The heart rate/oxygen consumption relationship during cold exposure of the king penguin: a comparison with that during exercise
1 School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15
2TT, UK
2 Centre d'Ecologie et Physiologie Energétiques, CNRS, 23 rue
Becquerel, 67087 Strasbourg Cedex 02, France
3 Laboratoire de Thermorégulation et Energétique de
l'Exercice, CNRS, Faculté de Médecine Lyon-Nord, 69373 Lyon
Cedex 08, France
* Author for correspondence (e-mail: p.j.butler{at}bham.ac.uk )
Accepted 20 May 2002
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Summary |
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Key words: heart rate, oxygen consumption, penguin, Aptenodytes patagonicus, exercise, metabolic rate, foraging, fasting, body condition, thermoregulation, oxygen pulse
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Introduction |
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![]() | (1) |
An increasing number of studies have investigated the relationship between
fH and
O2 (Bevan et
al., 1994
,
1995
;
Nolet et al., 1992
;
Boyd et al., 1995
;
Butler et al., 1995
;
Hawkins et al., 2000
;
Froget et al., 2001
;
Green et al., 2001
). In most
of these studies, exercise (running or swimming) was used to increase both
metabolic rate and fH. However, several factors have been found to
influence the relationship between fH and
O2, such as the
type of activity (Nolet et al.,
1992
; Butler et al.,
2000
), variation in body condition
(Froget et al., 2001
) or even
season (Holter et al.,
1976
).
Antarctic penguins are regularly faced with two thermal challenges
(exposure to cold wind on land and diving in cold sea water). Indeed, at
Possession Island, Crozet Archipelago, our research site, the climate is cold
(5°C annual average, -3°C in winter and +7°C in summer), wet (mean
rainfall 247 cm year-1) and windy (mean wind speed 45 km
h-1 with blasts attaining 180 km h-1). Thus, the
apparent temperature, using the equation from Siple and Passel
(1945) for wind-chill effect
on an animal, is on average -18°C in winter and +4°C in summer. This
environmental variation is likely to influence metabolic rate.
In a previous study, Froget et al.
(2001) found that the
relationship between heart rate and the rate of oxygen consumption obtained
for king penguins walking on a treadmill was affected by the body condition of
the animal. They concluded that the best estimate of the rate of oxygen
consumption was obtained by relating the OP to the body condition of the bird
and multiplying this by fH. Thus, in the present study, we compared
the relationship between fH and
O2 obtained by
exposing king penguins to environmental temperatures that exceeded the average
range routinely experienced in the field with that obtained in the previous
study of king penguins walking on a treadmill.
The aims of the present study were therefore (i) to investigate whether
exposure to low ambient temperature could be used as an alternative to
exercise for calibrating fH against
O2 for
subsequent use in free-ranging animals and (ii) to establish the relationship
between
O2, body
temperature and ambient temperature and to determine the lower critical
temperature (LCT) of adult king penguins.
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Materials and methods |
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In 1997-1998, 22 breeding king penguins were captured. As king penguins are
less likely to desert their nest while brooding a small chick, males were
captured either at the beginning or the end of their third foraging trip and
females at the beginning or the end of their second foraging shift (see
Fig. 1 in
Froget et al., 2001). Sex was
determined either by the song (Jouventin,
1982
) or by the behaviour (such as mating or egg-laying). All
birds were weighed, and measurements of their flipper size, bill length and
foot length to +1 mm were taken according to standard techniques
(Stonehouse, 1960
). At the end
of the experiment, each bird was weighed to ±20 g, and the stomach
contents of the bird were retrieved using the `water off-loading technique'
(Wilson, 1984
).
|
A nutritional index (NI) was then calculated using equations 3 and 4 from
Froget et al. (2001):
![]() | (2) |
In 1999-2000, nine king penguins were captured using the protocol described
above. The only difference from the 1997-1998 experiment was that the stomach
contents of the bird were retrieved before the experiment to obtain a better
estimate of the body mass and the NI
(Froget et al., 2001). The
bird was rested overnight prior to being placed in the respirometer. The bird
was then re-fed before its release.
Equipment
Each bird was equipped with an externally mounted pulse-interval-modulated
heart rate radio transmitter (Woakes and
Butler, 1975) or heart rate data logger in 1999-2000
(Woakes et al., 1995
). Both
were the same size and mass (4.5 cmx2.5 cmx0.6 cm and 15 g). Each
transmitter or logger had electrode leads made of stainless-steel wire which
terminated with hypodermic needles. In situ, the maximum distance
between the two electrodes was 37 cm. The body of the transmitter or logger
was wrapped in insulating foam and covered with Tesa tape (Beierdorsf AG,
Germany) for protection from attacks by the bird. The electrodes were placed
subcutaneously in a dorsal, midline position. One electrode was placed level
with the heart and the other in a more caudal location. This arrangement
provided a good electrocardiogram (ECG) signal. The body of the transmitter or
logger was attached to the back feathers using Tesa tape
(Bannasch et al., 1994
). The
transmitter or logger was externally mounted rather than implanted to avoid
any post-operative recovery time.
Rate of oxygen consumption was measured in an opencircuit system
(Fig. 1) similar to that
described by Barré and Roussel
(1986). The penguin was placed
in a thermostatic chamber with its head enclosed in an opaque respiratory hood
connected to the open-circuit flow for measurement of the rates of
O2 consumption and CO2 production. The hood was
ventilated with a constant airflow of approximately 24 l min-1,
measured using a digital flowmeter (Platon, model 2044). A sub-sample of the
outlet airflow was passed, via a drying agent (Silica gel), to a
paramagnetic oxygen analyser (Servomex 1100) and then to an infrared carbon
dioxide analyser (Servomex 1410B). Data were recorded on a PC using the
Labtech-Notebook software. The O2 and CO2 analysers were
calibrated before each experiment using oxygen-free nitrogen, atmospheric air
and a calibrating gas of 5% CO2 in N2. The signal from
the externally mounted transmitter was detected by a receiver (International
877R) and converted to an ECG by a decoder
(Woakes and Butler, 1975
). The
ECG was directed to a chart recorder (Graphtec). Heart rate was calculated by
counting the number of QRS waves of the ECG over 3 min.
In 1999-2000, the same system was used but, to determine whether the flow
rate had not been too low in 1997-1998, the airflow circulating through the
hood was higher, at approximately 45 l min-1. There were no
differences in measured
O2 between the
two years. Heart rate was recorded in the data logger every 2 s and later
downloaded to a computer for analysis.
Experimental protocol
After being equipped with a radio transmitter or data logger, the penguin
was placed in a container in the thermostatic chamber at 10°C and left
resting for at least an hour. Ambient temperature (Ta) was
then randomly varied between -30 and +10°C (with an increment of
approximately 5°C). The penguin was left at the chosen temperature for at
least 30 min or until steady-state conditions had been achieved (i.e.
stabilisation of the gas concentrations in the respirometer). Heart rate was
then recorded on a chart recorder over a 3 min period (for the birds of the
1998-1999 experiment). Each bird was exposed to at least nine different
temperatures. During all the experiments, the bird was resting while standing
in the container. In 1999-2000, body temperature was measured using a
thermistor (accuracy ±0.2°C) that was `ingested' by the bird, and
the connecting lead was fixed with Tesa tape at the opening of the bill. The
thermistor probe was located approximately 30 cm into the digestive tract.
Data analysis
Calculation of rate of oxygen consumption
The rate of oxygen consumption was calculated from the gas concentration
using the equation derived from Depocas and Hart
(1957) as modified by Withers
(1977
):
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Statistical analyses
All statistical tests were performed using the statistical package MINITAB
12.22 for Windows (Minitab Inc.). All values are presented as mean ±
S.E.M. The relationship between heart rate and the rate of oxygen consumption
was determined using least-squares regression. Regression equations were
compared using an analysis of variance general linear model (GLM, as reviewed
in Zar, 1999). Student's
t-tests were used to compare the significance of any difference
between the means of two populations. One-way analysis of variance (ANOVA)
with Tukey's HSD post-hoc testing was used when more than two
populations were compared. Results were considered significant at
P<0.05.
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Results |
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There were no significant differences in fH and mass-specific
O2
(s
O2) between
the two years (Fig. 3, multiple
comparisons with an unbalanced nested design: F1,17=1.91,
P=0.17; F1,17=1, P=0.32;
F1,17=0.05, P=0.82, respectively). It was
therefore possible to pool all the data from the two years.
|
Metabolic response to varying ambient temperature
According to the classic model for heat loss
(Scholander et al., 1950), the
relationship between
s
O2 and
Ta is expressed by two linear regression lines that
intersect at the lower critical temperature (LCT). The LCT is defined as the
lowest temperature in the thermoneutral zone and was determined from the
pooled data of the 31 king penguins by using the least-squares method
(Zar, 1999
). The mean
s
O2 at 10°C
was 10.5±0.46 ml min-1 kg-1; between 10°C and
-5°C, s
O2
remained relatively constant (at 10.6±1.52 ml min-1
kg-1). Between -5 and -31°C,
s
O2 increased
significantly to 18.5±0.57 ml min-1 kg-1
(Fig. 4). The linear regression
equations (equations 4 and 5), for the relationship between
s
O2 and ambient
temperature are as follows.
|
Between 10 and -5°C:
![]() | (4) |
![]() | (5) |
The lines for these two equations intersect at -4.9°C, which is taken to be the lower critical temperature.
Exercise versus temperature to calibrate heart rate against
O2
Although the range of fH (from 66 to 204 beats min-1)
for birds exposed to varying ambient temperatures was similar to that obtained
for birds resting and walking on a treadmill (57-189 beats min-1;
Froget et al., 2001), the
range of
O2
during cold exposure (82.8-314.6 ml min-1) was closer to that
obtained for birds resting within their thermoneutral zone (62.6-225.2 ml
min-1) than to that for birds exercising on the treadmill
(127.1-563.0 ml min-1; Froget
et al., 2001
). There was a significant positive relationship
between fH and
O2, but this was
significantly different from that obtained from birds walking on a treadmill
(Fig. 5).
|
The oxygen pulse was calculated above and below the LCT. There was a small but significant increase in the oxygen pulse between that measured at thermoneutrality and that measured for temperatures lower than the LCT (from 1.23±0.06 to 1.47±0.07 ml O2 beat-1; paired t-test, t=9.72, N=31, P<0.001).
There was a significant correlation between the nutritional index (NI) and
the oxygen pulse above or below the LCT. However, an analysis of covariance
(Zar, 1999) showed that there
was no significant difference in the slopes and the intercepts between the
equation obtained using the OP above the LCT and that obtained using the OP
below the LCT. It is then possible to use a common regression
(r2=0.32, P=0.015,
Fig. 6):
![]() | (6) |
|
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Discussion |
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The fH/O2
relationship and cold exposure
Although most previous relationships between fH and
O2 have been
obtained by exposing animals to different levels of activity
(Nolet et al., 1992
; Bevan et
al., 1994
,
1995
;
Hawkins et al., 2000
;
Froget et al., 2001
;
Green et al., 2001
), in some
studies (e.g. Morhardt and Morhardt,
1971
), a large range of fH and
O2 values were
obtained by exposing the animals to a variety of temperatures. Froget et al.
(2001
) established the
relationship between OP and NI for king penguins walking on a treadmill. Two
equations were derived depending upon whether the animal was active or
resting. Using an analysis of covariance
(Zar, 1999
) to compare the
relationship between OP and NI obtained in the present study (equation 6) and
that between resting oxygen pulse (ROP) and NI from penguins resting on a
treadmill (Ta=15 °C, range 7 to 20 °C; equation 8
in Froget et al., 2001
), we
established that there was no significant difference between the slopes of the
two equations (F1,39=2.96; P=0.0904):
![]() | (10) |
|
This suggests that, in king penguins, the use of reduced environmental
temperature to calibrate fH against
O2 is
inappropriate if the relationship is to be used for different levels of
activity, but should still be employed to estimate the metabolic rate of
penguins resting on sea water and on land. In other words, cold exposure
simply extends the range of resting fH and
O2 values. This
study confirms the influence of body composition (NI) on the
fH/
O2
relationship. Rates of energy consumption estimated from fH for king
penguins resting on sea water or at varying ambient temperature are in
agreement with values taken from the literature.
A major difference between walking on a treadmill and swimming in penguins
is that the birds do not use the same musculature for both activities: they
use their pectoral muscles during swimming and their leg muscles during
walking. Previous studies, on non-diving birds, showed that the OP could
differ depending on the muscle mass engaged in the activity (an increase in OP
from walking to flying in barnacle geese;
Nolet et al., 1992;
Butler et al., 2000
). However,
in gentoo penguins Pygoscelis papua, Bevan et al.
(1995
) found no significant
difference in the relationship between fH and
O2 during
swimming and walking.
Finally, while walking on a treadmill, king penguins are exposed to an unnatural situation, that is performing sustained intense exercise in their thermoneutral zone (or maybe sometimes above it). Thus, they have to face an extra challenge, the elimination of exercise-generated heat. While at sea, the elimination of exercise-generated heat is eased because the thermal conductance of water is 25 times that of air.
Thus, to use fH as an indicator of
O2 with more
confidence in free-ranging king penguins, the relationship between fH
and
O2 should be
calculated for animals resting at different temperatures (this study), while
walking (Froget et al., 2001
)
and perhaps also while swimming both at the surface and when submerged. It
would also be useful to perform experiments that associate thermoregulation
and activity; i.e. walking or swimming at different temperatures, although it
is possible that endotherms could use the `wasted' heat produced during
exercise, at least partly, to offset the costs of thermoregulation if the
animals are below their LCT (Butler and
Jones, 1982
; Handrich et al.,
1997
).
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Acknowledgments |
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