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First published online October 31, 2008
Journal of Experimental Biology 211, 3573-3580 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.023655
Metabolic costs of foraging and the management of O2 and CO2 stores in Steller sea lions
1 Marine Mammal Research Unit, Fisheries Centre, Room 247, Aquatic Ecosystems
Research Laboratory, University of British Columbia, Vancouver, BC, V6T 1Z4
Canada
2 Department of Biomedical Engineering, Linköpings Universitet, 581 85
Linköping, Sweden
3 Zoology Animal Care, 6199 South Campus Road, University of British Columbia,
Vancouver, BC, V6T 1Z4 Canada
* Author for correspondence (e-mail: andreas_fahlman{at}yahoo.com)
Accepted 15 September 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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O2/CO2)
was significantly lower during spontaneous trials compared with conditioned
trials. DMR was significantly higher during spontaneous trials and decreased
exponentially with dive duration. A similar decrease in DMR was not as evident
during conditioned trials. DMR could not be accurately estimated from the
surface interval (SI) following individual dives that had short SIs (<50
s), but could be estimated on a dive by dive basis for longer SIs (>50 s).
DMR decreased by 15%, but did not differ significantly from surface metabolic
rates (MRS) when dive duration increased from 1 to 7 min. Overall,
these data suggest that DMR is almost the same as MRS, and that
Steller sea lions incur an O2 debt during spontaneous diving that
is not repaid until the end of the dive bout. This has important consequences
in differentiating between the actual and `apparent' metabolic rate during
diving, and may explain some of the differences in metabolic rates reported in
pinniped species.
Key words: field metabolic rate, diving physiology, marine mammal, hypometabolism, O2 debt, CO2 exchange, physiological plasticity
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Considerable attention has been given over the past three decades to
measuring field metabolic rates of foraging animals using two techniques
– the heart rate technique and use of stable isotopes (doubly labelled
water) (Sparling et al.,
2008
). Recently Fahlman et al.
(Fahlman et al., 2008b) showed
that activity was also a reliable proxy for the metabolic costs of Steller sea
lions (Eumetopias jubatus Schreber 1776) during diving and while at
the surface. One disadvantage with both the heart rate technique and the
activity method for estimating field metabolic rate is that they need lengthy
calibration studies to establish the relationship between metabolic cost and
heart rate or activity for different species and for different activities
(e.g. swimming, walking and diving).
Respirometry is the `gold standard' for measuring energetic costs in
animals performing a variety of activities and is necessary for validation of
indirect methods, e.g. doubly labelled water, heart rate technique and
activity. However, it has been particularly challenging to measure metabolic
rates of animals while diving under realistic conditions. Several different
approaches have been used to overcome these logistical difficulties. One
approach has been to record gas exchange for animals contained in a body of
water that is covered naturally by ice
(Kooyman et al., 1973;
Ponganis et al., 1993;
Williams, 2001) or
artificially with grates (Sparling and
Fedak, 2004), forcing the animal to surface inside a respirometer
at a pre-determined place. Another approach has been to use trained animals in
a captive (Hurley, 1996) or
open ocean setting (Fahlman et al.,
2008b). This latter method has been used in a series of recent
studies to directly measure the O2 uptake and CO2
production rates following dives (Fahlman
et al., 2008a; Fahlman et al.,
2008b; Hastie et al.,
2006a; Hastie et al.,
2006b).
Trained Steller sea lions in a previous open ocean study performed repeated
foraging dives on their own volition and remained at the surface in the
respirometry dome for as long as they wished between dives
(Fahlman et al., 2008a). Each
of the animals remained within the dome following the last dive in a series of
dives (bout) until the O2 level had returned to the pre-dive level.
The estimated metabolic rate of a dive event (dive + surface interval; DMR)
was found to decay exponentially with dive duration suggesting that longer
dives cost proportionally less energy
(Fahlman et al., 2008b). In
addition, the first dive in a series was also found to have the lowest
metabolic cost compared with the last dive that had the highest DMR and had a
longer recovery period. This indicated that perhaps the animals terminated
their surface intervals before their O2 stores were fully
restored.
The diving studies suggested that Steller sea lions were diving with a
slight O2 debt throughout their dive bouts that was only paid back
during the prolonged recovery period at the end of the trial. Similar results
were reported for Weddell seals (Leptonychotes weddelli)
that took between 3 and 5 min for expired O2 to return to pre-dive
levels (Kooyman et al., 1973;
Ponganis et al., 1993).
Kooyman et al. (Kooyman et al.,
1973) suggested their results indicated that the animals incurred
an O2 debt during a dive bout that was not completely repaid during
the short surface intervals between dives but remained outstanding until the
animal incurred an extended recovery period at the end of the bout.
Consequently, estimating DMR by respirometry is complicated by the fact that
the apparent rate of oxygen uptake
(O2) during
individual repeated dives is lower than the actual metabolic rate.
The dive behaviours observed for Steller sea lions and Weddell seals are
consistent with certain optimal foraging models that assume that the length of
the surface interval is determined by the need to replenish depleted oxygen
stores (Kramer, 1988).
However, recent empirical research suggests that removal of CO2 is
the main driving force regulating surface interval duration
(Boutilier et al., 2001).
Although insufficient uptake of O2 would reduce the aerobic dive
duration, incomplete removal of CO2 leads to a continuous increase
in blood and tissue CO2 partial pressure
(PCO2)
(Fahlman et al., 2008c). The
surface interval is therefore a dynamic state determined by the need for
sufficient gas exchange, food availability and predator avoidance.
Physiological plasticity enables diving animals to enhance gas exchange during a surface interval and maximizes time underwater, thereby enhancing foraging efficiency. However, such adaptations complicate the ability to estimate the energetic cost of foraging since repeated dives in a dive bout may not be independent samples but may have to be considered collectively. Our study therefore aimed to improve understanding of how pinnipeds manage the O2 debt during a dive bout while seeking to develop a method that accounts for the O2 debt and accurately estimates the true metabolic costs of foraging.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Respirometry studies
All trials were performed in the morning and the sea lions were between 16
and 20 h postprandial. Before trials, each sea lion was weighed (±0.5
kg) and fitted with a webbed body harness. A VHF transmitter was attached to
the harness and was used to locate the sea lion in the event of it swimming
out of the trial area.
The animals were transported in a specially modified boat from their holding pen to the trial area, where they could dive from a floating respiratory dome to an underwater feeding tube placed at depth. Another research boat carrying the respirometry equipment and towing a floating barge was anchored in the trial area. The barge contained a rectangular hole through which a large wire cage (152 cmx152 cm) was placed in the water. The cage floor could be opened to allow the sea lion to enter and breathe in the dome. Closing the cage door made it possible to voluntarily contain the sea lion for short periods of time to measure metabolic rate while the animals were at the surface. Animals were seldom quiescent when in the cage. Thus, surface metabolic rate (MRS) varied and was not resting or basal metabolic rate.
A transparent Plexiglas dome (either 100 or 200 l internal volume) was placed above the cage to collect respiratory gases (O2 and CO2). A mass flow controller (Model 500H, Sable Systems, Las Vegas, NV, USA) pulled 475 l min–1 of air through the dome. This mass flow meter automatically corrected flow rates to standard temperature and pressure (STP) in the case of variations in temperature and barometric pressure. A subsample of the air was pulled through a canister of anhydrous CaSO4 (Drierite, W. A. Hammond, Xenia, OH, USA) to a paramagnetic O2 (FC-1 B O2, Sable Systems, Las Vegas, NV, USA) and an infrared CO2 analyzer (CA-10A, Sable Systems, Las Vegas, NV, USA). Air flow rate as well as O2 and CO2 levels were sampled at 2 Hz and saved to a laptop computer.
The gas analyzers were calibrated before and after a dive trial with ambient air (20.94% O2) and 1.0% CO2 in N2 from a commercial gas mixture (Praxair, Canada). Temperature (°C) and humidity (%) of the excurrent gas was measured using a commercial sensor (Springfield Precise Temp., Springfield Precision Instruments, Wood Ridge, NJ, USA). Average respirometer temperature was 16.6±6.1°C (range: 0.8–28.5°C; N=186), humidity was 77±15% (range: 35–100%) and barometric pressure was 102.0±0.7 kPa (range: 99.5–103.9 kPa). All flows were corrected to STP dry (STPD).
The accuracy in measured
O2 and rate of
CO2 production
(CO2) was
determined by simultaneous N2- and CO2-dilution tests
(Fahlman et al., 2005;
Fedak et al., 1981) and
estimated values were within 4% of the measured values. Addition of
CO2 confirmed that minimal amounts of CO2 were dissolved
and lost in the seawater. The effective volume of the system was either 120 l
or 220 l, including the volume of the respirometer (100 or 200 l) and the
plastic hose to the analyzers (20 l). With a flow rate of 475 l
min–1, this gave time constants of 0.25 and 0.46 min for the
small and large domes, respectively. The time required to reach a 95%
fractional transformation to a new steady state was 3.2 times the time
constant, or 48 s (small dome) and 90 s (large dome)
(Fahlman et al., 2005).
A dive trial consisted of either a single dive or a bout of repeated dives (2–15 dives) to a simulated foraging patch. A tube and pump system allowed fish (previously frozen herring) to be delivered to various depths at different rates (0–12 fish min–1) simulating the sea lion feeding on food patches of varying densities. Before diving, the sea lion was instructed by a trainer to enter the respirometry dome. Once inside the cage, the door was closed and the animal remained in the dome for 6–10 min while MRS was measured. Duration was extended if steady values of O2 and CO2 were not recorded during the last 2 min. The sea lion was then instructed to swim to the end of the feeding tube that was placed at depths between 10 m and 50 m. The sea lion returned to the metabolic dome at the end of each dive.
Two different diving protocols were used – `spontaneous' and `conditioned' trials. For spontaneous dive trials, the sea lion determined the duration of the dive and the surface interval without instructions from the trainer. During conditioned dive trials, the door was closed between dives and the sea lion remained in the respirometry dome until the O2 and CO2 returned to pre-dive levels, usually between 5 and 8 min. For both experimental protocols, the sequences of dive and surface intervals were repeated with two to eight dives in each trial (one trial per day) and the last dive was followed by a recovery period in the respirometry dome (6–10 min).
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Average O2
and CO2 was
calculated by integrating the instantaneous oxygen consumption rate over the
entire post-dive surface interval, and dividing this by the dive event
duration (Fahlman et al.,
2008b). All surface intervals were >60 s in a conditioned dive
series and >5 s in a spontaneous dive series.
Water temperatures at the surface and at the end of the feeding tube were monitored during each trial using remote temperature loggers (Onset Computer, Pocasset, MA, USA). Surface temperature ranged from 4.3 to 18.9°C (mean 12.4±4.0°C, N=159), and the range at depth was between 5.7°C and 17.3°C (mean 11.1±2.3°C, N=153). Water current at the surface and at depth was scored by eye as low, medium, or high.
Data assessment and statistical analysis
Mixed models regression was used to determine which model best described
the relationship between MRS or DMR and the independent variables.
Independent variables included ten experimental variables (dive duration,
depth, Mb, surface interval, water current at depth, water
temperature at the surface or at depth, respirometer temperature, the dive
number in a series of dives and respirometer humidity) as independent fixed
covariates and three factors (current, with or without harness, and
spontaneous or conditioned trial). Initially, a univariate analysis on each
independent variable was performed, and only those variables with
P<0.20 (Wald's tests) were considered in the multivariate
analysis. Stepwise techniques were used to search for the best model. Nested
regressions were compared with each other using the Akaike Information
Criterion (AIC) (Akaike, 1974)
and log-likelihood ratio testing. The models were analyzed and corrected for
departures from normality, outliers, and linearity as detailed by Neter et al.
(Neter et al., 1996).
Statistical analyses were performed using R (version 2.5.1, The R foundation
for Statistical Computing). Acceptance of significance was set at
P<0.05, and 0.05<P<0.1 was considered significant
for trends. All values were reported as means ± s.d., unless otherwise
specified.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Average dive durations and depths for conditioned dives (2.28±1.53 min and 20.1±14.3 m, respectively; N=479) were significantly longer and deeper than spontaneous dives (0.97±0.83 min and 11.5±6.3 m; N=717; P<0.01, mixed model ANOVA). Dive duration increased with depth (1.2±1.0 min at 10 m and 4.0±1.5 min at 50 m, P<0.01, mixed model ANOVA).
Rate of oxygen consumption (O2)
Fig. 1 shows a
representative spontaneous dive bout of five repeated dives to 40 m, and six
surface intervals during which
O2 and the
respiratory exchange ratio (RER,
CO2/O2)
were measured. Average surface metabolic rate for all animals was
1.45±0.44 l O2 min–1 (N=191;
Table 1) and did not differ
significantly between spontaneous (1.41±0.38 l O2
min–1, N=70) and conditioned (1.48±0.48 l
O2 min–1, N=121) trials (mixed model
ANOVA, LL-ratio test=1.90, P>0.1, 1 d.f.).
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The average metabolic rate during a dive event was 1.65±0.66 l O2 min–1 (N=1142), and was significantly higher for spontaneous dive events (DMRSpon) than for conditioned dives (DMRCond; mixed model ANOVA, LL-ratio test=15.9, 1 d.f., P<0.01) (Table 1). RER was higher for conditioned trials (normally falling within a range of 0.7–1.0, but occasionally reaching values as low as 0.6 and as high as 1.05). During spontaneous trials, RER was within the range 1.82 to 0.34. RER was also more variable during spontaneous trials compared with conditioned trials (Table 1). RER was low after a sea lion surfaced and began breathing, usually less than 0.7, and increased as the surface interval progressed (Fig. 1B). RER increased immediately before diving, which is suggestive of pre-dive hyperventilation (Fig. 1B). There was a positive correlation between RER and the surface interval (SI) for both conditioned and spontaneous trials (P<0.01). However, there was no relationship between RER and SI for SIs >1.7 min (P>0.05).
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 | (1) |
For all dive data, the best model predicting DMR included
log(Mb), depth (D), dive duration (DD), duration of SI and
the order of repeated dives (DiveNo). This was:
 | (2) |
For conditioned dives (dives with an SI >50 s), however, the best model
included only DD, log(Mb) and the water temperature at
depth (Tdepth):
 | (3) |
In all analyses, log10-transformed Mb was significantly correlated with log10-transformed MRS and DMR. The mass exponents for Eqns 1 and 3 were not significantly different from 1. Mass-specific surface metabolic rates (sMRS) and mass-specific dive event metabolic rates (sDMR) were thus estimated as MRSMb–1 and DMR Mb–1, respectively (Figs 2 and 3).
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O2 and the last
dive had the highest. There was also a positive relationship between estimated
O2 and the SI.
sDMR for all dives decreased exponentially towards sMRS with
increasing dive duration, and at times fell below sMRS
(Fig. 2). However, separating
the data into conditioned and spontaneous dives showed only
sDMRSpon decreased exponentially whereas there was only a weak
indication of a decrease in sDMRCond with dive duration
(Fig. 2). For dives longer than
1 min, sDMRSpon was significantly lower than sDMRCond
(P<0.01, t-test) and sDMRSpon commonly
decreased below sMRS (Fig.
2). Variability in sDMRSpon was larger than
sDMRCond, although variability decreased for sDMRSpon as
the SI increased (Fig. 3).
Rate of CO2 production (CO2)
Average surface
CO2 was
1.38±0.44 l CO2 min–1 for all trials and
did not differ between spontaneous (1.30±0.34 l CO2
min–1) or conditioned (1.42±0.47 l CO2
min–1) trials (P>0.1). Diving
CO2 decreased
exponentially with dive duration for spontaneous trials but it remained more
or less constant for conditioned trials
(Fig. 4A). For SI<1 min
(spontaneous dives), diving
CO2 was more
variable compared with conditioned trials
(Fig. 4B).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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) showed that the O2 taken up during the recovery
period after a forced submersion was less than expected based on the
assumption that the metabolic rate during the dive and surface interval would
be similar to the resting metabolic rate. Scholander
(Scholander, 1940) concluded
that this indicated diving induced hypometabolism, a probable adaptation in
diving animals to extend aerobic dive duration by reducing oxygen consumption
rates. Studies on voluntarily diving California sea lions (Zalophus
californianus) (Hurley and Costa,
2001) and Steller sea lions
(Hastie et al., 2007)
confirmed that the rate of O2 uptake during a dive event was lower
than the resting rate at the surface. O2 uptake rates during dive
events in California sea lions decreased most noticeably for dives longer than
3 min (Hurley and Costa,
2001). Although initial studies with Steller sea lions did not
indicate a difference in
O2 with duration
spent underwater (Hastie et al.,
2007), maximum dive durations were only 3 min. However, later
studies reported an exponential decrease in O2 uptake with
increasing dive duration (Fahlman et al.,
2008b), and that a reduction in DMR below MRS was most
pronounced and consistent during dives longer than 3 min [see
Fig. 2 in Fahlman et al.
(Fahlman et al., 2008b)].
Repeated dives and the effect of the O2 debt on DMR
Fahlman et al. (Fahlman et al.,
2008b) noticed that the first dive in a series of repeated
spontaneous dives had the lowest DMR whereas the last dive had the highest
DMR. Other studies have adjusted for this phenomenon by only analyzing dives
that have post-dive recovery periods long enough for O2 level to
return to within 2% of the pre-dive resting rate
(Williams et al., 2004). This
approach assumes that each dive performed in a bout is independent. However, a
series of repeated dives in a bout followed by a short surface interval may
lead to continuing changes in O2 stores and/or accumulation of
CO2 and its by-products (lactate, acid base balance disturbance).
Therefore, the last dive before an extended surface interval may be affected
by the previous dive sequence and estimates of DMR may be biased if only this
last dive is analyzed.
We hypothesize that the much lower DMR of the first dive event reflects incomplete restoration of O2 stores, and that the sea lions that undertake a series of continuous dives do so with an O2 debt that is incurred during the first dive. We investigated this by comparing spontaneous diving trials to trials consisting of a series of dives where the sea lion stayed in the respirometry dome until the O2 had returned to baseline levels between dives (conditioned dive). Results from these conditioned trials showed that the O2 uptake rate during repeated dives was independent of the order of the dive.
The explanation for such a pattern in energy cost with repeated dives relies on a strategy of minimizing time spent on the surface and maximizing time at depth. Blood and tissues should be fully saturated with O2 before the first dive in a dive bout, with levels of PO2 decreasing during the first dive. The overall decline of PO2 for a completely aerobic dive will depend on the metabolic rate of the tissues and the dive duration.
As the animal returns to the surface and begins breathing, O2
will be taken up and CO2 removed. Assuming no pulmonary diffusion
limitations, uptake of O2 into the blood is governed by:
 | (4) |
is a time
constant that determines the time to equilibrium. The time constant is
physiologically relevant and related to the solubility of the gas and the
blood flow rate.
Sea lions have a modified respiratory system allowing most of the air in
the lungs to be exchanged during a single breath
(Denison and Kooyman, 1973).
Therefore, dead space mixing can be assumed to be negligible and
PLO2 close to the ambient
PO2. Assuming that lung blood flow is constant
during a surface interval, O2 uptake will depend on the difference
between PvO2 and
PLO2.
When the animal returns to the surface there is a large
PO2 gradient between lung and mixed venous
blood, favouring diffusion of O2 into the blood. The large
PO2 gradient and the shape of the O2
dissociation curve allow large amounts of O2 to be taken up with
small changes in PvO2.
PvO2 increases as O2 is taken up by
the tissues, thereby reducing the partial pressure gradient and the
O2 uptake rate. For this reason, complete restoration of the
O2 stores is not as profitable due to the temporal decrease in the
O2 uptake rate (Kramer,
1988).
Without complete restoration of the O2 stores, the total
O2 uptake after the first dive is lower than the actual
O2 used during the dive event. During subsequent dives, the surface
interval is adjusted to maximize the O2 uptake rate and restore the
O2 that was used during the dive to avoid an accumulating
O2 debt. In other words, the animal will work to restore
O2 at the steep part of the O2 dissociation curve where
O2 gain is maximized while at the same time minimizing the surface
interval. Consequently, small changes in surface interval duration may result
in large differences in the total amount of O2 taken up during.
This explains the large variability in estimated DMR for short dives which
have a short surface interval (Fahlman et
al., 2008b).
During spontaneous diving bouts, the O2 uptake during the
surface interval depends on the previous history of dives and makes it
difficult to accurately estimate the energetic cost of foraging in Steller sea
lions on a dive-by-dive basis. Attempting to estimate the costs on a
dive-by-dive basis would artificially decrease the mean and increase the
variability of the DMR estimate for short dives with short surface intervals
(Kooyman et al., 1973).
Including the end-bout recovery period makes it possible to estimate the
overall metabolic cost of an entire bout, but without an end-bout recovery
period, a portion of the O2 debt will not be accounted for and the
average metabolic rate for the bout will appear lower than the actual cost.
However, only analyzing dives with a long surface interval may overestimate
the DMR. As a consequence, respirometry studies on continuously diving animals
need to consider the entire dive bout as a functional unit for the purpose of
estimating DMR.
Does CO2 removal determine the length of the surface interval?
Our respirometry system did not allow measurement of breath-to-breath gas
exchange unlike that used by Boutilier et al.
(Boutilier et al., 2001).
However, our instantaneous RER values were consistently <0.7 after the sea
lion surfaced and then increased to >1.0 as the surface interval progressed
(Fig. 1). This agrees with the
RERs reported for the harbour porpoise (Phocoena phocoena) and grey
seal (Halichoerus grypus)
(Boutilier et al., 2001)
suggesting that mostly O2 is exchanged during the first couple of
breaths followed by rapid exchange of CO2 towards the end of the
surface interval.
Although our data indicate that re-adjustment of the O2 stores
is not the principal variable that determines the length of the surface
interval, O2 stores are nevertheless not fully readjusted at the
end of SIs<50 s (Boutilier et al.,
2001). Instead, sea lions dive with a small O2 debt
that is not paid off until the end of the bout, similar to Weddell seals
(Kooyman et al., 1973). The
O2 debt takes >50 s to fully restore and most of the surface
intervals in a dive bout during spontaneous trials were shorter than this.
Despite this, the O2 stores are sufficiently restored within a few
breaths to allow the sea lion to dive without significantly altering the
aerobic dive duration. Following this, O2 is slowly taken up while
CO2 is still removed and the surface interval ends when sufficient
CO2 has been removed, so that consecutive dives do not lead to a
significant accumulation of CO2. Sea lions therefore strive to
optimize uptake of O2 while also trying to remove sufficient
CO2 to be in a dynamic equilibrium that does not result in a
continuous reduction in O2 stores or accumulation of
CO2. This agrees with the output of optimal foraging models when
applied to diving birds (Halsey and
Butler, 2006).
During a few spontaneous dive trials, the sea lions dived after extremely short surface intervals (<10 s) for the entire diving bout. For such a dive pattern, O2 may determine the length of the surface interval, leading to accumulation of CO2. Such dive behaviour may be beneficial if a sea lion encounters a particularly dense prey patch, but would inevitably lead to elevated tissue and blood PCO2. However, elevated tissue and blood PCO2 will ultimately force an animal to end a dive bout.
DMR and MRS versus BMR; evidence for hypometabolism?
Blood and tissues are saturated with O2 before each conditioned
dive. The O2 uptake during the recovery phase after a dive is
therefore a direct reflection of the resting O2 uptake rate during
the surface interval and reloading of the tissue and blood O2 that
was used during the dive. This represents the true O2 uptake rate
during the dive event and is therefore a better reflection of the actual
energetic cost of the dive. In addition, the cost is independent of previous
dives and only depends on activity during that particular dive
(Fahlman et al., 2008b). The
results from the conditioned trials are particularly interesting as they
suggest that diving metabolic rate is not much different from the pre-dive
sMRS, although sDMR decreases below sMRS during long
dives (Fig. 2).
We did not detect any changes in MRS between dives during
conditioned trials and there were no differences in pre-dive MRS or
the MRS during the recovery phase following a bout as would have
been expected if the sea lions had begun to digest their food (heat increment
of feeding). Others have measured a significant increase in the metabolic rate
of pinnipeds while resting on land several hours after their last dive. In
particular, Sparling et al. (Sparling et
al., 2007) noted that digestion was inhibited in grey seals
throughout a foraging bout and that MRS did not increase until long
after the dive bout had ended. Given that it takes more than 30 min for
MRS to increase in Steller sea lions after a meal
(Rosen and Trites, 1997) and
that the resting period that ended the dive bouts of the sea lions in our
study was a maximum of 10 min, the increase we recorded in DMR associated with
the last dive of each bout cannot be attributed to digestion. Instead, our
data are consistent with the finding of Sparling et al.
(Sparling et al., 2007) that
diving animals defer digestion while foraging.
The minimum measured MRS values were 0.90 l O2
min–1 for a 219.5 kg sea lion, 0.71 l O2
min–1 for a 166.2 kg animal and 0.71 l O2
min–1 for a sea lion weighing 129.9 kg. These values were 55%
to 85% higher than those predicted from Kleiber's equation for basal metabolic
rate (Kleiber, 1961). Average
MRS values, however, were as much as 230% higher than those
predicted by Kleiber (Kleiber,
1961). However, the pre-dive MRS values in water were
lower for both sea lions F97SI and F00BO than their previously MRS
values measured in air in previous experiments (1.92 l O2
min–1 and 1.36 l O2 min–1,
respectively) (Hastie et al.,
2007). The in-water MRS values were similar to those
reported for grey seals (Sparling and
Fedak, 2004), but slightly lower than the results reported for
California sea lions (Hurley and Costa,
2001).
Some of the differences between MRS values for grey seals,
California sea lions and Steller sea lions may be due to differences in
thermoregulatory costs. Seasonal air and water temperatures in our study of
Steller sea lions (Vancouver, Canada) and that of grey seals (St Andrews,
Scotland) were similar. However, the MRS for California sea lions
was measured at higher water temperatures (15–20°C)
(Hurley and Costa, 2001)
compared with the water temperatures in our study (4.3–18.9°C). The
relationship between MRS and water temperature was negative
(Eqn 1) with MRS
falling by 24% when resting in water at 18.9°C compared with 4.3°C.
Despite a shorter surface resting period and a water temperature as low as
4.3°C, sMRS for female Steller sea lions was lower (8.4 ml
O2 min–1 kg–1) than that measured
in California sea lions. Thus, our data suggest that the sMRS in
female Steller sea lions at water temperatures ranging from 4°C to
19°C is lower than for California sea lions.
Kooyman (Kooyman, 1989)
defined hypometabolism as a metabolic rate that is lower than that measured
under standard conditions of resting in a post-absorptive state. Average DMR
of the Steller sea lions decreased by 
8% when dive duration was extended
from 1 min to 6 min (Fig. 3;
Eqn 3). Overall, 32%
(N=160) of all conditioned dives were below MRS and 24%
(N=118) were below minimum MRS
(Table 1; MRSmin)
for each sea lion. Results from the conditioned dives showed that the
energetic cost of a dive event was only 8% higher than the average
MRS. Thus, DMR did not differ substantially from MRS
(Fig. 3).
Our results agree with those of others indicating that DMR is close to
MRS (Hurley and Costa,
2001; Sparling and Fedak,
2004). However, the relative decrease in DMR compared with
MRS is much less in our study than values reported for grey seals
and California sea lions. This could highlight methodological differences in
the respective experiments. In our study, the animals were unrestrained, while
the grey seals were active but restrained by the size of the pool, and the
California sea lions were inactive while submerged (see below).
The 8% decrease in DMR observed during longer dives in our study could be
due to reduced cardiac work by a reduction in heart rate, i.e. the dive
response. In Weddell seals, the metabolic cost of the heart was estimated to
be 12% of the total energy consumption
(Davis and Kanatous, 1999).
Assuming that cardiac work is directly related to heart rate means that
lowered heart rates would reduce overall metabolic rate by 6% based on a 50%
reduction in heart rate reported during a 6 min dive in California sea lions
(Ponganis et al., 1997).
Another possibility is that activity is lower during longer dives, thereby
decreasing overall DMR (Fahlman et al.,
2008b). This may facilitate a reduction in DMR and allow the sea
lions to dive for longer without exceeding the calculated aerobic dive limit
(cADL). Consequently, future studies should measure underwater activity
concurrently with DMR to resolve whether the decrease in DMR during longer
dives is a true hypometabolic state or whether it is caused by a behavioural
adjustment in activity.
The decrease in DMR with dive duration in our study was not as large as was
seen in California sea lions (Hurley and
Costa, 2001). One possible reason for this difference between
studies is that the sea lions we used swam freely and would have expended more
energy while swimming. We have previously shown that activity is a good
indicator of DMR (Fahlman et al.,
2008b). Therefore, any metabolic suppression induced by greater
dive duration may have been partly offset by the activity level during the
dive, potentially explaining why DMR did not decrease with dive duration as
much as in inactive California sea lions
(Hurley and Costa, 2001).
Depth, and thereby the overall distance that the sea lion had to swim to
the prey patches we created, did not affect foraging costs. We previously
showed that metabolic savings by passive gliding during descent were similar
to the additional cost of active swimming during ascent
(Fahlman et al., 2008b), which
explains why the metabolic cost of different dives to at least 50 m did not
differ. During shallow dives, diving lung volume will significantly affect
buoyancy and species that principally dive to shallow depths may adjust the
inhaled air volume to adjust buoyancy
(Fahlman et al., 2008a). During
deeper dives, lung compression will reduce the effect of inhaled air volume on
buoyancy (Bostrom et al.,
2008), explaining why our results differ from those of deeper
diving species (Williams et al.,
2004; Williams et al.,
1999). In fact, a previous study showed that New Zealand sea lions
(Phocarctos hookeri) that dived to deeper depths spent more time
gliding and had a lower field metabolic rate than individuals that made
shallow dives (Costa and Gales,
2000).
Conclusions
In summary, the exchange of O2 and CO2 during a
surface interval after breath-hold diving is a dynamic process. The first dive
in a series of repeated spontaneous dives has the lowest O2 uptake
rate, whereas the last dive has the highest. This is because of adjustments of
O2 stores. In addition, variability in estimated DMR decreases with
dive duration and surface interval duration during spontaneous dives,
suggesting that estimated DMR from a dive with a short surface interval is
unreliable. It is therefore difficult to accurately estimate the metabolic
cost of an individual dive using exchange of O2 when the surface
interval is short between repeated spontaneous dives. Rather, O2
exchange can be used to estimate metabolic cost of the entire diving bout. For
dives where the surface interval is more than 50 s, O2 uptake rate
is a suitable estimate of the energetic cost of the dive event in adult female
Steller sea lions. The RER increases throughout the surface interval,
reflecting an initial rapid exchange of O2 followed by mobilization
of tissue and blood CO2 that shows a delayed removal. The duration
of the surface interval is determined by the dual need to restore sufficient
O2 and remove CO2 so that neither becomes limiting. The
delayed removal of CO2 means that the surface duration is in most
cases determined by the need to remove CO2. When accounting for the
O2 debt, DMR appears to be almost the same as MRS in
Steller sea lions. DMR decreases with increasing dive duration, but it is not
clear if this is secondary to a reduction in activity or reflecting a true
hypometabolic state.
LIST OF ABBREVIATIONS
CO2/O2)
CO2
O2
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Acknowledgments |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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