Heart rate and energetics of free-ranging king penguins (Aptenodytes patagonicus)
1 School of Biosciences, University of Birmingham, Edgbaston, Birmingham,
B15 2TT, UK
2 Centre d'Écologie et Physiologie Énergétiques, Centre
National de la Recherche Scientifique, 23 rue Becquerel, 67087 Strasbourg
cedex, France
* Author for correspondence (e-mail: P.J.Butler{at}bham.ac.uk)
Accepted 9 August 2004
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Summary |
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An implanted data logger enabled fH and diving
behaviour to be monitored from 10 free-ranging king penguins during their
breeding period. Using previously determined calibration equations, it was
possible to estimate rate of oxygen consumption
(O2) when the
birds were ashore and during various phases of their foraging trips. Diving
behaviour showed a clear diurnal pattern, with a mixture of deep (>40 m),
long (>3 min) and shallow (<40 m), short (<3 min) dives from dawn to
dusk and shallow, short dives at night. Heart rate during dive bouts and dive
cycles (dive + post-dive interval) was 42% greater than that when the birds
were ashore. During diving, fH was similar to the `ashore'
value (87±4 beats min1), but it did decline to 76% of
the value recorded from king penguins resting in water. During the first hour
after a diving bout, fH was significantly higher than the
average value during diving (101±4 beats min1) and
for the remainder of the dive bout.
Rates of oxygen consumption estimated from these (and other) values of
fH indicate that when at sea, metabolic rate (MR) was 83%
greater than that when the birds were ashore [3.15 W kg1
(0.71, +0.93), where the values in parentheses are the computed
standard errors of the estimate], while during diving bouts and dive cycles,
it was 73% greater than the `ashore' value. Although estimated MR during the
total period between dive bouts was not significantly different from that
during dive bouts [5.44 W kg1 (0.30, +0.32)], MR
during the first hour following a dive bout was 52% greater than that during a
diving bout. It is suggested that this large increase following diving
(foraging) activity is, at least in part, the result of rewarming the body,
which occurs at the end of a diving bout. From the measured behaviour and
estimated values of
O2, it was
evident that approximately 35% of the dives were in excess of the cADL. Even
if
O2 during
diving was assumed to be the same as when the birds were resting on water,
approximately 20% of dives would exceed the cADL. As
O2 during diving
is, in fact, that estimated for a complete dive cycle, it is quite feasible
that
O2 during
diving itself is less than that measured for birds resting in water. It is
suggested that the regional hypothermia that has been recorded in this species
during diving bouts may be at least a contributing factor to such
hypometabolism.
Key words: diving metabolism, foraging, heart rate, aerobic dive limit, king penguin, Aptenodytes patagonicus, seabird
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Introduction |
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King penguins breed and forage in the Antarctic Ocean, where primary and
secondary productions are high (Huntley et
al., 1991). Information on their energy expenditure and thus food
consumption can be used in models of energy flux within the ecosystem
(Croxall et al., 1999
) or for
inclusion within fisheries models
(Croxall, 1984
). To date,
estimates of the field metabolic rate (FMR) have been made using data obtained
either from captive birds in a metabolic chamber or in a water channel
(Culik et al., 1996
), or from
free-ranging birds using the timeenergy budget (TEB) and the doubly
labelled water (DLW) methods (Kooyman et
al., 1992a
).
However, although DLW is still widely used to measure FMR
(Speakman, 1998), it does not
enable the determination of energetic costs associated with specific
activities, without a detailed time budget
(Butler et al., 2004
). Heart
rate (fH) has been proposed as an alternative indicator of
the rate of oxygen consumption
(
O2;
Butler, 1993
). This technique
has already been successfully used to monitor continuously the rate of energy
expenditure in several species (Bevan et al.,
1995
,
2002
;
Boyd et al., 1999
;
Green et al., 2003
). The
advantages of this technique include a monitoring period of up to several
months (Woakes et al., 1995
),
and the recorded fH can be divided into small time units
to allow the investigation of energetic costs of integrated behaviour
categories, such as foraging at sea and incubating ashore. In the present
study, miniature implantable data loggers for simultaneous recording of depth
and fH were utilised.
Froget et al. (2001)
presented three models for estimating
O2 of
free-ranging king penguins and two of these involved the use of oxygen pulse
(OP, the amount of oxygen consumed per heart beat). OP during rest (ROP) and
during activity (AOP) were used according to the activity state of the birds.
However, it is known that AOP is not usually constant over a range of activity
levels (Butler, 1993
), and it
is now known that ROP is different between birds resting in air (i.e. when
ashore) and resting in water (i.e. when at sea;
Fahlman et al., 2004
). Thus,
the primary aim of the present study was to record fH and
diving behaviour of free-ranging king penguins and, using the appropriate
equation from Fahlman et al.
(2004
), to estimate the energy
expenditure of the birds during the different phases of the foraging and
incubating shifts. From these, it was expected to shed new light on the `king
penguin's enigma' (Culik et al.,
1996
), which is that `king penguins seem to swim too fast and dive
for too long, and too often, to be in agreement with our physiological models
of diving' (Kooyman et al.,
1992a
).
Indeed, the aerobic dive limit (ADL) or diving lactate threshold (DLT),
defined as the diving duration beyond which there is an increase in post-dive
plasma lactate concentration (Kooyman,
1989; Butler and Jones,
1997
) has not yet been measured in free-ranging king penguins.
Thus a calculated ADL (cADL, which is the dive duration during which all
usable oxygen would be exhausted; Kooyman,
1989
) is often used as an indicator of the DLT. Previous
estimations of the cADL at 2 min for king penguins
(Kooyman et al., 1992a
;
Culik et al., 1996
) imply that
45% of all dives would exceed the cADL, which suggest that this calculation is
inaccurate. Thus, an associated aim of the present study was to estimate
O2 while
foraging (diving) in free-ranging king penguins, and thus cADL.
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Materials and methods |
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Heart rate data loggers
The data loggers (61 mmx24 mmx6 mm, 27 g, <0.3% of the body
mass of king penguins) had 4 MB of memory and were able to record
fH and hydrostatic pressure (to an accuracy of 1 m depth)
and were programmed to store these measurements every 2 s. After programming,
the loggers were encapsulated in wax and coated with medical grade silicone
rubber. Prior to implantation, the logger was bathed in a cold sterilising
solution for 2 h, and rinsed thoroughly with sterile water.
Surgical procedure
The implantation was performed 36 days after the egg exchange, so
that the bird was settled on the egg and sufficiently motivated to continue
incubating despite the disturbance caused by handling and implantation. A
portable enclosure was placed over the bird before capture in order to protect
its territory during the surgery. The enclosure consisted of wire mesh formed
into a circular fence that was approximately the area of a king penguin
territory (about 1.5 m diameter and 0.6 m high). The enclosure was also used
to confine the bird to the territory it previously held, while awakening and
recovering from anaesthesia, and to prevent other penguins (or sheathbills and
skuas) from attacking it. 30 min prior the surgery, the bird was injected with
0.5 ml of Valium (Virbac, Centravet Plancoët, France) subcutaneously on
the back. The penguin was captured by placing a sack over the adult and
lifting both it and its egg. The egg was immediately replaced under the bird
by a plaster egg that had previously been kept in an incubator at 38°C, to
prevent breakage of the real one. This procedure generally produced little
reaction from the bird. The real egg was kept in an incubator at 38°C
until its replacement under the adult.
The birds were anaesthetised with halothane in a mixture of O2:N2O (1:1) administered via a hood placed over their head. Induction with 4.5% Halothane (Virbac) usually took 35 min. After induction, the bird was weighed on a load cell balance (accurate to ±2 g) and placed on the operating table. The bird was then intubated, and the anaesthetic gas was altered to 1.5% halothane in pure O2. A long-acting antibiotic (Oxytetrin LA; Virbac) was injected into the pectoral muscle. Some feathers and the down surrounding the brood patch were removed. The remaining feathers around the brood patch and the incision area were deflected and held away using tape. The brood patch, tape and the surrounding feathers were then swabbed with an iodine solution (Betadine; Virbac). The electrocardiogram (ECG) and rectal temperature were continuously monitored throughout the surgical procedures. Xylocaine (lignocaine + 2% adrenaline; Virbac) was injected subcutaneously along the proposed incision lines to prevent bleeding.
The initial skin incision was made in line with the body axis, starting approximately 3 cm above the brood patch, and was about 5 cm long. The second incision, through the abdominal muscles, was made at right angles to the first, enabling an opening of the abdominal cavity of 3 cm length. The HRDDL was inserted into the body cavity, one of the ECG electrodes was placed close to the apex of the heart, its position was checked using an endoscope, and the other was placed pointing in the opposite direction, below the brood patch. The HRDDL was sutured into position with silk thread. Each logger incorporates a transmitter that emits a click on each detected QRS wave of the ECG and a receiver was used to confirm that the logger was detecting and recording the ECG. Heart rate was calculated from its mean period, by dividing the total duration of n heart beat periods by n, over the sampling period.
After the surgery the bird, still asleep, was replaced together with a warm dummy egg within the colony in its enclosure. After full recovery from the anaesthetic (usually 45 h later), the enclosure was removed. 12 days after the surgery, the real egg was replaced under the bird. Attendance behaviour was then monitored during the following experimental period at least twice a day. 34 days after the equipped bird returned to the colony from its foraging trip, it was recaptured with its chick and weighed. Prior to the removal of the data logger, the bird was anaesthetised and carried to the base to be X-rayed, to check the position of the logger and of the ECG electrodes. The procedures for the removal of the logger and for the replacement of the bird in the colony after surgery were similar to those described for implantation.
Data analysis
Birds were initially divided in two groups depending on the year the data
were obtained. Behavioural data were compared and, if no difference was
detected, the data from the 2 years were pooled.
The data were prepared and initially analysed using a purpose-written
computer program in the Labview programming package (version 5.0, National
Instruments, Austin, TX, USA). Further analyses were performed with the
statistical package MINITAB 12.22 for Windows (Minitab Inc.) and Excel 97
(Microsoft Corp.). Diving bouts were visually determined; a bout was deemed to
have started as soon as three deep dives (below 10 m) were interspaced by a
surface duration shorter than 10 min (Boyd
et al., 1994) and it ended as soon as the surface duration was
longer than 10 min. In king penguins, diving bouts are usually easily
determined visually from the depth trace (see
Fig. 1).
|
Estimating the rate of energy expenditure from heart rate
We used the linear regression equations 1 and 2A from Fahlman et al.
(2004) to estimate
O2 for animals
ashore and while at sea, respectively (see
Table 3). The standard error of
the estimate (S.E.E.) for the estimated
O2
(
O2,est) was
calculated from equation 11 in Green et al.
(2001
):
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|
All values (other than
O2est) are
presented as means ± S.E.M. of the mean values from each
animal. After verifying that the data were normally distributed and of equal
variances using a KolmogorovSmirnov normality test and F-test,
respectively, a Student's t-test was 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 test were used when more
than two populations were compared. Results were considered significant at
P<0.05. Woolf's test for differences and Z-tests were
used to compare estimates of
O2.
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Results |
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Finally, in three of the ten birds (D99, W99 and U00) there were, due to programming problems, slight discrepancies (24 min over 15 days) between the recordings of fH and depth, thus the data from these animals were excluded for the fine scale analysis of the cardiac response to diving. For this purpose a total of 10 343 dives was analysed from the remaining seven birds.
Fig. 1 illustrates fH over a 6 day period recorded from a bird at the transition between the incubation and the foraging shift. Note that departure from the colony and diving behaviour are clearly discernible from the fH trace.
Duration of foraging shifts
Birds left the colony on average 9±2 days after the implantation of
the HRDDLs when their mate returned from the sea. The average duration of the
foraging shift of the implanted birds was 16±2 days in 19981999
and 15±1 days in 19992000. In the second year, the mean duration
of the foraging shifts of implanted birds was compared with that of
non-implanted birds (18±5 days, N=13, P>0.05), at
the same stage of reproduction and in close proximity to implanted birds.
There was no significant difference between the two groups.
Diving behaviour
Due to sampling rate and the resolution of the pressure sensor, only dives
for periods longer than 4 s and deeper than 6 m were analysed. The deepest
dive depth recorded was 257 m (for a duration of 7 min 42 s). General details
of diving behaviour are given in Table
1. There was a significant positive correlation for the
relationship of dive duration to depth (depth=0.6xduration 56,
r2=0.82, P<0.05). There was a clear diurnal
dive pattern, with a mixture of deep long and shallow short dives from dawn
(between 05:00 h and 06:00 h) to dusk (around 21:00 h22:00 h), while at
night activity was limited to shallow short dives. This bimodal distribution
of dive depth gave peaks at 10 m and 70 m and a related bimodal distribution
of dive duration (2 and 3.5 min, Fig.
2). Thus, it was possible to establish two groups of dives: long
and deep (>3 min and >40 m) and short and shallow (<3 min and <40
m). 80% of the inter-dive intervals were less than 2.5 min.
|
|
Heart rate during the monitoring period
The frequency distribution of fH clearly differed
depending upon whether the birds were ashore or at sea. When the birds were
ashore, fH ranged between 50 and 150 beats
min1, whereas while they were at sea, fH
ranged between 50 and 260 beats min1, showing peaks at
8090 beats min1 when ashore and 120130 beats
min1 when at sea (Fig.
3). The mean fH of individual birds over the
recording periods ranged from 69.0 to 119.2 beats min1 (mean
fH=87.2±4.3 beats min1) when the
animals were ashore and from 110.9 beats min1 to 156.3 (mean
fH=130.8±5.1 beats min1) when
they were at sea (Table 2). The
overall mean fH of the free-ranging penguins was
111.1±0.3 beats min1. All of the
fH values monitored from the birds in the wild were within
the range of fH recorded during the calibration
experiments (from 47 beats min1 to 308 beats
min1; Fahlman et al.,
2004).
|
When the animals were ashore, no circadian pattern of fH was observed (see Fig. 1). On the other hand, when at sea (Fig. 4), there was a clear pattern, with a decline of fH at dawn (from 121.8±2.0 beats min1 at 00:00 h down to 113.8±1.4 beats min1 at 05:30 h), when the animals start to forage actively (indicated by the increase of mean depth). During the daytime, fH remained at a reasonably steady level (around 122 beats min1), while the birds regularly dived to greater depths (mean diving depth around 66 m). Then, around 21:00 h and after diving depth had begun to decrease, fH increased, to reach a peak of 135.6±2.2 beats min1 at approximately 23:00 h, before returning to the midnight value.
|
Changes in heart rate associated with diving
When dives were grouped according to their duration separated by 10 s
intervals (e.g. all dives between 130 to 139 s were grouped as dives of 134.5
s), a rapid decrease in fH was observed in all categories,
reaching a minimum 4 s after submergence
(Fig. 5). During long dives
(>3 min), fH then showed an increase for the subsequent
6 s, before steadily decreasing to a value similar to that measured when the
birds were ashore (lowest fH, 82.1±5.4 beats
min1; mean ± S.E.M.). During the shorter
dives (<3 min), this secondary increase in fH was not
observed, and fH was maintained at the low level achieved
in the first 6 s ofthe dive, which was also similar to that measured in birds
resting ashore (lowest fH, 88.8±5.2 beats
min1; mean ± S.E.M.; see
Fig. 5). Mean
fH during diving, for all dives, was significantly greater
than these values, but almost 30% below the value between bouts
(Table 2). When
fH was plotted relative to the time of surfacing, there
was no difference between short and long dives. Both showed a slight
anticipatory tachycardia, with the largest increase around 4 s prior to
surfacing. There was no significant difference between fH
pre- and post-dive. Similarly, in the 10 s prior to the dive,
fH did not vary significantly between short and long
dives.
|
Heart rate values between dives, during the dive and over the dive-cycle (dive + post dive interval, 126±4.2 beats min1) were not significantly different between long and short dives. For dives longer than 3 min, however, there were significant negative correlations between dive duration and (a) mean dive fH (r2=0.78, P<0.001), (b) mean dive-cycle fH (r2=0.83, P<0.001), and (c) mean post-dive interval fH (r2=0.78, P<0.001).
The mean fH during all diving bouts (123.5±3.1 beats min1; Table 2) was 40% lower than the mean fH recorded during the hour following the diving bout (168.7±10.2 beats min1; paired t-test, t=5.3, P<0.01, N=8). The mean fH during diving bouts was also 20% lower than the mean fH over the entire subsequent inter-bout interval (141.6±8.8 beats min1; paired t-test, t=2.64, P<0.05, N=8). The mean fH during the hour following a diving bout was, on average, 20% higher than mean fH over the entire inter-bout interval (paired t-test, t=12.01, P<0.001, N=8).
Field metabolic rate
Estimated O2
of birds was calculated according to equations 1 and 2A from Fahlman et al.
(2004
) as appropriate, and
then converted to estimated field metabolic rate FMRest
(Table 3). When at sea,
FMRest was 83% greater than when the birds were ashore. During
diving bouts (and dive cycles), MRest was 73% greater than when the
birds were ashore and MRest during the total period between bouts,
although 20% greater, was not significantly different from that during diving
bouts. However, during the first hour following a diving bout,
MRest was 52% greater than that during a diving bout and 33%
greater than that during the remainder of the interbout interval.
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Discussion |
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Frequency analyses of the dive durations are consistent with those
described elsewhere (Kooyman et al.,
1992a; Culik et al.,
1996
): up to 35% of all dives (deeper than 8 m) were of longer
duration than 3.5 min, and 80% of interdive intervals were shorter than 2.5
min.
The hypothesis developed by Kooyman et al.
(1992a) that king penguins
accumulate lactic acid during long dives and pay off the `oxygen debt' by
increasing surface times or surface frequency is not supported by the present
data. Since a surface time of 2.5 min is theoretically inadequate for the
metabolism of lactate after exceeding the DLT
(Kooyman et al., 1992a
), we
reach a similar conclusion to Culik et al.
(1996
), that these birds must
almost always dive within their DLT. This means that previous estimations of
the cADL of 2 min (Kooyman et al.,
1992a
; Culik et al.,
1996
) must be inaccurate. On the other hand, it is possible, at
least on some occasions, that any accumulated lactate could be metabolised by
the locomotory muscles and/or heart during relatively short, shallow dives
and/or when the birds are travelling to different foraging locations
(Butler, 2004
).
Physiology of diving
Few studies have investigated the variation of fH
during natural dives of birds or mammals. Most of the available data are
either from captive animals during forced
(Scholander 1940) or voluntary
submersion (Millard et al.,
1973
; Butler and Woakes, 1975,
1984
; Bevan et al., 1992) or
from animals in their natural environment but diving through an artificial ice
hole (Kooyman et al., 1992b
).
To our knowledge, only three published studies so far have investigated the
full range of changes in fH during diving in free-ranging
marine birds (Bevan et al.,
1997
,
2002
;
Green et al., 2003
). In the
present study, two different cardiac responses to the dive could be observed,
and from the diving behaviour it was possible to define two distinct types of
dive: short, shallow dives and deep, long dives (i.e. there were no long,
shallow dives). Interestingly, this segregation of the dives between short and
long dives is associated with a difference in temporal changes of
fH during the dive. During the first 6 s of the dive,
there was a rapid reduction in fH, similar to that
measured in unrestrained freely diving captive tufted ducks
(Bevan and Butler, 1992
). Then,
depending on the duration of the dive, fH either increased
in the subsequent 6 s if the bird was going to perform a long and deep dive,
then progressively decreased to a rate similar to the fH
when the birds were ashore. If the dive was short and shallow,
fH stayed low, and again stabilised around the level of
fH recorded when birds were ashore. However, both the
values for lowest fH during diving were significantly
(approximately 25%) lower than that for king penguins resting in water
(114±7.2, N=5; Fahlman et
al., 2004
).
The differences in fH during the first 6 s of
submersion in the long and short dives may relate to the effort involved
during this period. Sato et al.
(2002) indicate that king
penguins have to work harder at the beginning of deep dives than at the
beginning of shallow dives to overcome the increased buoyancy associated with
inhaling more air prior to the longer, deeper dives. However, as depth
increases, the buoyant force would decrease due to compression of the
air-filled spaces between the feathers, thus progressively reducing energy
requirement.
Mean values of heart rate when ashore and during diving bouts (see
Table 2) were similar to those
obtained for gentoo penguins (90 and 140 beats min1,
respectively; Bevan et al.,
2002).
Estimated metabolic rate
When a bird is at its nest incubating, it needs only to supply energy for
its maintenance metabolism (basal metabolic rate, BMR), any thermoregulatory
costs associated with the maintenance of the egg or the chick at its optimal
temperature, and any territorial defence activity. Croxall
(1982) estimated in a number
of penguin species that the energy cost of incubation was 1.21.4 times
the BMR, which is similar to that found in the present study (1.3x BMR;
calculated from the formula of Ellis,
1984
). The estimated, mass-specific metabolic rate of king
penguins ashore [3.15 W kg1 (0.71, +0.93), where the
values within parentheses are the computed S.E.E.; see
Table 3], is within the range
of data obtained by Kooyman et al.
(1992a
), who measured values
between 2.4 and 4.8 W kg1 using doubly labelled water, and
similar to the resting metabolic rate (RMR) obtained from king penguins in a
respirometer (2.8±0.1 W kg1,
Le Maho and Despin, 1976
;
3.0±0.3 W kg1,
Barré, 1980
;
3.7±0.1 W kg1,
Froget et al., 2001
). More
interestingly, fH, and thus FMRest, was at its
lowest when the birds were at sea during the first part of the foraging trip
(travelling before the first diving bout), and during a diving bout
(Table 3). There was then a
large increase in fH during the first hour following the
end of a diving bout. This may have been the result of the increased rate of
energy expenditure associated with the rewarming of the body that occurs at
the end of a diving bout (Handrich et al.,
1997
).
At sea, when the bird was at the surface, it was not possible to
distinguish between periods when the bird was resting and those when it was
porpoising or travelling from one foraging patch to another. However,
mass-specific MRest of the birds when at sea [5.77 W
kg1 (0.37, +0.40)] was 25% greater than that of birds
resting in water (4.6 W kg1;
Culik et al., 1996;
Fahlman et al., 2004
),
indicating that these animals were quite active when at sea. This level of
metabolism included all activities while the bird was at sea, such as the
period when the birds were travelling to and from the colony, and activity at
night when diving was reduced.
It is of interest to note that at sea, mass-specific FMRest from
the present study is 42% lower than the value of 9.95±0.33 W
kg1 obtained by Kooyman et al.
(1992a) using DLW. This
illustrates the apparent overestimation of MR of aquatic birds and mammals
when at sea by the DLW method (Butler et
al., 2004
).
Energy cost of diving and cADL.
The mass-specific
O2est during
diving bouts was determined in the present study to be 17.3 (0.95,
+1.01) ml min1 kg1. When tested against
the validation data in Froget et al.
(2001
), equation 2A in Fahlman
et al. (2004
) gives an average
algebraic overestimation of 2%. The available oxygen stores in diving king
penguins are estimated to be between 45 ml kg1
(Ponganis et al., 1999
) and 58
ml kg1 (Kooyman,
1989
). Using the estimated
O2 during diving
bouts and the upper value of usable O2 stores given above, the
calculated aerobic dive limit (cADL) is 3.4 min and approximately 35% of all
dives exceed this value (Fig.
2).
If our estimates of
O2 are correct,
this implies that king penguins are performing most of their foraging dives
(those greater than 3 min duration) by exceeding their cADL. Unfortunately,
with the exception of those on tufted ducks (see
Woakes and Butler, 1983
), no
study so far has been able to determine
O2 during diving
itself. The rate of oxygen consumption estimated over a complete dive cycle,
as in the present study, is the closest estimate that exists for free-ranging
king penguins. Thus either
O2 during diving
is much lower or/and the oxygen stores are much larger than estimated. In
fact, as Butler (2000
) points
out, even if the
O2 during diving
is the same as that when the birds are resting in water (14.1 ml
min1 kg1,
Culik et al., 1996
; and
15.3±1.3 ml min1 kg1,
Fahlman et al., 2004
), maximum
cADL would be 3.84.1 min and still approximately 20% of the dives would
exceed this duration (Fig. 2).
It is of course possible that
O2 during diving
itself, i.e. when the bird is actually submerged, is lower than when resting
in water (hypometabolism), and one possible mechanism by which this could be
achieved is regional hypothermia (Handrich
et al., 1997
).
Even though there is debate over the physiological significance of such
hypothermia (Ponganis et al.,
2003), Bevan et al.
(2002
) calculated that a drop
in body temperature of only 2.4°C would reduce resting
O2 in water to
such a level that all of the dives of gentoo penguins would be within their
cADL. This is very pertinent to the present discussion because, like the king
penguin, over 20% of the dives of gentoo penguins exceed their cADL, even if
O2 during diving
is assumed to be the same as that when resting in water
(Bevan et al., 2002
).
List of symbols and abbreviations
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Acknowledgments |
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References |
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