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First published online March 28, 2008
Journal of Experimental Biology 211, 1169-1179 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.013235
Heart rate regulation and extreme bradycardia in diving emperor penguins
Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California San Diego, La Jolla, CA 92093-0204, USA
* Author for correspondence (e-mail: jmeir{at}ucsd.edu)
Accepted 3 February 2008
 |
Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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O2 max.,
presumably facilitating oxygen loading and post-dive metabolism. The classic
Scholander–Irving dive response in these emperor penguins contrasts with
the absence of true bradycardia in diving ducks, cormorants, and other penguin
species.
Key words: diving, electrocardiogram (ECG), emperor penguin, heart rate, respiratory sinus arrhythmia, stroke frequency
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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)
with durations longer than 23 min
(Ponganis et al., 2007). This
exceptional diving capacity has stimulated much interest in the physiology
which underlies such behavior in this species
(Butler and Jones, 1997;
Kooyman and Ponganis, 1998;
Nagy et al., 2001;
Ponganis et al., 2003;
Stockard et al., 2005). The
duration of any given dive for an air-breathing animal is dependent on
available oxygen stores, the rate of utilization of these stores, and the
lowest tolerable level of oxygen (O2). Based upon Scholander's and
Irving's classic findings during forced submersion
(Irving et al., 1941;
Scholander, 1940;
Scholander et al., 1942), it
is hypothesized that a reduction in heart rate (fH) and
peripheral perfusion are the principal determinants of the depletion rate of
the respiratory and blood O2 stores. This is because the metabolic
rate of the kidneys, splanchnic organs and heart, which account for about half
of O2 consumption at rest
(Butler and Jones, 1997;
Schmidt-Nielsen, 1983), are
either perfusion dependent or directly related to fH
(Davis and Kanatous, 1999).
Adjustments in fH can influence dive duration by providing
both optimal loading of O2 stores before the dive and a reduction
and redistribution of blood flow to conserve O2 during the dive
(Butler and Jones, 1997).
In comparison to pre-dive tachycardic levels, most diving animals undergo a
decrease in fH upon submersion, with the magnitude of
response varying between species and with dive duration
(Butler and Jones, 1997;
Irving et al., 1941;
Scholander, 1940). Heart rate
has also been used as a measure of field metabolic rate in several studies,
based on the premise that O2 consumption is directly proportional
to fH (Bevan et al.,
1994; Boyd et al.,
1999; Butler, 1993;
Froget et al., 2004;
Green et al., 2003). A
relationship between mean fH during the dive and dive
duration has been documented in several diving species, including elephant
seals, grey seals and cormorants (Andrews
et al., 1997; Enstipp et al.,
2001; Thompson and Fedak,
1993).
The objective of this experiment was to evaluate the cardiac responses of
emperor penguins on a beat-to-beat basis using a digital electrocardiogram
(ECG) recorder, specifically to assess diving fH in
relationship to: (1) fH at the surface and at rest, (2)
dive duration (3) the aerobic dive limit [ADL; duration beyond which blood
lactate concentration increases above resting levels
(Kooyman, 1989); also termed
the diving lactate threshold (DLT) (Butler
and Jones, 1997)] and (4) stroke frequency. An additional goal was
to investigate variations in fH associated with
respiration while the birds were at rest and at the surface, and to consider
how these variations might parallel the diving fH
response. The isolated dive hole is a useful model for this study, since field
metabolic rate, the ADL and respiratory and blood O2 store
depletion rates have been determined for this species under these conditions
(Nagy et al., 2001;
Ponganis et al., 1997;
Stockard et al., 2005;
Ponganis et al., 2007).
We hypothesized that: (1) dive fH would correlate
negatively with dive duration, (2) a true bradycardia (fH
significantly <fH at rest) would occur during diving,
and (3) dive fH would be independent of swim stroke
frequency. Such findings would be consistent with the classic Scholander and
Irving dive response (Irving et al.,
1941; Scholander,
1940; Scholander et al.,
1942), with isolation of muscle and dependence of its metabolism
on its large myoglobin-bound O2 store. In addition, since
fH profiles at rest revealed a possible respiratory sinus
arrhythmia (RSA), the naturally occurring respiratory-induced variation of
fH, we investigated the coupling of this potential RSA
pattern and respirations with use of a chest impedance meter.
Respiratory-induced variations in fH were also compared to
dive fH values to assess any similarity in the
physiological response and possible cardiorespiratory control mechanisms
between these two conditions.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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15 birds/season, N=9 for this
study, 25.1±0.6 kg) were captured near the McMurdo Sound ice edge or at
Terra Nova Bay in October of 2001, 2004, and 2005 and were maintained for 2
months at an isolated dive hole enclosed within a corral at the Penguin Ranch
(Kooyman et al., 1992) on the
McMurdo Sound sea ice (77°41', 165°59'). The birds dived
and foraged under the ice daily, as evidenced by guano deposition and weight
gain. Birds at the isolated dive hole typically exit the water after a dive
and stand on the ice until initiating the next dive
(Kooyman et al., 1992;
Ponganis et al., 1997). All
procedures were approved under a UCSD Animal Subjects Committee protocol and
US Antarctic Treaty Permit. All animals were returned to the ice edge and
released upon completion of the study.
Heart rate profiles
Investigation of respiratory sinus arrhythmia
In four emperor penguins under general isoflurane anesthesia
(Ponganis et al., 2001), three
subcutaneous electrodes were inserted dorsally (one just left of midline at
the level of the axilla, the second just right of midline at hip level, and
the reference electrode approximately 10 cm to the left of midline and 5 cm
above the left hip). After recovery overnight, the electrodes were connected
via a cable to an ECG/Impedance system (UFI, Morro Bay, CA, USA), and
a BIOPAC A-D converter (BIOPAC Systems, Goleta, CA, USA) interfaced with a
laptop personal computer (PC). Impedance and ECG signals were recorded at 62.5
and 250 Hz, respectively. Penguins were standing calmly in a penguin transport
box (45x45x120 cm) located outside (ambient Antarctic temperature,
–10 to –20°C) during the experiment, with the necessary wires
and cords running back into the experimental hut where the hardware was
located. Changes in the baseline impedance signal result from
chest-volume-associated differences in skin impedance between inspiration and
expiration and allow for the calculation of respiration rate. ECG and
impedance signals were recorded simultaneously to accommodate analysis of
corresponding changes between the two channels. The
inspiratory–expiratory changes in the chest impedance signal were
visually verified by an observer peering into the box for a portion of the
recording cycle.
Heart rate at rest, during surface intervals, and during diving
Two-lead subcutaneous electrodes were inserted along the dorsal midline of
nine emperor penguins (conducted separately from above protocol), roughly at
the level of the axilla and just above the pelvis while birds were under
general isoflurane anesthesia (Ponganis et
al., 2001). The electrodes were connected to a custom-built
digital ECG recorder (UFI) in an underwater housing (283 g,
16x6x2.5 cm), secured to the feathers of the mid-back with 5 min
epoxy glue (Devcon; Danvers, MA, USA), a VelcroTM patch, and plastic
cable ties. ECG was recorded at a sampling rate of 50 Hz. An Mk9 time depth
recorder (Wildlife Computers, Redmond, WA, USA; sensitive to 0.5 m, 30 g,
6.7x1.7x1.7 cm) was also attached to record the time/depth dive
profile at 1 Hz. Transducer calibration from the TDR was verified in a
pressure chamber at the Scripps Institution of Oceanography. After overnight
recovery, the birds were provided access to the dive hole for 1–2 days.
At the end of the data collection period, the electrodes and recorders were
removed under general anesthesia.
Stroke frequency and heart rate
Five of the nine birds with the ECG recorder described above were
simultaneously outfitted with a two axis acceleration data logger (M190-D2GT,
Little Leonardo Ltd, Tokyo, Japan; 1.5 cm diameter, 6 cm length, 16 g). The
accelerometer measures depth and acceleration in the y (vertical) and
x (horizontal) axes. Depth was sampled at 1 Hz (±1 m accuracy
and 0.05 m resolution) and acceleration at 16 Hz via an accelerometer
sensor (model ADXL202E; Analog Device, Inc., Norwood, MA, USA). The measuring
range of the accelerometer is ±29.4 m s–2 with a
resolution of 0.0196 m s–2. The accelerometer was oriented so
that the y-axis (head-to-tail) or `surge' acceleration was in line with the
spine (longitudinal axis of the animal), placed approximately midline between
the apexes of the wings and secured with plastic cable ties and waterproof
TesaTM tape. In this configuration, high frequency fluctuations in the
y-axis acceleration signal correspond to `surge', or the acceleration caused
by the bird's stroking wing movements
(Sato et al., 2004;
Watanuki et al., 2003). The
unit was calibrated in seawater against the earth's gravitational acceleration
at the end of each experimental run.
Data analysis and statistics
All recorders were synchronized to the same PC clock, which was
automatically synchronized to an Internet time server. Data were graphed and
analyzed using Excel, Origin, SPSS, Acknowledge, and R software. Using a
customized peak detection program, R-wave peaks from the digital ECG records
were marked and R–R intervals calculated. All peaks were visually
verified in order to ensure marking accuracy. In birds with the accelerometer,
the same peak detection program was used to mark the high frequency
fluctuation of surge acceleration (strokes), with stroke frequency calculated
from the intervals between peaks. Instantaneous fH was
plotted with dive depth from the TDR to construct dive profiles, including
stroke frequency for dives with the accelerometer. These instantaneous values
are also reported throughout the text. For RSA data, fH
was plotted with chest impedance signal. Heart rates for different periods (at
rest, dives and surface intervals) were calculated by dividing the total
number of beats during the period by the period duration. This period
consisted of 1 h for birds at rest, over the entire dive for dive
fH, and over 1 min immediately prior to and immediately
following a dive for the surface interval fH (pre- and
post-dive). For RSA analysis, surface interval fH values
were also analyzed until the RSA pattern emerged after the dive (up to 5.2
min).
Heart rates from the different periods and within periods were log
transformed and compared by independent samples t-tests.
Log-transformed dive fH and minimum fH
were also used for linear regression to assess the relationship of these
variables to dive duration and stroke frequency. Dives were also divided into
two categories of duration, those that were shorter or longer in duration than
the previously measured ADL (5.6 min)
(Ponganis et al., 1997). This
value represents the transition point of a two-phase regression analysis of
post-dive lactate accumulation and dive duration in that study. Although the
ADL is probably a range of values, which shifts in accordance with factors
such as activity and variable oxygen consumption during the dive
(Ponganis et al., 1997), the
value of 5.6 min was used for this analysis to provide a fixed point by which
to categorize dives of different durations.
Individual variation among birds was addressed with ANOVA and Kruskal–Wallis tests. Testing for inter-individual effects specific to the fH vs dive duration relationship was addressed with a resampling approach (R custom script). In this script, the number of dives specific to an individual bird was randomly removed from the pooled data and the regression equation (linear fit of log-transformed fH vs dive duration) parameters from the resulting distribution recorded, with 1000 iterations. A penguin-specific regression equation was generated from another distribution with the specific dives of the individual bird removed from the pooled data. The parameters of the penguin-specific run were then compared to the distribution of parameters from the 1000 random iterations. If the penguin-specific parameter was not within the 2.5% tails of the random distribution, it was considered to fit within the distribution of pooled data. Otherwise, the data from this penguin were considered to significantly deviate from the pooled data. This procedure was repeated for each individual bird. Unless stated otherwise, statistical significance was assumed at P<0.05 and the significance level is quoted in the text. Values are expressed as means ± s.e.m.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Heart rate profiles: electrocardiogram signal and heart rate patterns
ECG records demonstrated high signal integrity in all dives and surface
intervals included in the analysis (Fig.
1). A characteristic pattern of fH during the
dives was evident, with high fH before and after the dive
(pre- and post-dive tachycardia), and a significant reduction in
fH during the dives. The dive fH
response consisted of an immediate decline upon submersion followed by a
readjustment in which fH increased briefly and then
declined once again, with a further progressive decline in longer dives
(Fig. 2). In 93% of the dives,
fH reached the level of fH at rest
within 1 min after submersion. In 71% of the dives, this level was reached
within the first 20 s of the dive. An increase in fH
during ascent (prior to surfacing) occurred in most dives. Surface interval
fH peaked immediately pre- and post-dive, with a maximum
instantaneous fH of 256 beats min–1.
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2=24.265, 35.556, 10.527;
P=0.002, 0.000, 0.230). The significant difference for dive
fH, however, appears only for bird 36. The resampling
approach and comparison of regression equations generated from the
fH vs dive duration relationship also revealed
differences among individuals, but when applying a Bonferonni correction due
to multiple sampling (P<0.006), this difference was once again
present for only one individual. Notably, if this one statistically deviating
individual were removed, the results presented above did not change
appreciably. Since inclusion of an outlier can only serve to weaken any
resulting relationship, this analysis further reinforces the robustness of
conclusions of the pooled data. Taking this into account, all nine individuals
were included in the pooled dataset in all analyses in the study. Mean data
from each of the fH periods is shown for each bird in
Table 1 (N=9, 125
dives).
The mean of dive fH for pooled data (determined as the
total number of beats divided by the dive duration) was 33% of the pre-dive
fH, and 78% of the mean fH at rest
(Table 2). This is similar to
that reported in a previous study of emperor penguins, in which diving
fH was about 85% of the resting value
(Kooyman et al., 1992).
Although dive fH was significantly lower than both
pre-dive and at rest values for pooled data, for individual birds, the mean
dive fH was not significantly lower than rates at rest
when considering dives of all duration collectively. To address
fH differences in relation to the previously measured ADL,
dives from all birds were pooled and divided into those shorter than the ADL
(35.2% of the dives in the study) and those longer than the ADL (64.8% of the
dives in the study). For pooled data, fH in dives longer
than the ADL was significantly less than: (1) fH in dives
shorter than the ADL, (2) fH at rest, and (3)
fH during surface intervals
(Table 2). This was also true
for each individual bird, with the exception of bird 49, in which
fH in dives longer than the ADL was not significantly
lower than fH at rest, but like other birds, was
significantly lower when compared to fH in dives shorter
than the ADL.
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Heart rate data of all birds were log transformed for regression analysis (Figs 3, 4, 7). Log transformation resulted in homoscedasticity and a linear fit for the fH and dive duration relationship (Fig. 4B). Minimum instantaneous fH recorded during the dive also decreased with dive duration, with a shape similar to that of the dive fH vs dive duration relationship and a similarly negative linear relationship between the log of the minimum fH vs dive duration (Fig. 3). There were no significant relationships between dive duration and max. depth of the dive, or between fH and max. depth.
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Stroke frequency and heart rate
Emperor penguins diving at the isolated dive hole stroked continuously
throughout the dive, with no prolonged periods of gliding. The highest stroke
frequencies (1.5–2.2 Hz) occurred during the initial descent
(Fig. 6). Excluding descents,
stroke frequency during the dive was very consistent, with typical values
around 0.45–0.70 Hz, depending on the individual bird. This steady
stroking frequency was usually achieved after the first 20–30 s of the
dive. Dive stroke frequency (the calculated mean of all values during the
dive) in relatively short dives was greater than that of long dives because of
the high stroke frequencies associated with the initial descent and a
relatively short post-descent period, during which stroke frequency was low
and stable. Longer dives had inherently longer post-descent periods
(Fig. 6). Because of this bias,
dives in which the initial descent period constituted 20% or more of dive
duration (generally dives shorter than 2.5 min, 15 out of the 62 dives
analyzed) were not considered when assessing the relationship between dive
stroke frequency and dive duration or to dive fH. This was
further justified by the fact that stroke frequency patterns showed no
differences in short and long dives (Fig.
6). With the exclusion of these dives, there is no significant
correlation between stroke frequency and the log of fH
during the dive (y=0.508x+1.27,
r2=0.082, P=0.051;
Fig. 7A). Stroke frequency had
only a weak negative relationship with dive duration
(y=–17.70x+0.72, r2=0.267,
P=0.0002; Fig. 7B).
The lack of coupling of stroke frequency and fH is most
apparent when considering individual dive profiles
(Fig. 6). Simultaneous profiles
of depth, stroke frequency, and instantaneous fH during a
dive revealed that changes in stroke frequency are not consistently associated
with changes in fH.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Grubb, 1983;
Kooyman et al., 1992).
Respiratory sinus arrhythmias (RSAs) have been documented in a variety of
birds and diving species (Andrews et al.,
1997; Bartholomew,
1954; Butler and Taylor,
1983; Casson and Ronald,
1975; Castellini et al.,
1994a; Castellini et al.,
1994b; Enstipp et al.,
1999; Irving,
1939) and are more pronounced in some species than others [for
example, in dogs (Hamlin et al.,
1966)]. Previous work on elephant seals has demonstrated that RSAs
can be used to estimate respiratory frequency in diving animals, even while at
sea (Andrews et al., 2000).
Apparent RSA has recently been used to determine probable breathing frequency
in resting king penguins (Halsey et al.,
2008). The complete ECG record afforded by the digital recorders
in this study reveal an RSA pattern in emperor penguins and validate the
inference of respiration rate from the regular, momentary tachycardias present
in fH data of birds at rest
(Fig. 5). Analysis of these
tachycardias in ECG records of emperor penguins at rest on the sea ice in
McMurdo Sound reveals a mean respiration rate of 4.1±0.3 breaths
min–1 (mean ± s.e.m., N=9; 1 h period/bird).
Respiration rates of the birds standing calmly in the carrier box for this
portion of the study (Table 3)
were equivalent. These data are comparable to observed emperor penguin
respiratory rates from a previous study
(Kooyman et al., 1971) and are
significantly lower than predicted respiratory rates based on allometry
(Calder, 1968)
(t-test, P=0.000).
The grand mean of minimum instantaneous fH in the RSA
(all minima during the 10 min period for all four birds; mean= 45.0±0.9
beats min–1, N=181) is strikingly similar to the
minimum fH in dives shorter than the ADL
(mean=44.8±2.7 beats min–1, N=44). That is,
fH during dives shorter than the ADL falls to a level only
equivalent to that reached during routine expiration at rest, as opposed to a
much more extreme drop in dives longer than the ADL (mean=14.3±0.9
beats min–1, N=81). This finding is similar to the
fH response during sleep apnea of elephant seals, in which
the apneic fH was comparable to the minimum value during
normal respiratory sinus arrhythmia
(Castellini et al., 1994a;
Castellini et al., 1994b).
Similar to what was conjectured for elephant seals, perhaps the reduction in
fH during dives shorter than the ADL in emperor penguins
is controlled by a similar level or mechanism of cardiorespiratory control to
that governing the respiratory sinus arrhythmia, with a further reduction in
fH (and true bradycardia as defined in this work)
occurring only in dives longer than the ADL.
Heart rate profiles: diving
Heart rates of emperor penguins in dives shorter than their ADL (<5.6
min) in this study are in agreement with fH of other
diving birds. For example, cormorants and several penguin species show a
significant decrease in diving fH as compared to pre-dive
values, with fH maintained throughout the dive at a level
similar to that at rest (Butler and
Woakes, 1984; Enstipp et al.,
2001; Froget et al.,
2004; Millard et al.,
1973). Mean fH in the emperor penguin in
pooled dives, and, more notably, in dives longer than the ADL, is
significantly lower than both surface interval fH and
fH at rest (Table
2), consistent with findings from the previous study of
fH in diving emperor penguins
(Kooyman et al., 1992). This
demonstrates a true bradycardia (fH significantly
<fH at rest) for the diving emperor penguin at the
isolated dive hole. Such a response has never been documented in any other
diving bird, even in dives greater in length than their calculated aerobic
dive limit (cADL; though this cannot be considered a direct comparison to the
measured ADL as reported here) (Butler and
Woakes, 1984; Enstipp et al.,
2001; Froget et al.,
2004; Millard et al.,
1973).
An immediate decline in fH upon submersion was
characteristic of all dives in the study. The intensity of bradycardia during
the dive increased with dive duration. This applies to individual dives (lower
fH as the dive progresses) and to the dive
fH and dive duration relationship (Figs
2,
4). Because
fH is indicative of the rate of blood O2
transport and delivery to the tissues, the bradycardia documented in this
study is probably associated with a reduction in blood flow to muscle and
other organs. Although it occurs immediately upon submersion, the initial
decline in fH in the emperor penguin is gradual, as
described in Scholander's forced submersion studies with penguins
(Scholander, 1940). This
initial decline occurs more gradually than that seen in some diving seals
(Andrews et al., 1997;
Thompson and Fedak, 1993).
Emperor penguins have 19% of their O2 stores in the respiratory
system (Kooyman and Ponganis,
1998) and dive upon inspiration
(Kooyman et al., 1971). Thus,
the gradual decrease in fH in the beginning of dives may
reflect the continued uptake from respiratory O2 stores during this
period. Deep diving seals, however, with <5% of O2 stores in the
lungs, would not benefit from maintenance of fH (i.e.
continued O2 extraction) in this respect, consistent with the
immediate drop to low fH in these species.
Heart rate decreased to extremely low values in long dives, in some cases
remaining below 5–6 beats min–1 for several minutes
(Fig. 2C,
Fig. 6C). Consistently low
levels of fH were frequent in dives longer than the ADL.
These data demonstrate that such extreme responses are a common component of
emperor penguin diving physiology. The minimum instantaneous
fH during the dive decreased significantly with increasing
dive duration (Fig. 3). This
distribution emphasizes that extremely low values are only present in longer
dives, with the degree of bradycardia reflecting dive duration. Such extremely
low values of fH have been demonstrated in free diving
seals (Andrews et al., 1997;
Thompson and Fedak, 1993), but
in birds, have only been documented in forced submersion or exclusion studies
(Butler, 1982;
Butler and Jones, 1968;
Folkow et al., 1967;
Jones, 1969;
Jones et al., 1988;
Jones and Holeton, 1972;
Ponganis and Kooyman, 2000;
Stephenson et al., 1986). Low
fH, present in later portions of long dives, may reflect a
reinforcement of the initial bradycardia by low O2 partial pressure
(PO2), through a possible chemoreceptor
response (Butler and Stephenson,
1988; Enstipp et al.,
2001). It is also interesting to note that some extremely low
fHs correspond to sudden reversals (descent immediately
following an ascent) in the depth profile
(Fig. 2C,
Fig. 6C), as has been
documented in other diving species (Andrews
et al., 1997). These reversals in the depth profile in emperor
penguins diving at the isolated dive hole have been associated with the
ascents and descents of foraging events
(Ponganis et al., 2000). In
addition, in some cases, such reversals might indicate an additional descent
after a return toward a hole in which exit was blocked by other birds or an
occasional Weddell seal.
Assuming stroke volume is constant
(Butler and Jones, 1997), the
ratio of dive fH to fH at rest is
equal to that of the respective cardiac outputs. Considering the mean of dive
fH for all dives longer than the ADL, this indicates a
mean 44% reduction in cardiac output during these dives. For the longest dive
in the study (18.2 min), mean cardiac output would be decreased by 77%. During
the periods of very low fH toward the end of longer dives
(Fig. 2C,
Fig. 6B,C), cardiac output may
be reduced by as much as 93% for five or more minutes. This is consistent with
a low blood O2 depletion rate while diving, and demonstrates an
extreme diving response, as originally proposed by Scholander and Irving in
their early work with forced submersion studies
(Irving et al., 1941;
Scholander, 1940;
Scholander et al., 1942).
An increase in fH during ascent (prior to surfacing)
was a common feature in most dives. Such a response has been observed in many
diving species, including other penguins, and has been termed an `ascent' or
`anticipatory tachycardia' (Andrews et al.,
1997; Froget et al.,
2004; Green et al.,
2003; Millard et al.,
1973; Thompson and Fedak,
1993). It has been hypothesized that this response may serve to
replenish the O2 supply to depleted tissues, thereby lowering the
PO2 in blood, and providing a larger gradient
to maximize O2 uptake at the surface, and perhaps to minimize
recovery time (Butler and Jones,
1997; Millard et al.,
1973; Thompson and Fedak,
1993). If the number of beats in this period of increased
fH during ascent are counted and multiplied by the stroke
volume of the emperor penguin (Kooyman et
al., 1992), an estimate of the amount of blood circulating in that
time period can be obtained. Such a calculation provides the percentage of
blood available that could contribute to the supply of depleted tissues at the
end of the dive. For example, considering the longest dive in this study
(Fig. 2C) and the known blood
volume of an emperor penguin (Kooyman and
Ponganis, 1998), 92% of the blood volume would be circulated
during this ascent period. For the 10 min and 11 min dives in
Fig. 6B,C, these values are 47%
and 43%, respectively. For shorter dives of 1.5 min and 5.8 min
(Fig. 2A,B), 96% and 69% of the
blood volume is circulated during this ascent period. These values imply that
over a wide range of dive durations, a significant portion of the blood volume
is circulated during the period of increased heart rate during ascent. The
distribution of this increased blood flow to tissue (brain, heart, central
organs and/or muscle) is unknown but would be dependent on sympathetic
responses in individual birds during the ascent.
Heart rate profiles: surface intervals
Heart rate during surface intervals was measured over 1 min immediately
prior to and following a dive because total surface interval data (i.e. the
entire time period between dives) were not considered relevant for the present
study. Time spent on the surface post-dive at the isolated dive hole is not
necessarily an indicator of diving recovery, as these emperor penguins are
subject to other influences and distractions such as interactions with other
birds in the corral or activities and personnel at the Penguin Ranch
campsite.
Pre- and post-dive periods of tachycardia presumably serve to load
O2 stores pre-dive, and to eliminate carbon dioxide and replenish
O2 stores post-dive. Tachycardia and high respiration rates
facilitate rapid gas exchange during the surface interval and allow for a
quick recovery from dives (Fedak et al.,
1988; Kooyman et al.,
1971; Le Boeuf et al.,
2000). The maximum instantaneous surface interval
fH in this study is the highest ever recorded for emperor
penguins (256 beats min–1), and is in the range of
fH recorded during maximum O2 consumption
(O2max) of
emperor penguins swimming in a flume
(Kooyman and Ponganis, 1994).
The similarity of the peak values obtained in these two studies, and the
consistent range of the fH values immediately prior to and
following dives among individual birds suggest that emperor penguins are
operating at a maximum of oxygen uptake during these periods of the surface
interval.
While fH is at its highest immediately pre- and
post-dive, there is little variation in fH and a distinct
RSA pattern is not evident. As the fH decreased after the
initial extreme tachycardia during the post-dive surface period, the RSA
pattern did emerge in many cases. Similar RSA patterns have been demonstrated
in sleep apnea studies of elephant seals. Although the RSA is present in seals
throughout the post-apneic period, it is much more pronounced as the
tachycardia decreases during recovery
(Castellini et al., 1994a). A
decrease in the sinus arrhythmia index (the difference between inspiratory and
expiratory fH) at high fH has also
been observed in other mammals (Mazza et
al., 1980). The time until the RSA pattern emerged after dives in
this study ranged from 11–311 s with a mean of 107±10 s
(N=43). By this time, when respiration can once again be inferred by
the RSA, it is not significantly elevated above the resting range. Previous
data on emperor penguins document vigorous hyperventilation after dives
greater than 1 min in duration, with rates of up to 25 breaths
min–1 (mean 15 breaths min–1) during
the first minute after surfacing (Kooyman
et al., 1971). The time required for post-dive respiratory rate to
return to resting levels (3 min), as inferred by post-dive RSA patterns,
is consistent with that observed in the previous study
(Kooyman et al., 1971).
Stroke frequency and heart rate
Consistent with a previous study (van
Dam et al., 2002), emperor penguins diving at the isolated dive
hole stroked continuously throughout the dive, with a stroke-glide pattern but
no prolonged periods of gliding. The highest stroke frequencies (1.5–2.2
Hz) occurred during initial descent, as the penguin overcame its positive
buoyancy at shallow depth (Sato et al.,
2002; van Dam et al.,
2002). High stroke frequencies also occurred occasionally later in
the dive, during descents from shallow depths.
The classical exercise response includes increases in
fH and muscle blood flow in response to increasing work
effort, in both terrestrial and marine animals
(Fedak et al., 1988;
Williams et al., 1991).
Consequently, if working skeletal muscle were perfused during diving,
fH during the dive would be expected to increase with
stroke frequency, reflecting the increase in work effort. As discussed in the
results, it is clear that there is no significant correlation between mean
stroke frequency and dive fH
(Fig. 7A). This is also
apparent when considering individual dive profiles. Review of simultaneous
depth, stroke frequency, and instantaneous fH profiles
reveals that high stroke frequencies are always associated with descents but
not usually associated with corresponding changes in fH
(Fig. 6). As discussed
previously, fH profiles during the dive are characterized
by an immediate decrease in fH upon submersion, followed
by a readjustment period where fH briefly increases before
gradually decreasing. Despite this immediate and quite drastic reduction in
fH, stroke frequency is at its maximum during this initial
descent period. According to classical exercise physiology, if
fH were significantly influenced by stroke frequency, high
fH would be expected during the descent when stroke
frequency is at its maximum, however, the reverse holds true. Heart rates are
conversely at their most significant rate of decrease in this period, reaching
the level of fH at rest within the first 20 s in 71% of
dives, whereas maximum stroke frequency is sustained. Excluding descents,
dives are characterized by constant stroke frequencies for the entire
duration, yet fH is variable and toward the end of longer
dives, is often 2–4 times lower than during the first half of the dive
(Fig. 6). An increase in
fH during ascent was also present in most dives, while
stroke frequency remains constant in this period.
Circulatory adjustments are expected in order to maintain blood pressure
because of reduced cardiac output during diving (reductions in
fH, and unchanged or slightly decreased stroke volume)
(Butler and Jones, 1997;
Irving, 1938). A substantial
redistribution of blood flow during forced submersion and diving studies has
been documented in many birds and mammals, often with more pronounced changes
as the dive approaches or exceeds the ADL
(Butler and Jones, 1997;
Davis et al., 1983;
Irving, 1938;
Kooyman, 1989;
Millard et al., 1973;
Murdaugh et al., 1966). The
`true bradycardia' and the lack of coupling of fH and
stroke frequency in dives of emperor penguins at the isolated dive hole are
consistent with decreased or absent muscle blood flow during dives. This
assumption is supported by prior studies. In emperor penguins, the temperature
of the pectoral muscle, one of the two primary underwater locomotory muscles
of penguins, consistently increased during diving and decreased during the
surface interval (Ponganis et al.,
2003). The magnitude and pattern of the temperature fluctuations
were consistent with what would be predicted if there were little to no muscle
blood flow during dives, and if the metabolic rate of the muscle were
calculated on the basis of complete depletion of myoglobin-bound O2
stores within the ADL (Ponganis et al.,
2003). Recent data also demonstrate that blood lactate levels in
emperor penguins do not increase significantly during the dive, even in dives
longer than the ADL (P. J. Ponganis, unpublished data). Blood lactate does not
increase until the post-dive surface interval period
(Ponganis et al., 1997). The
true bradycardia, the lack of a fH–stroke frequency
relationship, pectoral muscle temperature increases and lactate washout into
the blood during the post-dive period all support the concept of peripheral
vasoconstriction, isolation of muscle from the blood O2 store and
reliance of muscle metabolism on a myoglobin-bound O2 store.
Review of fH profiles also reveals that during the
initial descent of a dive, fH immediately decreases, then
transiently increases, and gradually decreases again (Figs
2,
6). This pattern has also been
seen in diving king and macaroni penguins
(Froget et al., 2004;
Green et al., 2003). It might
be argued that this initial readjustment in fH could imply
a redistribution of blood back to muscle after intense stroking effort
associated with the descent. This suggestion was offered to explain the
comparable fH readjustment pattern in deep dives of king
penguins and a delayed increase of pectoral muscle temperature observed in
these birds (Froget et al.,
2004). The hypothesis posed for king penguins was based on the
fact that the readjustment was seen only in deep (long) dives in that study
(not in shallow, short dives), and was thereby suggested to reflect an
increase in work effort possibly due to increased buoyancy from a higher
inspired air volume before deep, long dives
(Froget et al., 2004;
Sato et al., 2002). Contrary
to these king penguin results, however, emperor penguin dives at the isolated
dive hole demonstrated this initial fH readjustment in all
dives. Emperor and king penguins exhibit differences in diving behavior,
diving capacity, and ecological constraints, and thus physiological
disparities may simply be due to the fact that the two species rely on
different diving strategies. In order to make a more appropriate comparison
between these two species, however, it would be necessary to obtain
fH profiles of emperor penguins during deep dives while
foraging at sea. Regardless of the distribution of blood flow during the
transient increase in fH during descent, increased cardiac
output should facilitate respiratory gas exchange and the transfer of
O2 from the respiratory store to the blood O2 store
during this time period.
The value of digital ECG
Although digital ECG records result in more laborious data processing than
their R-wave detector (fH data logger) counterparts, they
reveal the full extent of the cardiac response, allowing validation of
extremely high fH values associated with surface intervals
and extremely low fH during the latter parts of long
dives. Application of digital ECG could resolve studies employing
fH data loggers, which have resulted in disparate
fH data for the same species
(Green et al., 2005;
Green et al., 2003). The
detailed beat-to-beat analysis afforded by digital ECG also reveals
physiological patterns such as the RSA.
Differences in diving fH between this and the previous
study on fH in emperor penguins
(Kooyman et al., 1992) can
most likely be attributed to the difference in technology, as the previous
study used an R-wave recorder which averaged fH over 15 s
intervals. Most of the dives in that study were much shorter than those in
this one, which also contributes to the higher dive fH
found by Kooyman et al. (Kooyman et al.,
1992). However, even in a 10 min dive in the previous study,
fH was reported to decline to a minimum of only about 30
beats min–1, as compared to instantaneous minimum
fH values of 5–10 beats min–1 for
dives of similar duration in this study. Although some of the dive
fH values for particular durations were consistent between
the two studies, Kooyman et al. (Kooyman
et al., 1992) did not find a correlation between
fH and dive duration, as compared to the present study
(Fig. 4). These differences in
findings may be secondary to differences in sample size and the range of dive
durations, to a loss of variation in fH due to averaging
by the R-wave detector, or to possible miscounting of T-waves or other
waveforms in the ECG profile by the R-wave detector in the earlier study.
Digital ECG avoids the latter two potential problems by providing the entire
record of the ECG signal. It also eliminates imposing an upper limit for
fH, as was necessary with the R-wave recorder to avoid the
incorrect counting of T waves as R waves
(Kooyman et al., 1992). In
order to avoid such double counting in the previous study, it was necessary to
impose an upper limit of 120 beats min–1, which was
significantly below surface interval fH revealed by both
the post-dive analog ECG in that study and the digital ECG in this study.
In summary, we have validated the hypotheses posed in this study, and have determined that: (1) in contrast to any other free diving bird, a true bradycardia and extremely low fH occur routinely during dives of emperor penguins at the isolated dive hole, (2) peak surface interval fHs (the highest surface interval fHs ever recorded for this species) are likely consistent with maximum oxygen uptake, (3) respiratory rate can be inferred from the RSA in this species, and (4) fH and stroke frequency are not coupled in diving emperor penguins.
LIST OF SYMBOLS AND ABBREVIATIONS
O2max
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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