Predicting metabolic rate from heart rate in juvenile Steller sea lions Eumetopias jubatus
Marine Mammal Research Unit and Department of Zoology, University of
British Columbia, Hut B-3, 6248 Biological Sciences Road, Vancouver, British
Columbia, Canada V6T 1Z4
Present address: Alaska SeaLife Centre and the University of Alaska,
Fairbanks, PO Box 1329, Seward, Alaska 99664, USA
* Author for correspondence (e-mail: consortium{at}zoology.ubc.ca)
Accepted 9 March 2003
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Summary |
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Key words: heart rate, energy expenditure, Steller sea lion, Eumetopias jubatus, oxygen consumption, metabolic rate.
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Introduction |
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The DLW method suffers from two major limitations. The first is that it
provides only a mean estimate of metabolism over the entire period between
blood samplings. The second limitation is that there is a finite time over
which the measurement can be made, due to the biological half-life of the
chemical agents. In large vertebrates, this period is usually 510 days,
after which the animals must be recaptured for blood sampling. Many
assumptions, estimates and logistics needed to use DLW also compromise the
applicability of this technique (see
Costa, 1987;
Speakman, 1993
).
Recording heart rate is a technique for estimating energy expenditure that
offers the possibility of monitoring metabolism for a year or longer, with a
fine time resolution of hours or minutes that can be related to specific
activities (Butler, 1993;
Bevan et al., 1995b
;
Woakes et al., 1995
;
Andrews, 1998
). When coupled
with dive profiles from timedepth recorders, for example, heart rate
may be used to estimate the energy expenditure of specific dives. Several
comparative studies have shown that this technique is as robust as using the
DLW method (Nolet et al.,
1992
; Bevan et al.,
1994
,
1995a
;
Boyd et al., 1995
).
The heart rate method is based on Fick's relationship of oxygen consumption
(O2) and heart
rate (fH) (Fick,
1870
):
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Several studies have found close correlations between
fH and
O2 when animals
are exercising in a steady state. However, diving animals present a unique
problem. Dives may include a significant amount of anaerobic metabolism, and
single dives may not be considered a steady state, given the inherent
intermittency of gas exchange and large changes in heart rate that occur upon
surfacing and submerging (Fedak et al.,
1988
; Butler,
1993
). However, average heart rate and oxygen consumed may be
correlated over complete dive cycles (surface plus dive time)
(Fedak, 1986
).
Significant correlations between fH and
O2 have been
found using average dive cycles in captive diving gray seals Halichoerus
grypus, California sea lions Zalophus californianus, harbour
seals Phoca vitulina and bottlenose dolphins Tursiops
truncatus (Williams et al.,
1991
,
1993
;
Butler et al., 1992
;
Boyd et al., 1995
;
Hurley, 1996
). While it is
probable that the general pattern holds true for Steller sea lions, there is
no reason to expect the predictive relationship to be identical between the
diverse species or between life stages already studied, given differences in
phylogeny, body mass, diving behaviour, and foraging patterns. Resulting
differences can reveal much about the physiological adaptations of these
species and the development of physiological processes in Steller sea lions.
Therefore the specific relationship between fH and
O2 must be
determined for this species, particularly before it can be applied to animals
in the wild.
Our objective was to test the feasibility of using heart rate to monitor
metabolic rate in Steller sea lions using captive, juvenile animals. Alaskan
Steller sea lion populations have declined to less than 20% of their peak
mid-1970s abundance (Trites and Larkin,
1996). Changes in the animals' energy budget due to changes in
their prey base have been considered a potential reason for the decline
(Alverson, 1992
;
Merrick et al., 1997
;
Rosen and Trites, 2000
).
Testing this hypothesis by measuring the energy expenditures of free-ranging
Steller sea lions using DLW is difficult, however, given the problem of
recapturing an aquatic mammal in a set time interval. The heart rate method
permits data to be collected with a finer time resolution, allowing the
metabolic cost of specific activities to be estimated. Additionally, long-term
data can be recorded and retrieved from dataloggers, avoiding restrictive time
constraints for animal recapture.
We tested whether a relationship exists between heart rate and postabsorptive oxygen consumption in each of four captive Steller sea lions. Data were collected while each animal rested in a dry metabolic chamber or while swimming, diving or resting within a swim mill. The results were evaluated in terms of the future potential of using the heart rate technique to monitor energy expenditure of free-ranging Steller sea lions.
Additionally, we wanted to investigate how feeding may change the
fH/O2
regression. To our knowledge, no studies have examined this potential factor.
Instead, the
fH/
O2
relationship has been determined for subjects fasted prior to any experiments
(thus, excluding food effects completely)
(Butler, 1993
;
Boyd et al., 1995
) or after
the subjects had the opportunity to ingest a meal (excluding comparison
between data with and without food)
(Williams et al., 1991
;
Li et al., 1993
;
McCrory et al., 1997
). Only
one study on bottlenose dolphins (Williams
et al., 1993
) and one on Antarctic fur seals
(Boyd et al., 1999
) have
determined the
fH/
O2
relationship over a period that was likely to have involved some feeding.
Close relationships between fH and
O2 were reported
in these studies, but whether or not feeding changed the relationship was not
tested. We performed a preliminary investigation into the accuracy of
estimating energy expenditure from heart rate over periods of time that
encompassed feeding by comparing the regressions of a single sea lion when fed
and when fasted.
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Materials and methods |
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Experimental apparatus
Monitoring heart rate
Two dorsal electrodes were attached to each sea lion while under
anaesthesia in areas that gave the cleanest electrocardiogram (ECG) signal
either one above each scapula, or one above a scapula and the other
above the pelvis on opposing sides. Four previous styles of electrodes were
tested before the final, most appropriate design, was applied (see
McPhee, 2001, Appendix 2).
These final electrodes consisted of two basic parts: (1) 12 cm of 28-gauge
bioelectric cable inserted subcutaneously and (2) an external base of epoxy
resin containing a female underwater connector soldered to the subcutaneous
cable, and underlaid with a portion of neoprene that was glued with
fast-setting cyanoacrylate to the fur of the animals.
The ECG was sampled and recorded at 100 Hz by a datalogger housed in the pocket of a nylon and neoprene harness worn by the sea lion.
Monitoring oxygen consumption
Open circuit respirometry measured the oxygen consumption of each animal
during dry and swimming trials as described by Rosen and Trites
(1997,
2002
). For dry trials, the sea
lions entered a sealed opaque metabolic chamber through which air was drawn at
a constant rate of 153 l min1. From a desiccated subsample
of expired air, an S-3 A/I solid oxide cell analyzer (Ametek Inc., Pittsburgh,
PA, USA) determined oxygen concentration while an AR-60 infrared gas analyzer
(Anarad Inc., Santa Barbara, CA, USA) determined carbon dioxide concentration.
A Sable Systems (Henderson, Nevada, USA) Data Acquisition System calculated
average concentrations from 200 subsamples of expired air every second. The
system was base-lined to known ambient air concentrations before and after
each trial and periodically calibrated with gases of known concentrations. The
amount of oxygen consumed during a trial was calculated from the difference in
oxygen concentration between airflow into and out of the chamber, with flow
corrected to STPD. Air temperature within the chamber varied between 2°C
and 25°C (see McPhee,
2001
, Appendix 1). A video camera and lighting within the chamber
allowed activity to be monitored.
For swimming trials, the animals entered a seawater-filled swim mill
(active space = 3.2 m length x 1.8 m width x 1.0 m depth). The sea
lions could only surface to breathe under a transparent Plexiglas dome at one
end of the swim mill. Air was drawn through the dome at a rate of 142 l
min1. The system was base-lined to known ambient air
concentrations at the beginning of a swimming session and after every
following hour. Oxygen concentrations were determined as above for the dry
trials using carbon dioxide concentrations to mathematically remove their
affect on oxygen readings (equation 3b in
Withers, 1977).
To promote a range of oxygen consumption and heart rates from the animals, the water current speed within the swim mill was altered. Previous experience had shown that swimming activity increased with increasing water speed. However, swim speed was not always equivalent to water current speed. When there was current, the animals often swam in a circular pattern toward the back of the swim mill, where they would briefly rest before swimming against the current to return to the dome to breathe. Occasionally, they would rest motionless on the bottom or beneath the dome. For these trials the water speed within the flume was set at 0.0, 0.9, 1.1 and 1.3 m s1. Male 1 was also tested at 1.5 m s1. Water temperature varied between 2°C to 11°C for Male 1, but remained between 9°C and 11°C for the other three animals.
Protocol for fasting trials
For each data-collecting period, the sea lions wore their harnesses with
the datalogger in the pocket. The free end of each of the two wires from the
datalogger ended in a specialized male connector (Underwater Systems, Stanton,
California, USA) to match the female connector of each electrode. Once the
wires were attached to the electrodes, the logger began to record ECG. The
animals were usually fasted for the previous 1224 h. However, they were
occasionally fed a small amount of herring (up to 200 g) prior to a session of
heart rate trials to ensure cooperation. The animals were then enclosed in
either the swim mill or the metabolic chamber, during which time their ECG and
oxygen consumption rates were monitored simultaneously.
A swimming session was divided into a series of 18 min trials. Each trial
consisted of a 10 min period to allow the animal to reach a physiological
steady state at the set water current speed and to allow air to equilibrate
within the enclosed system. This was followed by an 8 min period of
O2 data
collection, which was sufficient to derive a stable reading of
O2, and was the
minimum length of time that the animals were trained to remain reasonably
calm. During each trial, the animals swam in the swim mill at one of the
randomly preselected water current speeds. At the completion of the trial, the
water current would remain the same or would be switched to a new speed and
another 18 min trial would begin. There was no water current during the first
trial in a series. If an animal appeared to become agitated while swimming
against a certain water speed, the next trial was run without a current. A
swim session continued for a maximum of 6 h, depending on the animals'
cooperation, yielding a maximum of 18 trials in a day's session. Occasionally,
at the end of a session, the animals would be directed to remain as motionless
as possible with their heads above water in the respirometry dome (denoted as
a `hold') so that resting values in the mill could be obtained. No holds were
obtained from Male 2.
A dry session for resting values comprised a 15 min equilibration period
once the animal was enclosed in the metabolic chamber, followed by a 15 min
O2 data
collection period. Only one dry trial was run in a day. Dry trials were
obtained from only Male 1 and Female 1, as Male 2 and Female 2 would not enter
the chamber.
Protocol for feeding sessions
Data were collected after feeding events from Male 1 in the swim mill. The
equipment and protocols were the same as for the fasting trials with the
following exceptions. The sea lion entered the swim mill 3273 min after
having ingested a bulk amount of either 6 or 12 kg of herring. This typically
represented a half or full daily ration, and was equivalent to the intake
predicted for wild Steller sea lions
(Winship et al., 2002). Each
swimming session was 3 h and consisted of monitoring the animal's heart rate
and oxygen consumption rate while swimming in the swim mill without any
applied current. After an initial 10 min air-equilibration phase, each session
was split into successive trials lasting 5 min each. When one 5 min trial
ended, another began immediately following it until 3 h had passed since the
first trial. Three swimming sessions preceded by 6 kg feedings were performed
on three separate days in close succession, followed by another three sessions
after 12 kg feedings.
Analysis
Heart rate
After the initial equilibration periods, mean heart rate was calculated
over the following 5 min in the swim mill and the following 15 min in the dry
chamber. The mean heart rate during the first 5 min of a hold was also
calculated. These intervals were chosen based on stabilization of the heart
rates or as the most representative of the heart rates during a trial.
The recorded electrocardiogram was downloaded from the datalogger to a desktop computer after each session. Mean heart rate in beats min1 over the required interval was derived from interbeat intervals on the ECG.
Oxygen consumption
Mean rate of oxygen consumption was calculated from differences between
incurrent and excurrent oxygen concentration and measured flow rates corrected
to STPD. There was variation in the body mass of individuals over the course
of the experiments, as well as substantial differences between individuals
(Table 1). Therefore, the
potential effect of body mass on the relationship between heart rate and
oxygen consumption had to be considered.
Past studies have attempted to `correct' for changes in mass by expressing
oxygen consumption rates on a mass-specific basis
(O2
M1). However, there is no physiological or
empirical basis for assuming such a conversion
(Packard and Boardman, 1988
;
Hayes, 2001
). We decided to
empirically derive an appropriate exponent by calculating a multiple factor
power relationship. This allowed us to compensate for differences in body mass
without making any a priori assumptions of what the correction factor
should be.
The analysis was performed on all of the pooled fasting data from all animals. It was inappropriate to perform analyses on each animal as changes in individual body mass were much smaller than differences between individuals (Table 1), and the source of the mass changes (i.e. metabolically active tissues or inactive blubber) was unknown.
The data were log-transformed so that a linear multiple regression analysis
could be generated using Systat software (Systat, Inc., Richmond, California,
USA). This transformation was based on the relationship that:
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As many previous studies have assumed a linear relationship between
fH and O2, we then produced general linear regressions for
each individual as well as the pooled data based on the derived exponent for
body mass that followed the general form:
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In addition, to aid comparison with results of other published studies, we
derived a linear model from the pooled data using the general mass-specific
equation:
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fH/O2
relationships
For each animal, a simple linear regression between fH and the
corresponding O2
values calculated from the swim and dry trials was run using Systat software.
The data points used were the mean fH and
O2 values from
each 8 min analysis period of the swim trials or from each 15 min dry trial.
Since a mean 2.8 min delay was incurred between the time the air was drawn
from the respirometry dome to when it reached the oxygen analyzer,
O2 data were
shifted ahead by 2.8 min to temporally synchronize oxygen consumption with
heart rate. The resulting regression was then plotted with fH on the
abscissa and
O2
on the ordinate axis. Probability levels of P<0.05 were considered
significant. Analysis of covariance (with heart rate as the covariate) was
used to compare the resulting regressions from each animal. Residuals
(calculated as the vertical distance of the recorded
O2 from the
estimated
O2 of
the regression line) were plotted in the order of data collection and fit with
lowess-smoothed curves for each animal to detect any temporal trends in the
data.
To determine a mean regression, all four data sets were pooled and fitted with a mixed linear procedure (PROC MIXED, SAS). Data from each animal were treated as a repeated-measures set, as were data collected within any single day within an animal. Because timing of data collection was imbalanced within each animal (time intervals between successive data points were not equivalent), a compound symmetry covariance structure was considered. This analysis was performed using both forms of the `mass-corrected' oxygen consumption data (i.e. M0.6 and M1.0).
Comparison of fasted and fed data
The regression obtained during the feeding trials for Male 1 was compared
with the regression obtained from the same individual during the fasting
trials. For each of the six feeding sessions, a time series using mean heart
rate from each 5 min trial and a second using mean oxygen consumption rate was
constructed to investigate behaviour of the variables as digestion progressed
after feeding.
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Results |
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Relationship between fasted heart rate and oxygen consumption
Plotting mean heart rate (beats min1) and the
corresponding mean rate of oxygen consumption (ml O2
h1 kg0.60) from each trial showed a linear
relationship between the two variables for each animal
(Fig. 1). Slopes varied between
47.7 and 101.5 ml O2 beat1
kg0.60, with intercepts between 1028.0 and 3536.6 ml
O2 h1 kg0.60, and
r2 values between 0.21 and 0.78
(Table 2).
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Comparing the slopes of the four regressions (Fig. 1) revealed that only those of Male 2 and Female 1 were statistically similar (P>0.10). All regression intercepts were significantly different among animals (P<0.01).
Smoothing the residuals (arranged by order of data collection) showed that the regressions poorly described the data collected from the females at the beginning and end of the study (Fig. 2). Possible explanations include some unknown change in equipment during collection or a physiological change in the animal (resulting in a change in the heart rate and oxygen consumption relationship). A similar but slighter trend was evident for Male 1, while residuals from Male 2 were evenly distributed about a mean of zero (Fig. 2).
|
A mean regression for all four Steller sea lions could be determined by
calculating the mean slope and intercept of the four linear regressions
(Table 2,
Fig. 3A). However, a better
method was to pool the four data sets and fit the resulting set with a mixed
linear model, treating all data from an animal (and from a day within an
animal) as a repeated-measures set with a compound symmetrical covariance
structure. The mean regression relating oxygen consumption rate (in ml
O2 h1 kg0.60) to heart rate
resulting from this analysis (Fig.
3B) was
O2
=(71.3fH±4.3)(1138.5±369.6) (means
± S.E.M.) (r2=0.69, P<0.01). To aid
comparisons to some previously published studies, the analysis was rerun with
the rate of oxygen consumption in ml O2 h1
kg1.0, yielding
O2
=(0.19fH±0.01)(4.12±1.3)
(r2=0.69, P<0.01).
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Effect of feeding on heart rate
Rate of oxygen consumption significantly increased over time following
ingestion of all 6 and 12 kg meals (Fig.
4). However, heart rate was more variable and increased slightly
in only one of the six trials (a 12 kg feeding). Heart rate either declined or
showed no significant change as
O2 rose in all
feeding trials (Fig. 4,
Table 3).
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When the 12 kg feeding trial data were considered alone,
O2 changes were
independent of fH (P=0.13), while the 6 kg trials
had only a weak linear
fH/
O2
relationship [
O2
=(32.65fH±5.04)+(1855.77±391.41);
r2=0.28, P<0.01].
When all feeding data was considered, the relationship between fH
and O2 was weak
(Fig. 5;
r2=0.20, P<0.01) compared to when the animal
was fasting (r2=0.69, P<0.01). These two
regressions (i.e. fasting trials only and feeding trials only) were
significantly different (P<0.05), indicating that digestion of
food alters the
fH/
O2
relationship derived for fasted animals.
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Discussion |
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Factors affecting the
fH/O2
relationship
A number of factors might explain the variability in the measurements of
heart rate and oxygen consumption within and between individual animals
(Fig. 1). They include possible
changes or differences in stress level, fitness and other physiological
parameters of the study animals.
Considerable data on humans, dogs and rhesus monkeys have shown that
psychological stress brought on by threatening stimuli can lead to heart rate
variations that do not always correspond positively with variations in
metabolism (Johnson and Gessaman,
1973; Obrist et al.,
1974
; Stromme et al.,
1978
; Langer et al.,
1979
,
1985
). Stress (through the
release of epinephrine to beta-adrenoreceptors) can cause the heart rate to
increase beyond levels that can be predicted from measured oxygen uptake
(Blix et al., 1974
;
Stromme et al., 1978
;
Turner and Carroll, 1985
;
Wilhelm and Roth, 1998
).
Physical fitness, which increases the functional capacity of the
cardiovascular system, may also affect the
fH/O2
relationship. As fitness improves, the heart enlarges, ventricular stretching
is enhanced, and blood volume increases, resulting in an increased stroke
volume, allowing reduction in the heart rate for a given oxygen consumption
relative to that of more sedentary individuals
(Swaine et al., 1992
;
Plowman and Smith, 1997
;
Mtinangi and Hainsworth,
1999
).
Other factors for consideration are potential ontogenic changes, including
mass fluctuations and changes in the allometry of the circulatory system. The
potential of these changes to contribute to the variability in the
fH/O2
relationship is of concern given the extended period over which some of the
data were collected. Unfortunately, published studies specifically discussing
the effects of ontogenic factors on the
fH/
O2
relationship were not found. This includes a dearth of data on developmental
changes in the allometry of the heart, lungs or other components of the
circulatory system that would theoretically alter the
fH/
O2
relationship.
Changes in body mass might also alter the
fH/O2
relationship, particularly if these are due to changes in percentage of lipid
mass. Unfortunately, whether fat-free or absolute body mass is the primary
predictor of resting metabolic rate is the subject of considerable debate
(Cunningham, 1991
; Ferraro and
Ravussin, 1992), and changes in total body mass do not always reflect changes
in either lipid or lean tissue mass in pinnipeds. In the present study, the
strongest regression was obtained from the individual that had the greatest
changes in body mass (Male 1). However, changes in body mass may still have to
be taken into account when applying the heart-rate method over extended
periods.
It is not clear to what extent the above factors may have affected the
fH/O2
relationship of our study animals. The negative to positive trend in the
regression residuals (plotted in the order of data collection) of the female
Steller sea lions showed initially high heart rates for a given oxygen
consumption. This suggests either a decrease in stress, an increase in
fitness, or a decrease in body condition as our study progressed
(Fig. 2). We ruled out seasonal
changes as a factor, given that the bulk of the data were collected within a
short time frame (a month or less) and the overall residual trends did not
change when the data were separated into various time blocks. Despite a 50%
mass increase over the study period and data collection spanning nearly a
year, the regression of
O2 on
fH for Male 1 showed a high r2 value
and only a slight trend in the regression residuals. The lack of a trend and
high r2 in the regression on data from Male 2 suggests no
effect of stress, fitness, changing body composition or mass changes (which
were insignificant as in the females) over time. Data were collected in a
week, thus no seasonal effects were assumed. However, with several factors
potentially affecting the
fH/
O2
relationship, it is possible that concurrent contrary effects would result in
a constant
fH/
O2
relationship by chance in Male 2.
Stroke volume and oxygen extraction
As per Fick's original equation (Fick,
1870), the heart rate method assumes that stroke volume and
arteriovenous oxygen extraction remain constant or vary in a
predictable, systematic manner in order to reliably estimate
O2 from heart
rate measurements.
The r2 values from the regressions of
O2 on
fH suggest that fH explains 7178% of the
variation in measured
O2 for the
males, and 2145% of the increase in the females
(Table 2). However, a closer
examination of the data in Fig.
1 reveals that
O2 increased
approximately 2.54.0 times while fH only doubled
across the ranges recorded in the four sea lions. This suggests that the heart
rate data can physiologically explain only 3887% of the increase in
O2. A
systematically increasing stroke volume and/or tissue oxygen extraction might
explain the remaining increase in
O2 if heart rate
is truly, linearly related to
O2, which may or
may not be true in Steller sea lions.
Ideally, stroke volume and tissue oxygen extraction should be measured as
they have been in other mammals. In horses, steers, goats, calves and some
dogs, mass-specific stroke volume remains constant over a range of exercise
(Horstman et al., 1974;
Taylor et al., 1987
;
Jones et al., 1989
). Oxygen
extraction, however, increased with exercise in a systematic curvilinear
manner. In rats and some dogs, both stroke volume and extraction increased in
a linear fashion with exercise (Gleeson
and Baldwin, 1981
; Horstman et
al., 1974
). Similar changes in Steller sea lions (i.e. a
systematically increasing stroke volume and/or extraction) would help explain
the remainder of the increase in
O2.
Data from other diving pinnipeds is scarce and contradictory. Over a range
of workloads, harbour seals showed a slightly decreasing stroke volume while
surface-swimming. However, while swimming submerged, the seals showed a
constant stroke volume that was about half that observed during
surface-swimming (Ponganis et al.,
1990); oxygen extraction was not reported. California sea lions,
on the other hand, have been shown to maintain a constant stroke volume over a
continuous period of short submergence and surface-swimming events, regardless
of workload (Ponganis et al.,
1991
). Stroke-volume changes in Steller sea lions are probably
similar to those reported for California sea lions, since swimming in our
study involved short dive and surface events and the species are
evolutionarily related.
If it is true that stroke volume remains constant, extraction might be
responsible for the observed increase in
O2 that is not
explained by fH. However, without recorded values, this is purely
speculative. We would expect over the course of a dive that the
arteriovenous oxygen difference would change; thus, oxygen extraction
per heart beat might change. However, such a change may not be evident during
a swim trial that includes only very short dives. In the wild, Steller sea
lions dive an average of 46 min during foraging bouts and so the
validity of applying a swim-mill regression to free-ranging animals is
uncertain.
Steller sea lion regressions and data collection
A degree of variability in data collection is normal and does not mean that
the heart rate method is inadequate, especially relative to other available
techniques. It may have been possible to reduce some of the variation in the
Steller sea lion data set by experimentally collecting all data within 24 h.
This has been done previously in some captive marine bird and mammal studies,
where significant
fH/O2
relationships were obtained with minimal variation (r2
values were above 0.70) (see Williams et
al., 1991
; Butler et al.,
1992
; Bevan et al.,
1994
,
1995a
,b
).
Although prompt data collection on captive animals would be likely to reduce
variation due to development, fitness levels and stress, the application of
the regressions to wild Steller sea lions living in the open ocean will
probably be done over several days or months. Wild Steller sea lions would
experience such changes in physiological parameters throughout a monitoring
period. Thus, it is probably more meaningful to calibrate regressions on
captive animals over an extended time period, as we have done, rather than in
a single day.
Comparison with other methods and species
Studies on other species such as California sea lions
(Butler et al., 1992;
Boyd et al., 1995
), barnacle
geese (Nolet et al., 1992
),
gentoo penguins (Bevan et al.,
1995b
) and black-browed albatrosses
(Bevan et al., 1994
) have
concluded that heart rate is a good indicator of metabolism, despite
significant differences between slopes and intercepts of individual
regressions. These studies compared predicted to observed oxygen consumption
and found that heart rate could predict oxygen consumption with an error less
than or equivalent to that predicted by use of doubly labelled water. In
captive swimming California sea lions, doubly labelled water turnover
overestimated metabolic rate by as much as 36.4% on average (range 10%
to 86%), while heart rate overestimated by an average of only 2.7% (range
28% to +23%) (Boyd et al.,
1995
). However, both techniques were considered valid. Thus,
although regressions in our study differed among individuals, heart rate may
still yield a better estimate of oxygen consumption relative to the doubly
labelled water technique. However, validation experiments to determine the
mean regression's ability to accurately estimate metabolism are still needed
before it can be applied with confidence to estimate the mean metabolism of
groups of Steller sea lions in the field.
The mean
fH/O2
regression,
O2
=(71.3fH±4.3)(1138.5±369.6),
determined from the four Steller sea lions in our study had a reasonably tight
fit to the data (r2=0.69)
(Fig. 3A). Re-running the mixed
linear models to determine a mean regression with oxygen consumption measured
in ml O2 min1 kg1 for
comparison with other marine mammal studies resulted in the equation
O2
=(0.19fH±0.01)(4.12±1.3). This
regression is different from that of other marine mammal species, although it
is most similar to other otariids, and suggests that regressions of
fH and
O2 may be
species-specific (Fig. 6). As
expected from their larger body mass, males generally consumed less
O2 kg0.60 of mass than the females
(Fig. 3A), indicating that
there may even be separate regressions for the sexes, an idea suggested by
Hurley (1996
) with California
sea lions that should be explored further.
|
The effect of feeding
As seen in previous experiments, oxygen consumption of the sea lion
continued to rise over all 3 h feeding runs regardless of meal size,
indicative of the heat increment of feeding
(Blaxter, 1989;
Rosen and Trites, 1997
).
However, heart rate increased in only one 12 kg feeding run, and either
remained unchanged or decreased over time during the other 6 and 12 kg feeding
trials (Fig. 4,
Table 3).
Unlike many human studies where the haemodynamic response to feeding may
continue for hours, haemodynamic variables in other mammals (dogs, calves and
pigs) return to baseline values at the end of feeding
(Fronek and Stahlgren, 1968;
Houpt et al., 1983
;
Kelbaek et al., 1989
). In
those studies where cardiac output increased with postprandial metabolism,
there was also considerable conflicting data on whether increased stroke
volume or heart rate was the major contributor
(Kelbaek et al., 1989
;
Waaler et al., 1991
;
Muller et al., 1992
;
Sidery and MacDonald, 1994
).
In young lambs, oxygen extraction appeared to be responsible for the increase
in
O2.
Additional potential haemodynamic responses included increased oxygen
extraction (Grant et al.,
1997
) and the redirection of blood flow from other vascular beds
in the body to the digestive organs (Yi et
al., 1990
).
Regressing oxygen consumption on heart rate with data collected after 12 kg
feedings failed to produce a significant relationship. Data from the 6 kg
feedings provided only a weak relationship. Regressing
O2 onto
fH from all feeding trials (both 6 and 12 kg) yielded a
poor relationship that was significantly different from the fasting regression
(Fig. 5). The above findings
indicate that digestion alters the
fH/
O2
relationship when compared to a fasting condition. Curiously, increases in
rates of oxygen consumption induced in king penguins through increased thermal
challenges also failed to induce comparable changes in heart rate
(Froget et al., 2001
).
We were unable to properly explain the effect of feeding on the
relationship between fH and
O2 with our
limited data. Our results are included here only to draw attention to the
possibility that feeding may alter the relationship. Further study examining
temporal effects with a larger sample size and longer trials is needed.
Consideration should also be given to studying feeding while swimming at
various speeds to further elucidate the behavior of the feeding regression at
the higher levels of oxygen consumption and heart rate that are experienced in
the wild.
Captivity versus free-ranging environment
The assumption that the
fH/O2
relationship determined from captive animals is similar to that existing in
free-ranging animals warrants discussion. Accurately calibrating a
relationship in free-ranging animals undergoing completely natural,
undisturbed behaviour is currently difficult, if not impossible. We do not
know to what extent our results were affected by the confining nature of the
swim mill and metabolic chamber. The dive intervals of the animals in our
study were too short to result in a perceptible bradycardia. Therefore, it is
difficult to speculate how this and other aspects of the dive response (e.g.
vasoconstriction) would affect the relationship between
O2 and
fH. An obvious next step would be to collect similar data from
animals swimming in a much larger pool equipped for direct respirometry, or
swimming beneath a respirometry hood alongside a boat in the open ocean. Both
approaches offer reduced confinement and may yield more natural behaviour.
To simulate field conditions more closely, food intake could be varied and live fish could be introduced. Regressions determined from such data could then be used to estimate metabolism from heart rate in free-ranging animals with more confidence.
In conclusion, our study provides important basic information on an otariid
species that could be useful in comparative studies. However, our results
raise a number of questions regarding the potential effects of gender, season,
age class, digestive state, stress and body condition on the
fH/O2
relationship that necessitate more detailed examination. Using regressions
determined from captive animals to predict metabolic rate from heart rate in
free-ranging animals should therefore be approached with caution.
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Acknowledgments |
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References |
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