 showed the
U-shaped relationship with flight speed that might be expected if the general
relationship between mechanical power and speed predicted by most aerodynamic
models (Rayner, 1979
;
Pennycuick, 1989
;
Rayner and Ward, 1999
) were
reflected in variation in metabolic power
(Fig. 4). However, the
predicted mechanical power based on one aerodynamic model (model 1A of
Pennycuick, 1989
) also had an
almost flat relationship with flight speed for the speed range in which our
geese were prepared to fly, so our data are consistent with the predictions
from this particular aerodynamic model and with the measurements of the
fH of barnacle geese flying behind a truck
(Butler and Woakes, 1980
).
This result suggests that further measurements of fH in geese that
aim to elucidate any changes in metabolic rate during flight with respect to
flight speed in a wind tunnel may not be useful because any such changes are
likely to be small in relation to other sources of variation in fH or
O2 over the
range of flight speed at which the geese would fly. Lack of dependence of
aerobic metabolic rate upon sustainable flight speed in geese also leads to
the prediction that migratory flights should be conducted towards the upper
end of the speed range to minimise time and energy constraints. However, there
is great variability in the fH of barnacle geese during migration
(Butler et al., 1998
) that we
are not currently able to explain in relation to possible changes in the
energetic cost of flight, although in the short term they could be associated
with descent or periods of gliding and in the long term with changes in body
mass and/or physiology.
Prediction of the flight costs of wild migratory barnacle geese
The slope of the relationship between fH and
O2 was greater
and the intercept was lower for flying than for walking geese of both species
(Fig. 3). Predictions of
O2 during flight
in the wind tunnel based on the relationship between fH and
O2 for the same
bird during walking would underestimate measured
O2 during flight
by 38-54% for barnacle goose B-B and by 54-65% for bar-headed goose BH-O. The
error in predicting
O2 during flight
from the
fH/
O2
relationship that is appropriate during walking varies with fH
because the relationships between fH and
O2 for walking
and flying geese diverge with increasing fH
(Fig. 3). It is therefore not
possible to calculate
O2 during flight
using a relationship between fH and
O2 derived from
walking birds in combination with a simple correction term. These data confirm
the suggestion (Nolet et al.,
1992
; Butler et al.,
2000
) that the
O2) of wild
migratory geese cannot be predicted from fH and a calibration between
fH and
O2 during
walking. The measurements and predictions were made in the same individuals in
the current study, so our results are not confounded by potential
physiological differences between individuals or among the groups of captive
and free-living geese. The greater change in
O2 for a given
change in fH during flight than during walking is likely to be
related to a greater cardiac stroke volume
(Bishop and Butler, 1995
;
Butler et al., 1998
). In
addition, the flight muscles of barnacle geese have a much greater mass and
aerobic capacity than their leg muscles (Bishop et al.,
1995
,
1996
). Thus, flying geese would
be expected to be able to extract more oxygen from the blood per heart beat
than walking birds (Butler et al.,
1977
), leading to the observed greater
O2, and greater
rise in
O2 for a
given increase in fH, during flight.
The mean fH of wild barnacle geese was 317 beats min-1
at the start of the autumn migratory flight in Svalbard, falling to a minimum
of 226 beats min-1 when the birds were approximately 70% of the way
through their migration (Butler et al.,
1998). The relationship between fH and
O2 measured
during flight in a wind tunnel in the autumn in barnacle goose B-B predicted
that these values of fH would correspond to mean
O2 values of
144±40 ml min-1 at the start of migration and 15±55
ml min-1 when the birds are 70% of the way through migration. The
latter mean value of
O2 is clearly
impossible, and even the mean value from the start of the migration represents
48% of the
O2
calculated from the heart mass of migratory barnacle geese
(Butler et al., 1998
) or 49%
of the mean
O2
predicted from fH during flight without a mask in the wind tunnel.
Our calibration of the relationship between the fH and
O2 of captive
geese flying in the wind tunnel cannot therefore be used directly to calculate
the
O2 of wild
migratory geese from measurements of their fH. We also show
(Fig. 5) that the variation in
fH recorded during migration
(Butler et al., 1998
) is
likely to be related to variation in
O2. Possible
reasons for the difference in the relationship between
O2 and
fH of barnacle geese flown in the wind tunnel and that of their
free-living migratory conspecifics are discussed in Bishop et al.
(2002
).
Comparisons with previous studies
The barnacle geese for which we measured
O2 during flight
in the wind tunnel in the current study (1.98±0.08 kg, N=4)
were heavier than those for which
O2 was measured
during flight in a wind generator (1.68±0.17 kg, N=3;
Butler et al., 2000
). We
therefore expected that
O2 would be
greater for the barnacle geese in the current study (438±48 ml
min-1 compared with 332±9 ml min-1 for those
flown in the wind generator) since the power required for flight increases
with bird mass (Pennycuick,
1975
; Rayner,
1988
; Kvist et al.,
2001
). The
O2 of barnacle
geese flying in the wind generator without a mask was estimated to be 12%
lower than that during flight with a mask by Butler et al.
(2000
). The current study
suggested that
O2 was reduced
by 21% during flight without a mask. If this revised value for the difference
in
O2 between
flight by barnacle geese with and without a mask is applied to the birds that
flew in the wind generator, their mean
O2 would be 262
ml min-1 or 158 ml kg-1 min-1 (close to the
value of 168±12 ml kg-1 min-1 calculated for
barnacle goose B-B in the present study). The fH during flight in the
wind tunnel without a mask (451±23 beats min-1 in autumn)
was higher than that measured in the wind generator (378±15 beats
min-1) but lower than that of barnacle geese trained to fly
following a truck (512±4 beats min-1;
Butler and Woakes, 1980
).
New technology is stimulating an increasing number of measurements of
fH in free-living animals, such as the work reported by Bevan et al.
(1994,
1995
), Butler et al.
(1998
) and Weimerskirch et al.
(2001
). However, quantitative
interpretation of the data from such studies in terms of the energetic
consequences for flying animals is limited unless the correct relationship has
been established between fH and the rate of energy consumption during
flight. Without appropriate calibration of such relationships, the energetic
correlates of changes in fH during flight cannot be determined. Our
data clearly show that the relationship between fH and
O2 during
forelimb exercise (i.e. flight) of two species of geese is substantially
different from that during hindlimb exercise (i.e. walking), and this is also
likely to be the case in other species of flying animal. In addition, the
relationship between fH and
O2 differs
between captive and wild migratory barnacle geese. This is most likely to be
due to differences between the physiological condition of captive barnacle
geese and their wild migratory conspecifics, but could also be influenced by
variation in environmental conditions such as temperature, altitude or
turbulence.
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References |
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