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Accurate methods for estimating the energy expenditure of
free-ranging animals in the field are essential both for studies
of foraging ecology and when constructing models of energy
flux within ecosystems (Bevan et al., 1994, 1995c). Three
techniques are commonly used to estimate the energy
expenditure of free-ranging animals: time-energy budgets
(TEBs), the doubly labelled water method (DLW) and the use
of heart rate (f
H
). Each of the three techniques has its
advantages and weaknesses when applied in the field, and so
two or more are often used together.
The TEB is constructed by monitoring an animal’s activity
patterns in the field, then multiplying the duration of each
behaviour by its known or approximate energetic cost
(Goldstein, 1988; Nagy, 1989). The TEB method is time-
consuming (Weathers and Nagy, 1980; Williams and Nagy,
1984), but relatively easy to use in the field and does not
require catching or handling animals.
The DLW technique is more disruptive than the TEB, as it
involves catching the subject and sampling body fluid (e.g.
blood), injecting isotopes of oxygen and hydrogen (H
2
18
O and
either
2
H
2
O or
3
H
2
O), allowing them to equilibrate with the
body water, sampling body fluid again and releasing the
subject. At the end of the experimental period, which depends
on the biological half-life of each isotope in the study species,
the subject must be recaptured and a final body fluid sample
taken. The difference between the turnover rates of the
18
O and
2
H or
3
H labels can be used to calculate the rate of carbon
dioxide production (V
.
CO
∑), and therefore energy expenditure,
during the experimental period (Lifson and McClintock, 1966;
Nagy, 1980; Tatner and Bryant, 1989; Speakman, 1997).
2819
The Journal of Experimental Biology 203, 2819–2832 (2000)
Printed in Great Britain © The Company of Biologists Limited 2000
JEB2898
The relationship between heart rate (f
H
) and rate of
oxygen consumption (V
.
O
∑) was established for a marine
diving bird, the common eider duck (Somateria mollissima),
during steady-state swimming and running exercise. Both
variables increased exponentially with speed during
swimming and in a linear fashion during running. Eleven
linear regressions of V
.
O
∑ (mlkg
−1
min
−1
) on f
H
(beatsmin
−1
)
were obtained: five by swimming and six by running the
birds. The common regression was described by
V
.
O
∑=10.1+0.15f
H
(r
2
=0.46, N=272, P<0.0001). The accuracy
of this relationship for predicting mean V
.
O
∑ was
determined for a group of six birds by recording f
H
continuously over a 2-day period and comparing estimated
V
.
O
∑ obtained using the common regression with (i) V
.
O
∑
estimated using the doubly labelled water technique
(DLW) and (ii) V
.
O
∑ measured using respirometry. A two-
pool model produced the most accurate estimated V
.
O
∑ using
DLW. Because of individual variability within mean values
of V
.
O
∑ estimated using both techniques, there was no
significant difference between mean V
.
O
∑ estimated using f
H
or DLW and measured V
.
O
∑ values (P>0.2), although
individual errors were substantially less when f
H
was used
rather than DLW to estimate V
.
O
∑. Both techniques are,
however, only suitable for estimating mean V
.
O
∑ for a group
of animals, not for individuals.
Heart rate and behaviour were monitored during a bout
of 63 voluntary dives by one female bird in an indoor tank
1.7m deep. Tachycardia occurred both in anticipation of
and following each dive. Heart rate decreased before
submersion but was above resting values for the whole of
the dive cycle. Mean f
H
at mean dive duration was
significantly greater than f
H
while swimming at maximum
sustainable surface speeds. Heart rate was used to estimate
mean V
.
O
∑ during the dive cycle and to predict aerobic dive
limit (ADL) for shallow dives.
Key words: Somateria mollissima, Branta leucopsis, Aythya fuligula,
heart rate, bradycardia, tachycardia, oxygen consumption, doubly
labelled water, telemetry, exercise, energy expenditure.
Summary
Introduction
ESTIMATION OF THE RATE OF OXYGEN CONSUMPTION OF THE COMMON
EIDER DUCK (SOMATERIA MOLLISSIMA), WITH SOME MEASUREMENTS OF
HEART RATE DURING VOLUNTARY DIVES
P. A. J. HAWKINS
1
, P. J. BUTLER
1,
*, A. J. WOAKES
1
AND J. R. SPEAKMAN
2
1
School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, UK and
2
Aberdeen Centre for
Energy Regulation and Obesity (ACERO), Department of Zoology, University of Aberdeen, Tillydrone Avenue,
Aberdeen AB24 3TZ, UK
*Author for correspondence (e-mail: P.J.Butler@bham.ac.uk)
Accepted 20 June; published on WWW 22 August 2000
2820
Validation studies indicate that the DLW method provides
an accurate (within 5%) estimate of CO
2
production across
groups of individuals, but individual estimates are less accurate
(Speakman, 1997, 1998). DLW is minimally invasive and non-
toxic, but expensive to apply. It also measures total field energy
expenditure only, not its components. These must be estimated
by using DLW in conjunction with other techniques in field
bioenergetics, such as TEBs (Nagy, 1989; Tatner and Bryant,
1989).
A number of studies have investigated the relationship
between f
H
and rate of oxygen consumption (V
.
O
∑) and
shown that mean V
.
O
∑ can be predicted with reasonable
accuracy for a group of animals by determining mean f
H
and
applying the previously calibrated relationship between
the two variables (e.g. Bevan et al., 1992, 1994, 1995a,c;
Butler et al., 1992; Nolet et al., 1992; Boyd et al., 1995).
This technique is the most invasive of the three, as heart-
rate loggers are usually surgically implanted (Bevan et al.,
1994, 1995b,c). It has proved to be useful in the field,
however, as data can be collected over relatively long periods
and f
H
may be used to estimate components of energy
expenditure (Bevan et al., 1995a; Butler et al., 1995; Boyd et
al., 1999).
The V
.
O
∑/f
H
relationship and the accuracy of this method
of estimating V
.
O
∑ in comparison with DLW and direct
respirometry has been evaluated in two species of waterfowl:
the tufted duck Aythya fuligula, a small-bodied freshwater
diving duck (mass approximately 600g; Woakes and Butler,
1983; Bevan et al., 1992), and the barnacle goose Branta
leucopsis (mass approximately1780g; Nolet et al., 1992). The
present study aimed to calibrate and validate these techniques
in a large, marine diving duck, the common eider (Somateria
mollissima L; mass approximately1800g) and to compare the
correlations between V
.
O
∑ and f
H
obtained during running and
swimming exercise using a treadmill and water channel,
respectively.
Heart rate was also recorded during a bout of 63 dives
performed by a female bird. The first investigations into
the physiology of diving were undertaken using restrained
animals who were forcibly submerged (e.g. Scholander,
1940; Andersen, 1966). Those studies described a set of
cardiovascular adjustments to submersion known as the
‘classic’ dive response, which includes a reduction in f
H
below
the resting level, or diving bradycardia. In contrast to forced
immersion, voluntary dives generally involve foraging activity,
are relatively short in duration and occur in a series (Butler and
Woakes, 1979). Investigations into free dives in birds using
radiotelemetry (Millard et al., 1973; Butler and Woakes, 1979;
Kanwisher et al., 1981; Woakes and Butler, 1983; Furilla and
Jones, 1987; Stephenson et al., 1986, 1992) have shown that
the cardiovascular response to voluntary dives does not
correspond to the ‘classic’ pattern. For example, in the tufted
duck, a period of pre-dive tachycardia ceases on submersion,
but f
H
does not fall below resting levels, i.e. there is no true
bradycardia (Butler and Woakes, 1979; Woakes and Butler,
1983; Stephenson et al., 1986), and blood flow to the
(locomotory) leg muscles increases to five times the resting
rate (Bevan and Butler, 1992).
The differences in body size and ecology between the tufted
duck and the eider duck may qualitatively or quantitatively
affect the cardiovascular response to voluntary dives. Common
eiders in the field have been reported to dive to depths of 60m,
although shallow dives (1–6m) are common and the species is
also often observed to dabble at low tide (Cantin et al., 1974).
The present study was undertaken using a tank 1.7m deep, so
the results are applicable to shallow dives in the field but
cannot be extrapolated to deeper dives.
Materials and methods
Use of f
H
and DLW to estimate V
.
O
∑
This section of the present study was undertaken in two
parts: (1) calibration of the relationship between f
H
and V
.
O
∑
over a range of running and swimming exercise levels, and (2)
validation of the accuracy of this relationship by using it to
estimate V
.
O
∑ from f
H
recorded continuously over a 2-day
period, and comparing this with V
.
O
∑ simultaneously estimated
using the DLW technique and directly measured using
respirometry.
Experimental animals
Rearing and husbandry
Eider duck (Somateria mollissima L.) eggs were collected
from a colony on the Isle of May, Firth of Forth, Scotland, with
the permission of Scottish Natural Heritage. The ducklings
were imprinted on the experimenter for ease of handling and
reduction of stress. Up to 8h a day were spent with the birds
during their first month, and they were taken for a daily walk
for the first 6 weeks. They were initially housed in an indoor
enclosure 2.1m×3.6m, containing a pool 2.1m×2.2m and
0–22cm deep. A brooder lamp was supplied, but was only used
by the birds on the first day. At 6 weeks old, they were moved
to an outdoor enclosure 18m×7.4m×2m (length×width×
height), with an area of grass, an area of gravel and a pond
8.1m×3.8m×0.7m deep. The ducklings were regularly taken
into the laboratory to habituate them to the sight and sound of
the experimental apparatus, but were only kept indoors when
required for procedures.
The ducklings were fed initially on commercial grower’s
chick crumbs and introduced to Special Diets Services ‘Diet
A’ sinkers in the second week. The latter food contains animal
protein and sinks in water, which is appropriate for a
carnivorous, diving animal. By the third week, the ducklings
were fed ‘Diet A’ alone and grit was supplied on the bottom
of their pool. When fully grown, the birds preferred the gravel
surrounding their pond to grit, so this was also provided
indoors. The ‘Diet A’ sinkers encouraged the birds to use all
three dimensions of their tank or pond, made them spend more
of their time foraging for their food and provided them with
supplementary exercise. Environmental stimulation was
provided indoors by submerging rubber bungs, mussel shells,
pebbles and bricks in their pool and fastening chains and
P. A. J. HAWKINS AND OTHERS
2821Heart rate and oxygen uptake in exercising eider ducks
plastic cable ties securely to the side of their pen and tank
(Hawkins, 1998).
After studies involving the ducks had finished, the remaining
birds were certified fit by a veterinary surgeon and rehomed in
a private collection with the permission of the local Home
Office Inspector.
Preparation for procedures
At 8 weeks of age, the first three ducks were brought inside
and housed in a tank 1.6m×1.0m×1.7m deep, with a dry area
1.5m×0.6m at one end. 10 weeks after hatching, the ducks had
attained a mean body mass of 1669±33g (mean ± 1 S.E.M.;
N=10), which was 87% of their maximum final mass. The
birds were therefore deemed to be large enough for a pulse-
interval-modulated electrocardiogram (ECG) radiotransmitter
(mass 10g; Butler and Woakes, 1989) to be implanted into the
abdominal cavity. The implantation procedure and subsequent
experimental techniques were licensed under the UK Animals
(Scientific Procedures) Act 1986. All surgical procedures took
place under sterile conditions and general anaesthesia, as
has been described previously (Stephenson et al., 1986).
Antibiotic (tetracycline, 0.1mlkg
−1
) and painkiller (Temgesic,
0.1mlkg
−1
) were administered intramuscularly before surgery,
so that they could begin to take effect before the operation
ended. Behaviour was normal following the operation except
that the tail was held down for up to a day, and the duck
immediately preened the abdominal feathers (none of which
were removed) to cover the wound. A further dose of Temgesic
was administered if the tail was still down after 24h. 2 weeks
after the transmitters had been implanted, the ducks’ mass had
increased to 1791±49g (N=10; 93% maximum final mass),
and they were used in metabolic experiments for the first time.
It was originally intended that the same six ducks would be
used in each section of the present study. This proved to be
impossible, as four of the ducks died from aspergillosis (no
results are presented here that were obtained from sick birds).
Therefore, different ducks were used for calibrations using the
water channel and treadmill and the DLW validations, and the
N numbers vary between these treatments. This was
unfortunate, but could not be avoided.
Experimental techniques
Respirometry
Ducks were placed in respirometry boxes, which were either
self-contained or sealed around a water channel or treadmill
(see below). A flow meter (GEC Marconi Process Control Ltd)
was used to measure the air drawn through the boxes by a
pump (Normand Electrical Co. Ltd) at 25–30lmin
−1
(exercising) or 15–20lmin
−1
(resting overnight). The contents
of the boxes were mixed by three fans, and the concentration
of CO
2
was kept below 0.5%. A subsample of the outlet
flow was dried in a column of silica gel and passed to a
carbon dioxide analyser (detection range 0–1%, Analytical
Development Co.). CO
2
was then removed by a column of soda
lime before the sample passed to an O
2
analyser (detection
range 0–100%, Servomex Ltd). The sample flow was switched
either manually or, during overnight experiments, by a
solenoid valve (RS Components Ltd) to sample ambient air for
2min every 20min, in order to allow compensation for any
inherent drift in the instruments. Nitrogen dilution tests used
to calibrate the system (Fedak et al., 1981) showed that there
were no leaks and that the system was accurate to within 2%.
The output from the analysers entered a purpose-built
interface, the output from which was displayed on a thermal
chart recorder (Graphtek WR7700).
Telemetry
The signal from the radiotransmitter was passed from the
receiver to a purpose-built decoder. This extracted ECG data,
which were passed to a tape recorder (TEAC A450). Ambient
temperature and relative humidity were measured with a probe
(Vaisala, Helsinki HMP35A) inside the box. The output from
the probe entered the same interface as that from the analysers.
The water channel
The ducks were trained to swim on a variable-speed water
channel (Armfield Engineering Ltd), with a test section
0.5m×1.2m×0.4m deep. The water channel was fitted with an
anti-turbulence grid, and water speed was measured by
a Braystoke current flow meter (BFM0002, Valeport
Developments Ltd). An open-circuit Plexiglas respirometer
0.65m×0.45m×0.3m deep was placed over the bird after
several training sessions. The side edges of the respirometer
projected 5cm below the surface of the water, and the front
and back edges were made airtight using flexible polythene
sheets. At water speeds of 1.1ms
−1
and above, the system was
found to leak air due to increased turbulence at the transverse
seals. As the percentage of N
2
lost (Fedak et al., 1981) was
consistent at each of the three top speeds, correction factors
could be calculated. A previous study (Woakes and Butler,
1983) found that calculations of CO
2
production were
inaccurate as a result of absorption of CO
2
by the flowing
water, so this variable was not measured.
The treadmill
The ducks were trained to run on a variable-speed treadmill
(Powerjog EV2, Sports Engineering). The same respirometer
box that was used on the water channel was mounted on a
wooden frame 0.65m×0.3m×0.15m high. The system was
made airtight using brushes on the lower edges of the frame,
draught excluder foam below the side edges of the box and
parcel tape to seal the front and back edges. The apparatus was
calibrated using N
2
injection (Fedak et al., 1981), and the
system was found not to leak at working speeds.
Protocols
Resting f
H
and V
.
O
∑
To obtain resting heart rate and oxygen consumption, each
duck (N=6) was fasted for 10h, then placed overnight in an
opaque respirometry box. Heart rate and rate of oxygen
consumption were monitored every 60s from 21:00h to
09:00h and one mean measurement was calculated for every
2822
5min period between 23:00h and 07:00h, so that 96
measurements were taken for each bird.
The water channel
Initially, each duck (N=5) swam between grids of plastic
netting placed vertically in the flume. After 1–2 weeks of
training, the ducks could swim at speeds of up to 1.3ms
−1
for 20min. Each duck swam at a designated speed until the
concentration of oxygen in the air leaving the box became
constant. The duck swam for a further 20min so that
measurements could be made. Random number tables were
used to determine the order of swimming speeds, so that the
ducks did not become accustomed to a set pattern of speeds.
However, no more than two ‘high-speed’ (1.0ms
−1
and
above) swims of 20min duration were performed without
an intermediate period at low (below 0.7ms
−1
) or zero
speed. Each bird remained in the respirometer on the water
channel for up to 3h per day, swimming at nine different
speeds, including periods of rest with the flume motor both
on and off. Water temperature during experiments was
13.7–19.0°C.
The treadmill
The experimental procedure was essentially the same as that
for the flume; the birds (N=6) ran for 20min at speeds up to
0.8ms
−1
. Care was taken not to overwork them, and they had
at least one slow or resting period per hour. Each duck
remained on the treadmill for approximately 2h per day.
Validation of estimates of V
.
O
∑
obtained using f
H
and DLW
against respirometry
The energy expenditure of eider ducks (N=6) estimated
using DLW and the relationship with f
H
was compared with
that obtained by respirometry over 2 days. Oxygen
consumption was monitored continuously during the
experiments using respirometry, and f
H
was recorded by
transmitting ECG data to a data logger (Woakes et al., 1995)
connected to the decoder using purpose-built leads.
On the first day of the procedure, the duck was weighed and
a blood sample of 1ml was taken from the brachial vein to
measure background enrichment. The plasma was separated
using a centrifuge at 13000g for 5min, then samples of
approximately 10µl were flame-sealed into heparinised
capillary tubes. An isotope mixture of approximately
0.3mlkg
−1
of H
2
18
O (90.02%) and 0.15mlkg
−1
of
2
HHO
(99.8%) was injected into the pectoral muscle at 10:00h.
The first blood sample was taken 4h after the injection, as
this was an adequate time for the isotope mixture to equilibrate
in barnacle geese of identical mass (Nolet et al., 1992). The
duck was then immediately placed on the water channel and
measurements of V
.
O
∑ and f
H
began. A final sample and body
mass measurement were taken 48h later. The bird was kept on
the flume continuously during the experiment and exercised at
various speeds for up to 6h per day. Waterfowl diet pellets
were offered inside the respirometer box, but some of the ducks
refused to eat.
During the first three validations (birds 1, 2 and 6), the
ducks’ feathers became damp at the end of the 48h period on
the flume. The protocol was therefore altered for the remaining
three experiments (ducks 3, 10 and 11). At 20:00h each day,
the ducks were removed from the water channel and placed in
the darkened respirometer box that was used for the resting
measurements, with a foam rubber mat to rest on. They
remained in the box until 08:00h the following day, when they
were returned to the water channel. Of the 12h they spent on
the channel, they were exercised for 6h, as before. Although
a few minutes of data were lost during the transfers, the ducks
were able to preen at night, so were able to maintain the
integrity of their feathers and were not stressed by becoming
waterlogged on the flume (see also Nolet et al., 1992).
Calculations
Respirometry
Oxygen consumption was calculated according to equation
1(d) of Withers (1977). Carbon dioxide production was
calculated according to Withers (1977) and Culik et al. (1990).
Results obtained during the training sessions were used to set
the respiratory quotient, RQ, at 0.8 for exercising and 0.7 for
resting birds.
Doubly labelled water
Plasma samples were vacuum-distilled in Pasteur pipettes
(Nagy, 1983). The resultant water samples were converted to
carbon dioxide or hydrogen gas for mass spectrometric
analysis of
18
O or
2
H using the guanidine chemical conversion
procedure (Boyer et al., 1961; Speakman et al., 1990) and zinc
reduction (Wong and Klein, 1987), respectively. Isotope
enrichments were determined by gas-source isotope-ratio mass
spectrometry using a dual-inlet mass spectrometer (VG
Optima, Micromass Ltd). All samples were measured relative
to a working standard gas in the reference side of the inlet. The
working standard was characterised relative to the international
SMOW/SLAP standards provided by the International Atomic
Energy Agency. Day-to-day variation in performance of the
mass spectrometer was accounted for using a series of enriched
internal standards of known enrichment relative to the
international enriched standards (302a, 302b, 304a and 304b).
Enrichments relative to SMOW/SLAP were converted to parts
per million (p.p.m.) using the known absolute ratios of these
standards.
All isotope analyses and calculations were performed blind
on the respirometry data. Calculations were performed using
the DLW analysis program (Lemen and Speakman, 1997;
www/natureware/double.htm), and V
.
CO
∑ was estimated from
the isotopic enrichment of the plasma samples according to five
different equations: (i) Lifson and McClintock (1966),
equation 35; a one-compartment model, i.e. it assumes that the
dilution spaces available to the labelled H and O are equal; (ii)
Schoeller et al. (1986), equation A6; this and all subsequent
equations are two-compartment models and are corrected to
allow for the nonaqueous (body fat) pool into which
2
H is
incorporated (Lifson et al., 1955); (iii) Speakman (1993),
P. A. J. HAWKINS AND OTHERS
2823Heart rate and oxygen uptake in exercising eider ducks
equation 4; this includes the population ratio of the hydrogen
and oxygen dilution spaces; (iv) Speakman et al. (1993),
equation 3, with a revised dilution space ratio obtained from a
large number of published studies; (v) Speakman (1997),
equation i; an updated version of Lifson and McClintock
(1966), equation 35, with an adjusted evaporative water loss
term.
The results were converted to V
.
O
∑ using the mean measured
RQ of 0.77 obtained during treadmill exercise.
Statistical analyses
Results are presented as means ± S.E.M. Differences between
pairs of mean values were tested using Student’s t-tests
(P<0.05), with significance levels adjusted for repeated testing
using a Bonferroni correction where appropriate. In linear
regressions, the Pearson product–moment correlation
coefficient is given. The 95% confidence interval for y was
calculated and slopes and elevations compared according to
Zar (1984, pp. 274, 300–302).
Heart rate during voluntary dives
Protocol
The ducks were housed on the deep indoor tank (see above).
They dived in response to mussels (Mytilus edulis) and sand
eels (Ammodytes spp.) thrown onto the water and also to play
with rubber bungs and stones that lay on the bottom of the
tank. ECG was decoded and recorded as above. All the birds
dived frequently when they were juveniles, but were reluctant
to dive while an observer was present as they grew older and
would not dive at all from a respirometry box. It was therefore
only possible to obtain f
H
data from one female duck
(individual 1).
Calculations
Heart rates were calculated from the ECG traces at intervals
before, during and after each dive and at the instants of
immersion and emersion of the duck’s head. Mean f
H
was
calculated for each instant in the dive cycle. Differences
between pairs of mean values were tested using Student’s t-
tests (P=0.05).
Results
Use of f
H
to estimate V
.
O
∑
Heart rate and oxygen consumption: resting and swimming
Table 1 lists the overnight resting results for six fasting
ducks in air. Five birds were exercised on the water channel
(Table 2). There was no significant difference between mean
resting values of f
H
and V
.
O
∑ measured with the flume motor on
and off (paired-sample t=1.251 and 0.709, respectively;
P>0.2). Mean values for f
H
and V
.
O
∑ at rest with the motor off
were 134±16beatsmin
−1
and 30.6±2.6mlkg
−1
min
−1
,
respectively. Heart rate while resting on water with the fan off
was 1.4 times greater than that while resting in air, and V
.
O
∑ was
2.4 times greater. Both variables increased exponentially with
swimming speed above 1ms
−1
(Fig. 1). No duck was able to
swim at speeds over 1.3ms
−1
. At the maximum speed, mean
V
.
O
∑ was 55.5±3.6mlkg
−1
min
−1
, which was 4.3 times the
overnight resting value and 1.8 times mean resting V
.
O
∑ on
water (Tables 1, 2) and mean f
H
was 182±19beatsmin
−1
, twice
that when resting overnight and 1.4 times that when resting on
water with the fan off.
Heart rate and oxygen consumption: running
Maximum sustainable running speeds ranged from 0.72 to
0.82ms
−1
in all six ducks apart from duck 4, who would not
run at speeds above 0.6ms
−1
(Table 2). The relationship
between V
.
O
∑ and speed was linear (Fig. 2). Mean V
.
O
∑ at
maximum speed was 39.0±2.1mlkg
−1
min
−1
, which was 3.0
times the mean value recorded while resting overnight, while
f
H
increased to 195±19beatsmin
−1
, a mean increase factor of
2.1. Mean RQ during running exercise was 0.77±0.12, which
was not significantly greater than that recorded while resting
overnight (t=2.279, P=0.049).
Table 1. Mean resting heart rate (f
H
), rate of oxygen consumption (V
˙
O
2
), rate of carbon dioxide production (V
˙
CO
2
) and
respiratory quotient (RQ) measured in air in six fasting eider ducks
Mass f
H
V
˙
O
2
V
˙
CO
2
Duck Sex (g) (beatsmin
−1
) (mlkg
−1
min
−1
) (mlkg
−1
min
−1
)RQ N
1 F 1756±15 108±1 13.0±0.2 96
2 M 1980±17 96±1 12.6±0.5 7.3±0.2 0.58 96
4 F 1632±20 79±1 11.3±0.7 8.3±0.5 0.73 48
5 M 1808±36 80±1 12.7±0.3 10.5±0.6 0.82 96
6 M 1765±29 89±3 13.0±0.2 6.7±0.5 0.51 96
7 F 1799±19 107±1 14.3±0.4 7.6±0.6 0.53 96
Mean 1790±46 93±5 12.8±0.4 8.1±0.7 0.63±0.06 6
N, number of observations; values are means ± 1
S.E.M.
Measurements were made in air.
The mean mass shown for each duck is the body mass during all experiments apart from validations.
The carbon dioxide analyser was not available when resting V
˙
O
2
was recorded for duck 1.
N=48 for duck 4 because V
˙
O
2
was not stable for long-enough periods.
2824
Calibration of the relationship between V
.
O
∑
and f
H
The relationship between V
.
O
∑ and f
H
, for all the birds, was
most accurately described by a linear regression, as opposed
to log-transforming either or both of the variables (Table 3).
Eleven regressions of V
.
O
∑ on f
H
were obtained, six by running
birds on the treadmill (e.g. Fig. 3) and five by swimming them
on the flume. Resting values were included in the regressions.
Seven different ducks were used; four of these (ducks 2, 4, 5
and 6) were exercised on both the flume and the treadmill. A
pairwise comparison (Zar, 1984) was performed on all 11
regressions. The slopes were significantly different (i.e.
P<0.05) in 19 of the 55 pairs, while the intercepts were
significantly different in 33 instances. Of the four ducks who
both swam and ran, both the slope and intercept differed
significantly between the two modes of exercise in one bird
(individual 2), the intercept differed for individuals 4 and 6,
and the slope differed for individual 5 (P<0.05 in each case).
A multiple comparison of all 11 lines (Zar, 1984) indicated that
the slopes and intercepts were significantly different (F=13.53
and 14.30, respectively; P<0.001 in each case).
The data were initially grouped according to whether they
P. A. J. HAWKINS AND OTHERS
Table 2. Mean heart rate (f
H
), rate of oxygen consumption (V
˙
O
2
) and rate of carbon dioxide production (V
˙
CO
2
) during swimming
and running exercise, and respiratory quotient (RQ) during running, in seven eider ducks
Flume Treadmill
Rest Rest
Swimming Running
Motor off Motor on 1.0 m s
−1
1.3ms
−1
0.7–0.8ms
−1
f
H
V
˙
O
2
f
H
V
˙
O
2
f
H
V
˙
O
2
f
H
V
˙
O
2
f
H
V
˙
O
2
V
˙
CO
2
(beats (mlkg
−1
(beats (mlkg
−1
(beats (mlkg
−1
(beats (mlkg
−1
(beats (mlkg
−1
(mlkg
−1
Duck Sex min
−1
) min
−1
) min
−1
) min
−1
) min
−1
) min
−1
) min
−1
) min
−1
) min
−1
) min
−1
) min
−1
)RQ
1 F 133±8 (2) 27.8±1.2 132±3 (3) 27.2±0.9 162±6 (3) 33.5±1.9 220 (1) 57.2
2 M 165±7 (3) 32.5±1.3 164±16 (3) 35.1±1.6 170±8 (3) 40.0±1.1 203±7 (3) 54.6±4.2 268±1 (2) 39.5±2.2 33.7±0.6 0.82
4 F 174±9 (3) 39.7±2.1 176±6 (3) 38.3±1.6 179±10 (3) 47.0±1.3 196±9 (3) 59.9±2.3 207 (1) 46.6 32.6 0.70
5 M 95±4 (3) 24.6±1.3 108±3 (3) 27.3±1.7 100±2 (3) 25.9±1.9 112±1 (2) 42.2±2.5 173±15 (3) 32.2±2.6 23.6±2.4 0.73
6 M 102±16 (3) 28.4±2.4 161±5 (3) 26.5±0.7 202±12 (3) 35.4±1.5 181±10 (3) 63.6±2.1 143 (1) 39 32.5 0.83
7F 187 (1) 40.4 29.4 0.73
8F 191±4 (3) 36.5±0.4 29.8±0.4 0.82
Mean 134±16 30.6±2.6 148±12 30.9±2.4 163±17 36.4±3.5 182±19 55.5±3.6 195±19 39.0±2.1 30.3±1.6 0.77±0.12
N 5555 5555 6666
Values are means ± 1 S.E.M. and numbers in parentheses are number of observations (N) for each duck at each speed. N=2 for duck 1 with
the flume motor off because she only became settled on two occasions. Where N<3 for maximum speeds, the duck could not maintain these
speeds in a steady state for three times.
Heart rate and V
˙
O
2
during swimming did not increase until speeds above 1.0ms
−1
were reached. The maximum sustainable swimming speed
was 1.3ms
−1
.
The maximum running speed was 0.72–0.82ms
−1
for all ducks except duck 4, who refused to run at speeds above 0.6ms
−1
. Consistent
resting values could not be obtained on the treadmill.
0
50
100
150
200
250
0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 1.1 1.2 1.3
f
H
(beats min
-1
)
o
A
B
0
10
20
30
40
50
60
70
0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0 1.1
1.2
1.3
Speed (m s
-1
)
V
O
2
(ml kg
-1
min
-1
)
.
Off
Off
On
On
Fig. 1. Mean heart rate f
H
(A) and rate of oxygen consumption V
.
O
∑
(B) at various swimming speeds in an eider duck (individual 1). The
first two points on each graph were measured at rest, with the flume
motor on and off. Values are means ± 1
S.E.M.; N=3 in each case
except rest (motor off; N=2) and 1.3ms
−1
(N=1).
2825Heart rate and oxygen uptake in exercising eider ducks
had been obtained from swimming or running birds. The
relationship between V
.
O
∑ and f
H
for swimming birds was
described by the equation:
V
.
O
∑ = 10.9 + 0.16f
H
(r
2
=0.55, N=165, P<0.0001), (1)
where V
.
O
∑ is in mlkg
−1
min
−1
and f
H
in beatsmin
−1
, and for
running birds by:
V
.
O
∑ = 11.6 + 0.12f
H
(r
2
=0.37, N=107, P<0.0001). (2)
The slopes and intercepts of the two regressions were
significantly different (F=33.16 and 147.98 respectively;
P<0.0001 in each case). The six regressions obtained by
running birds and the five by swimming birds were also
significantly different within their groups (running, slopes
F=3.27, P=0.01; intercepts F=16.29, P<0.001; swimming,
slopes F=47.43, P<0.0001; intercepts F=11.03, P<0.0001).
A common regression was obtained by pooling the data:
V
.
O
∑ = 10.1 + 0.15f
H
(r
2
=0.46, N=272, P<0.0001). (3)
The common regression line for the pooled data thus explained
46% of the variation (Table 3; 95% confidence interval of
mean estimate of V
.
O
∑ calculated below), whereas the
regressions for data obtained by swimming and running birds
explained 55% and 37%, respectively.
Validations
Heart rate
Table 4 lists the validation results and the accuracy of the
estimated oxygen consumption for each duck. The mean
estimate of V
.
O
∑ obtained using the common regression line was
Fig. 2. Rate of oxygen consumption versus running speed in an eider
duck (individual 6). Mean values (±1
S.E.M.) were calculated for each
speed class (N=33). The line through the points is described by the
regression V
.
O
∑=14.5U+28.8, where U is speed; r
2
=0.82, P=0.005.
The resting values were not included in the regression.
0
5
10
15
20
25
30
35
40
45
0 0.1 0.2 0.3 0.4 0.5 0.6 0.7
Speed (m s
-1
)
V
O
2
(ml kg
-1
min
-1
)
.
Table 3. The relationship between rate of oxygen consumption and heart rate in seven exercising eider ducks
Duck Exercise a 95% CI b 95% CI r
2
NP
1 Swim −9.6 7.8 0.27 0.05 0.79 38 0.001
2 Swim −12.5 13.9 0.30 0.08 0.67 30 0.01<P<0.001
2 Run 7.0 12.8 0.13 0.07 0.53 15 >0.2
4 Swim 16.4 18.5 0.16 0.10 0.29 27 0.01
4 Run −2.7 13.3 0.21 0.08 0.65 18 0.01
5 Swim −4.8 11.0 0.33 0.10 0.51 40 0.1<P<0.01
5 Run 5.4 10.8 0.15 0.06 0.53 23 0.1<P<0.01
6 Swim 15.3 11.5 0.25 0.05 0.77 30 0.1<P<0.01
6 Run −11.9 13.0 0.36 0.11 0.79 15 0.01
7 Run −15.6 10.7 0.30 0.07 0.84 16 0.01
8 Run −12.2 20.1 0.23 0.11 0.51 20 >0.2
Common 10.1 3.3 0.15 0.02 0.46 272 <0.0001
V
˙
O
2
, rate of oxygen consumption (mlkg
−1
min
−1
); f
H
, heart rate (beatsmin
−1
).
A linear relationship (y=a+bx), where y=V
˙
O
2
and x=f
H
, described the data most accurately, as opposed to an exponential, logarithmic or
power regression (95% CI=95% confidence intervals of the mean estimates of V
˙
O
2
). The common regression was obtained by stacking and
regressing all the data together.
0
5
10
15
20
25
30
35
40
45
80 100 120 140 160 180 200
f
H
(beats min
-1
)
V
O
2
(ml kg
-1
min
-1
)
.
Fig. 3. The relationship between V
.
O
∑ and f
H
in an eider duck
(individual 7) running on a treadmill. The relationship is described
by the equation V
.
O
∑=0.30f
H
−15.6; r
2
=0.84, P<0.01, N=16.
2826
32.3±2.6mlkg
−1
min
−1
, which overestimated the mean
measured V
.
O
∑ of 31.3±2.5mlkg
−1
min
−1
by an algebraic mean
of 3.7±4.2%. This was not significant (paired-sample t=0.769,
P>0.2). However, the individual errors ranged from −14.1 to
+16.6%, so that the mean absolute deviation (the mean average
of the magnitudes of the errors) was greater, at 8.4%. The
relatively small difference between the absolute and algebraic
means is due to all the estimates apart from that for duck 11
exceeding the measured value. The 95% confidence interval
of the mean estimate of V
.
O
∑ was 6.26mlkg
−1
min
−1
(Zar,
1984).
DLW
Four of the five equations estimated mean V
.
O
∑ across
individuals with an accuracy within 5% except for Speakman
(1997) equation i, which overestimated oxygen consumption
by an algebraic mean of 10.8% (Table 5). However, the
absolute errors ranged from −75.2 to +71.5%, and all five
equations produced estimates with mean absolute errors over
40%. In pairwise comparisons, the only two equations that did
not produce differing mean estimates of V
.
O
∑ significant at
P=0.05 were equation S3 from Speakman et al. (1993) and
equation 4 from Speakman (1993) (t=0.478; P>0.2 following
P. A. J. HAWKINS AND OTHERS
Table 4. Mean oxygen consumption (V
˙
O
2
) and heart rate (f
H
) obtained from six eider ducks over 2 days, with estimates of V
˙
O
2
derived from a previously calibrated relationship between V
˙
O
2
and f
H
(see Table 3)
Mass V
˙
O
2
f
H
V
˙
O
2
est
Duck Sex (g) (mlkg
−1
min
−1
) (beatsmin
−1
) (mlkg
−1
min
−1
) ∆
1 F 1646 29.5 162 34.4 16.6
2 M 2293 32.2 164 34.7 7.8
3 F 1505 27.1 128 29.3 8.1
6 M 2300 41.9 216 42.5 1.4
10 M 1530 24.2 98 24.8 2.5
11 F 1510 32.7 120 28.1 −14.1
Mean 1797±159 31.3±2.5 148±17 32.3±2.6 3.7±4.2
Absolute mean ∆ 8.4
V
˙
O
2
est
, estimated V
˙
O
2
.
Mean vales are ±
S.E.M.
∆, Difference between measured and estimated V
˙
O
2
, expressed as a percentage of the measured value.
Absolute mean ∆, mean ∆, ignoring the sign of the error.
For the paired t-test between V
˙
O
2
and V
˙
O
2
est
: t=0.769, P>0.2.
Table 5. Estimates of oxygen consumption (V
˙
O
2
) obtained for six eider ducks over 2 days, using the doubly labelled water (DLW)
technique and five different equations
Mass N
O
N
H
Equation*
Bird (g) (mol) (mol) N
H
/N
O
kO/kH (ml kg
−1
min
−1
) L&M 35 S A6 S 4 S 3 S i
1 1646 58.94 60.22 1.02 1.32 29.5 49.4 47.2 44.8 45.3 52.6
2 2293 76.68 80.81 1.05 1.25 32.2 25.2 24.1 22.6 22.8 27.3
3 1505 59.11 60.45 1.02 1.61 27.1 24.9 23.8 22.8 23.1 25.6
6 2300 72.65 74.98 1.03 1.22 41.9 39.1 37.4 34.8 35.1 42.9
10 1530 64.93 68.34 1.05 1.56 24.2 41.5 39.9 38.3 38.7 42.9
11 1510 60.30 64.33 1.07 1.56 32.7 8.7 8.4 8.1 8.1 8.9
Mean 1797±159 65.44±3.10 68.19±3.39 1.04±0.01 1.42±0.07 31.3±2.5 31.5±6.0 30.1±5.7 28.6±5.4 28.9±5.5 33.4±6.4
Algebraic mean ∆ 4.9 0.4 4.6 3.6 10.8
Absolute mean ∆ 41.5 41.2 41.3 41.5 41.9
Mean values are ±
S.E.M.
Algebraic mean ∆, mean difference between measured and estimated V
˙
O
2
(∆) expressed as a percentage of the measured value.
Absolute mean ∆, mean ∆, ignoring the sign of the error.
N
O
, oxygen dilution space; N
H
, hydrogen dilution space; kO/kH, isotope elimination rate ratio.
*Five equations were used to convert isotope enrichments (p.p.m.) to V
˙
O
2
: L&M 35, equation 35 from Lifson and McClintock (1966); S A6,
equation 6 from Schoeller et al. (1986); S 4, equation 4 from Speakman (1993); S 3, equation 3 from Speakman et al. (1993); S i, equation i
from Speakman (1997).
V
˙
O
2
2827Heart rate and oxygen uptake in exercising eider ducks
Bonferroni correction, Table 6). The estimate produced by
equation 6 from Schoeller et al. (1986) had the lowest algebraic
mean difference from measured V
.
O
∑ (Table 5), but none of the
estimates using any of the equations was significantly different
from the measured V
.
O
∑ (0.052<t<0.792 for all comparisons;
Bonferroni t critical value for P=0.05 is 2.750).
Comparison between the two methods and indirect
calorimetry
Measured V
.
O
∑ values were compared with estimates
calculated using f
H
and equation 6 from Schoeller et al. (1986),
which provided the estimate with the lowest algebraic mean
error of the five equations used to estimate V
.
O
∑ (Table 5).
Because of the substantial range of errors within each method,
there was no significant difference between values of V
.
O
∑
obtained by respirometry, DLW or f
H
(P>0.2 following
Bonferroni correction, 0.354<t<0.954 for all three
comparisons; Bonferroni t-critical value for P=0.05 is 2.694).
Heart rate during voluntary dives
The dive cycle
Dives lasted for a mean duration of 15.9±0.7s (N=63). Dive
durations ranged from 4.3 to 26s; most dives were less than
21s in duration. Surface intervals ranged from 0.7 to 40.8s,
with a mean of 8.9±0.8s (N=60). The mean dive/surface cycle
lasted 24.8±1.3s (N=60).
Heart rate
Heart rate was recorded during a bout of 63 dives (N differs
at each time point due to variable dive durations and radio
interference). Pre-dive f
H
10s before submersion was
243±27beatsmin
−1
(N=7), which was significantly greater
than the mean value of 132±3beatsmin
−1
(N=3) recorded
while the duck (individual 1) was resting on water (Fig. 4;
t=4.08, P=0.01). The highest f
H
before diving was recorded 1s
before immersion of the duck’s head (310±6beatsmin
−1
,
N=62, 2.3 times resting f
H
). The lowest mean f
H
during diving
was recorded 0.5s after immersion (194±5beatsmin
−1
, N=63,
1.5 times resting f
H
).
Heart rate then increased over the next 7s, before falling
slightly and stabilising at 239±6beatsmin
−1
(N=50) at mean
dive duration, which was significantly greater than the mean
f
H
of 216±5beatsmin
−1
(N=6) recorded while the duck was
swimming at speeds of 1.1–1.3ms
−1
in a water channel
(t=2.94, P<0.01). Heart rate had already begun to increase 5s
before surfacing, and the highest f
H
recorded after her head
broke the surface was 340±4beatsmin
−1
, N=63, 2.6 times
resting on water f
H
value. This was significantly higher than
the highest pre-dive f
H
value (t=4.16, P<0.01).
Heart rate 10s after emersion (260±25beatsmin
−1
, N=7)
was still significantly higher than the resting value on water
(t=5.08, P<0.001). Only two pauses between dives were long
enough to include heart rates 15 and 20s after surfacing. Mean
f
H
over a whole dive cycle (a dive and the interval after it) was
259±10beatsmin
−1
(N=60).
Table 6. Results of pairwise comparisons between different
equations for estimating V
˙
O
2
using the DLW technique
Group 1 Group 2 t-statistic Significance
L&M S A6 5.250 *
L&M S 4 4.798 *
L&M S 3 4.766 *
L&M S i 3.304 *
S A6 S 4 4.275 *
S A6 S 3 3.979 *
S A6 S i 4.102 *
S 4 S 3 0.478
S 4 S i 4.160 *
S 3 S i 4.079 *
The Bonferroni t critical value for P=0.05 is 3.070; * denotes a
significant difference between two means.
See Table 5 for identification of equations.
3
4
7
21
45
62
62
55
44
24
17
15
33
50
61
43
28
7
2
2
0
50
100
150
200
250
300
350
400
-20 -15 -10 -5 0 5 10
Time (s)
f
H
(beats min
-1
)
-5 0 5 10
15 20 25
Fig. 4. f
H
(beatsmin
−1
) during
voluntary dives by a female
eider duck (individual 1).
Values are means ±
S.E.M.
Numbers above points indicate
N; where no number is given,
N=63. The instants of
immersion and emersion are
shown by the downward and
upward pointing arrows,
respectively. The upper
horizontal line is mean f
H
for that individual while
swimming at maximal speeds
(between 1.1 and 1.3ms
−1
;
216±5beatsmin
−1
; N=6) and
the lower line is resting f
H
on
water for that individual duck
(132±3beatsmin
−1
; N=3). The
dashed lines are ±1
S.E.M
2828
Oxygen consumption
The previously derived common relationship between f
H
and
V
.
O
∑ was used to estimate V
.
O
∑ during diving. Mean f
H
over the
dive/surface cycle (259±10beatsmin
−1
, N=60) was substituted
into equation 3 above, which produced an estimated mean V
.
O
∑
value of 49.0±1.5mlkg
−1
min
−1
.
Discussion
Resting
The mean resting V
.
O
∑ recorded from eider ducks in the
present study (12.8mlkg
−1
min
−1
, Table 1) is similar to the
values obtained by substituting the mean body mass of 1.79kg
into the predictive equation for members of the anseriforms in
Table 2 from Zar (1969) (13.2mlkg
−1
min
−1
for a resting bird)
and Grubb (1983) (12.24mlkg
−1
min
−1
for any resting bird).
The equations given in Bennett and Harvey (1987, p. 339)
predict the lowest resting V
.
O
∑ of 11.7mlkg
−1
min
−1
, which
approximated the mean for one bird in the present study.
The mean resting RQ in the eider duck was 0.63±0.06, but
the lowest individual RQ was 0.51, in duck 6. Nolet et al.
(1992) also reported low respiratory exchange ratios in
barnacle geese (mean 0.67±0.02, N=5). However,
comparatively low RQ values between 0.6 and 0.7 are thought
to be normal in birds (King, 1957), perhaps due to incomplete
oxidation of fat and nonpulmonary carbon dioxide loss (Chaui-
Berlinck and Bicudo, 1995; Walsberg and Wolf, 1995), and
this may also have explained the very low RQ values in some
of the eiders.
Swimming
The exponential increase in f
H
and V
.
O
∑ with swimming speed
(Fig. 1) has also been described in other anseriforms such as
the barnacle goose (Nolet et al., 1992), tufted duck (Woakes
and Butler, 1983; Butler and Turner, 1988) and mallard Anas
platyrhynchos (Prange and Schmidt-Nielsen, 1970). When
swimming at their maximum sustainable speed, the mean
aerobic scope (V
.
O
∑
max
/V
.
O
∑
rest
) of the eiders was 4.3 (Tables 1,
2). This is comparable with that of other swimming
anseriforms, as aerobic scopes have been recorded of 4.1 for
the mallard (Prange and Schmidt-Nielsen, 1970), 3.5 for the
tufted duck (Woakes and Butler, 1983), 3 for Anas superciliosa
(Baudinette and Gill, 1985) and 4.9 for the barnacle goose
(Nolet et al., 1992).
Running
A linear increase in V
.
O
∑ with running has been observed in
all species of bird examined to date (Brackenbury, 1984)
including gentoo penguins Pygoscelis papua (Bevan et al.,
1995c), barnacle geese (Nolet et al., 1992) and black-browed
albatross Diomedea melanophrys (Bevan et al., 1994). At
maximum running speed, V
.
O
∑
max
/V
.
O
∑
rest
was 3.0, while mean f
H
increased by a factor of 2.1 (Tables 1, 2). Although the ducks
appeared to be running as fast as was possible, their oxygen
uptake was not elevated by as much as it was at maximum
swimming speed. V
.
O
∑ and f
H
were significantly higher over the
entire range of attainable speeds on the treadmill than on the
flume, but heart rate was elevated relatively more than V
.
O
∑,
which may have contributed to the significant differences
between regression equations 1 and 2. This effect may have
been due to a f
H
increase that was not accompanied by a
corresponding increase in V
.
O
∑ (‘additional’ heart rate), which is
taken as an indicator of psychological activation and emotional
states (Blix, 1974; Deroanne and Pirnay, 1978). Prolonged
running is not a natural activity of the eider duck.
Calibration
The individual regressions of V
.
O
∑ on f
H
had correlation
coefficients ranging from 0.29 to 0.84 (Table 3). There are
several sources of variation in the relationship between V
.
O
∑ and
f
H
. Psychogenic factors such as stress and social interactions
elevate f
H
(Owen, 1969; Eisermann, 1992), and metabolism
varies diurnally and seasonally (Gessaman, 1980). The shapes
and slopes of linear regressions of V
.
O
∑ on f
H
vary between
individuals and within the same animal at different times
(Morhardt and Morhardt, 1971; Woakes and Butler, 1983) or
when undertaking different forms of exercise (present study,
regression equations 1 and 2). The significant but inconsistent
differences between the slopes and intercepts of the regressions
obtained by swimming and running eider ducks have not been
reported previously in other species of bird. No significant
differences were found in the relationships between V
.
O
∑ and f
H
obtained by walking and swimming gentoo penguins (Bevan
et al., 1995c), and few differences were observed between
regressions obtained from barnacle geese using these two
methods (Nolet et al., 1992).
The ducks used in the present study were hand-reared in an
attempt to minimise ‘additional’ heart rate, but it still remains
a possibility that this is included in data obtained from some
individuals while running on the treadmill or from nervous
ducks such as individual 4. Heart rate depends on a variety of
physiological and psychological factors, apart from the level
of exercise that the animal is undergoing (Blix, 1974;
Gabrielsen et al., 1977). The variety of V
.
O
∑/f
H
relationships that
occur in this study and in the literature emphasises the need to
keep animals as calm and unstressed as possible, so that the
effect of ‘additional’ f
H
can be at least kept to a minimum and
the well-being of the animals improved.
Validation
There was wide variation between the slopes and intercepts
of the individual regressions of V
.
O
∑ on f
H
in the present study,
and the 95% confidence intervals of the mean estimate of V
.
O
∑
were ±6.26mlkg
−1
min
−1
, which represents a large proportion
(19%) of the mean (32.3mlkg
−1
min
−1
). This is relatively high
in comparison with the albatrosses studied by Bevan et al.
(1994), for which the confidence intervals were 6% of the
mean estimated rate of oxygen consumption. However, the
pooled common regression (equation 3, r
2
=0.46, P<0.0001)
provided an accurate estimate of mean V
.
O
∑ in the validation
experiments, as has been found in previous studies on other
species (e.g. Nolet et al., 1992; Bevan et al., 1994, 1995b,c).
P. A. J. HAWKINS AND OTHERS
2829Heart rate and oxygen uptake in exercising eider ducks
In agreement with many other validation studies of the DLW
method (reviewed in Speakman, 1997, 1998), the arithmetic
mean deviation across the group of birds was close to the
reference mean determined by indirect calorimetry (<5%
difference), and was independent of the calculation method
used. The best fit in this instance was provided by the Schoeller
et al. (1986) equation A6, which is a two-pool model equation.
Previous studies on mammals have indicated that the two-pool
model equations are most appropriate for larger animals
(>5kg; Speakman, 1990, 1997); recent validations in large
birds (i.e. bald eagles Haliaeetus leucocephalus weighing
4.23kg; Dykstra et al., 1997) have confirmed that the single-
pool model provides a better fit than two-pool equivalents. A
previous validation in tufted ducks (Bevan et al., 1995a)
weighing on average 0.63kg also concluded that a single-pool
model equation provided the best fit to the reference method
data, but for barnacle geese (Nolet et al., 1992) weighing
1.78kg, the best fit was provided by a two-pool calculation.
This may indicate that the transition of superiority between
single- and two-pool models occurs at a lower body mass in
anseriforms than in other birds or mammals, but further
validation is necessary to confirm this suggestion. Since two-
pool model calculations provide lower estimates of energy
demands than the single-pool model equations, this might have
important implications for calculation of energy flows in wild
anseriform birds.
Although the accuracy of the DLW method was normally
better than 5% on average across the group of birds, the
individual estimates were considerably more discrepant. This
has also been reported previously both in ducks (Bevan et al.,
1995b) and in other species (e.g. Speakman and Racey, 1988),
including man (Schoeller et al., 1986). Since individual
deviations can be large, our observations confirm that this
method is best suited to measurement of average energy
demands across groups of animals, as has been previously
emphasised (Speakman, 1998).
In the few validation studies that have been performed using
active animals, the f
H
method for predicting energy
expenditure has thus proved to be as accurate as the DLW
method and to provide less variable mean estimates, if data are
obtained from a sufficient number of animals and the
relationship between the two variables is properly calibrated
(Nolet et al., 1992; Bevan et al., 1994, 1995b,c). The f
H
method
is also advantageous in that within-day energy expenditure
during different activities can be estimated, although there may
be a reduction in accuracy over very short time scales (Bevan
et al., 1995c). Heart rate (and body temperature, if a thermistor
is fitted; Woakes et al., 1995) can be monitored for periods of
up to a year, which makes this an accurate and useful technique
for long-term field studies.
Diving behaviour and heart rate
The duck was seen to inhale and exhale deeply two or three
times before each dive, then exhale immediately before diving.
She lunged forward and under the water, pulling herself under
with half-folded wings, and dived to the bottom of the tank by
beating the (still partly folded) wings and stroking with the
feet, which beat simultaneously. Ascent was entirely passive;
the duck stopped beating her wings and feet and floated to the
surface. This resembled the diving behaviour of the common
eider duck observed by Humphrey (1958).
In the tufted duck, tachypnoea before submersion is
associated with tachycardia and occurs in anticipation of diving
behaviour (Butler and Woakes, 1979). Although respiratory
frequency was not measured in the present study, the eider
would have needed to load her oxygen stores before a diving
bout (Woakes and Butler, 1983; Butler and Woakes, 1984) and
remove accumulated CO
2
between dives, and was seen and
heard to take deep breaths before diving. Like the common
eider in the present study, the tufted duck also exhales on
submersion, possibly to reduce buoyancy and thus energetic
costs (Butler and Woakes, 1979).
The changes in f
H
during free dives to 1.7m recorded in the
female common eider in the present study were qualitatively
similar to those recorded previously in free dives by the tufted
duck (Butler and Woakes, 1979; Woakes and Butler, 1983;
Stephenson et al., 1986; Keijer et al., 1988; Bevan and Butler,
1992), Pekin duck Anas platyrhynchos (Gabrielsen, 1985),
cormorant Phalacrocorax carbo and Canada goose Branta
canadensis (Kanwisher et al., 1981). Heart rate began to
decrease before the moment of submersion, with a minimum
value of 194±5beatsmin
−1
recorded 0.5s after immersion of
the beak, then increased following submersion, stabilising in
the latter part of the dives. Mean f
H
at mean dive duration was
significantly greater than that while swimming at maximum
sustainable surface speeds of 1.1–1.3ms
−1
(cf. Butler and
Woakes, 1979; Kanwisher et al., 1981; Woakes and Butler,
1983; Gabrielsen, 1985). This result suggests that the cardiac
response to voluntary (shallow) diving in the common eider
may be similar to that for exercise in air, as has been proposed
for other species of diving duck (Butler, 1982). The relatively
higher f
H
during voluntary dives in comparison with Aythya
spp. may occur because the pectoral muscles are active in the
eider, whereas the tufted duck and pochard use the feet alone
(Butler and Woakes, 1979).
Oxygen consumption and dive duration
Although free-ranging animals are not always in a steady
state, particularly diving animals such as the common eider,
there is a systematic relationship between V
.
O
∑ and f
H
if the
latter is averaged over a dive/surface cycle (Woakes and
Butler, 1983; Bevan et al., 1992; Butler, 1993). The estimated
mean V
.
O
∑ over the dive cycle of 49.0±1.5 mlkg
−1
min
−1
is 1.8
times that individual bird’s mean resting V
.
O
∑ on water, which
is comparable with the twofold mean increase in V
.
O
∑
measured over an entire dive cycle in the tufted duck (Bevan
et al., 1992). When the eiders in the present study swam at
maximum speeds on the surface of a water channel, mean V
.
O
∑
was 55.5±3.6mlkg
−1
min
−1
, which is not significantly
different from the estimated V
.
O
∑ during diving to 1.7m
(t=2.87, P=0.1, t test for a predicted y value, Zar (1984)
p. 275). It should be noted, however, that buoyancy is the
2830
dominant force against which ducks initially work while
descending and that work against buoyancy decreases with
depth (Stephenson et al., 1989; Stephenson, 1994). The mean
diving V
.
O
∑ and f
H
values estimated in the present study
cannot, therefore, be extrapolated to deeper depths.
Keijer and Butler (1982) calculated that the maximum
usable tissue oxygen store for a tufted duck is 41.5mlkg
−1
.
Assuming that tissue oxygen stores are similar for the common
eider and substituting the estimated mean diving V
.
O
∑ value of
49.0mlkg
−1
min
−1
, the maximum dive duration during which
metabolism would be aerobic (i.e. the aerobic dive limit, ADL)
would be 51s for the bird in the present study. The dives
observed in the present study were all well within the estimated
ADL, as none exceeded 26s. Although the prediction of ADL
in the present study makes assumptions about diving V
.
O
∑ and
O
2
stores in the eider, it appears likely that this species does
not exceed its ADL in the field when making relatively shallow
dives, which conforms to foraging strategies observed in
animals diving mainly for sedentary or sessile prey
(Guillemette et al., 1992).
The authors would like to thank BBSRC for funding
P.A.J.H. We acknowledge the technical assistance of Peter
Thomson for isotope analysis and thank Dr Mike Harris for
enabling us to acquire the eggs. Special thanks to the ducks,
Stephanie, Trojan, Fiona, Sappho, Hector, Nigel, ZaZa,
Nightshade, Roger and Gribble, without whom this study
would not have been possible.
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