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First published online June 15, 2006
Journal of Experimental Biology 209, 2576-2585 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02273
The effect of myoglobin concentration on aerobic dive limit in a Weddell seal
Department of Marine Biology, Texas A&M University at Galveston, Galveston, TX 77551, USA and Department of Wildlife and Fisheries Sciences, Texas A&M University, College Station, TX 77843, USA
* Author for correspondence (e-mail: traywright{at}hotmail.com)
Accepted 18 April 2006
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Key words: Weddell seal, Leptonychotes weddellii, myoglobin, diving, ADL, postabsorptive, postprandial
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;
Williams, 2001). For Weddell
seals, these physiological adaptations and behavioral strategies result in an
aerobic dive limit (ADL) of about 20 min
(Davis and Kanatous, 1999;
Ponganis et al., 1993a; Kooyman et al.,
1980).
If body oxygen stores are the primary physiological limit to dive duration,
why are they not larger? During the evolution of marine mammals, what
physiological factors may have set the upper limit to blood volume, Hct and
muscle Mb concentration? Weddell seals have a blood volume as high as 21% of
their body mass (Ponganis et al.,
1993), almost three times larger than predicted for a terrestrial
mammal of the same size (Stahl,
1967). The upper limit to blood volume may be a compromise between
increasing oxygen stores and the resultant increase in body mass or abdominal
volume.
The Hct of Weddell seals (ca. 60%), which is 1.5-times higher than in most
terrestrial mammals, increases blood oxygen stores and maintains convective
oxygen transport to organs and tissues as the partial pressure of oxygen in
the blood decreases during diving. However, the increased Hct also increases
blood viscosity, circulatory resistance and heart work
(Elsner and Meiselman, 1995).
As a result, the large spleen of Weddell seals sequesters red blood cells,
lowers the hematocrit, and decreases blood viscosity when they are at the
surface. Only when they begin diving does the spleen contract and release the
red blood cells into the circulation, which increases the hematocrit while
heart rate is reduced due to the dive response
(Hurford et al., 1996). A
hematocrit greater than 60% would further increase blood viscosity, increase
heart work, and could decrease rather than increase convective oxygen
transport. (Hedrick and Duffield, 1986). Consequently, the elevated Hct of
Weddell seals and other marine mammals may be at its physiological maximum for
optimizing blood oxygen storage and convective oxygen transport.
The concentration of Mb in the skeletal muscles of Weddell seals is about
10-times greater than in most terrestrial mammals
(Snyder, 1983). Oxygen bound
to Mb represents one-third of the total oxygen store in Weddell seals, so it
is a major factor in setting the ADL (Davis
and Kanatous, 1999; Kooyman
and Ponganis, 1998). However, it is not clear what physical or
physiological factors may have set the maximum concentration of muscle Mb. The
objective of this study was to model the effects of different muscle Mb
concentrations on the ADL of Weddell seals. Specifically, we wanted to know
how increasing or decreasing Mb concentration beyond normal levels would
affect the ADL. Although lowering the Mb concentration would obviously
decrease the ADL, would increasing the concentration automatically increase
it? To answer this question, we used a previously published model of
convective oxygen transport and tissue oxygen consumption
(Davis and Kanatous, 1999). We
ran the model at different myoglobin concentrations for various levels of
muscular exertion under postabsorptive and postprandial conditions to
determine their effect on ADL.
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O2) and the
rate of oxygen consumption
(
O2) in a
hypothetical Weddell seal during aerobic dives at different levels of muscle
oxygen consumption
(MO2) (see List
of symbols and abbreviations). A detailed description of the model and an
explanation of the assumptions and equations under postabsorptive conditions
has been published (Davis and Kanatous,
1999). This study differed from that of Davis and Kanatous in that
we ran the model with four different muscle Mb concentrations during aerobic
dives under both postabsorptive and postprandial conditions. The numerical
process iteratively determined arterial blood oxygen concentration
(CaO2) and venous blood oxygen concentration
(CVO2) for various tissues and
organs based on the circulatory diagram shown in
Fig. 1 and Eqn 1 (Fick's
principle):
 | (1) |
is blood flow rate (l
min–1). Cerebral, coronary and skeletal muscle regional
circulations were incorporated into the model individually, while splanchnic,
renal and cutaneous circulations were grouped together with all other organs
and tissues (e.g. bone and fat). The average temporal resolution (i.e. the
period between consecutive computations) was 0.22 min.
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This model considers only dives that are within the seal's ADL
(Kooyman et al., 1980;
Ponganis et al., 1993a). The term ADL was used in this model to describe the
maximum duration of an aerobic dive under specific conditions. The basal
contribution of anaerobic metabolism in harbor seals has been shown to
constitute approximately 2% of ATP production in a resting state and 1% during
active swimming (Davis et al.,
1991). For this model, this small basal contribution of anaerobic
metabolism is ignored, and tissues are considered aerobic as long as there is
no increased reliance on anaerobic metabolism resulting in an increase in
blood lactate over resting levels. While terms such as diving lactate
threshold (DLT) and calculated aerobic dive limit (cADL) are useful for
certain applications (Butler and Jones,
1997), they were not applicable to all conditions used to
terminate a dive in this model. DLT was not used because increased blood
lactate resulting from anaerobic metabolism was not necessary to terminate a
dive in this model. The term cADL is historically used to denote a calculation
of aerobic dive limit based on total useable oxygen stores divided by whole
body metabolism. While this model does calculate an ADL, it does so through
modeling of blood flow and metabolism in individual tissues, which can produce
vastly different results than whole body calculations in some metabolic
states. The rate of oxygen consumption in the tissues is maintained until
convective oxygen delivery falls below a critical level and endogenous oxygen
stores (skeletal muscle only) are depleted, resulting from a combination of
ischemic and hypoxic hypoxia. When any organ (e.g. splanchnic organs) or
tissue (e.g. skeletal muscle) no longer has sufficient oxygen to support
aerobic metabolism (i.e. the point at which anaerobic energy metabolism
commences), then the ADL has been reached and the dive is terminated.
Assumptions and equations
Organ and tissue masses were based on published values for a 450 kg adult
Weddell seal (Fujise et al.,
1985; Zapol et al.,
1979) as described by Davis and Kanatous in their table 1
(Davis and Kanatous, 1999). The
resting O2
values for Weddell seal organs and tissues were estimated from the metabolic
mass-adjusted O2
for the equivalent organs of a human or rat
(Diem and Lentner, 1970;
Field et al., 1939;
Kety, 1957). The basal, whole
body O2 (897 ml
O2 min–1 or 2.0 ml O2
min–1 kg–1) was calculated by combining
individual organ and tissue metabolic rates. The calculated basal metabolic
rate was similar to the minimum metabolic rates measured for adult Weddell
seals during rest or sleep (Castellini et
al., 1992b; Ponganis et al., 1993a;
Williams et al., 2004).
Resting heart rate (fH) (51.5 beats
min–1), cardiac output
(b) (42.7 l min–1)
and stroke volume (VS) (0.83 l) were based on measured
values for Weddell seals (Zapol et al.,
1979). During a simulated dive,
b was varied from 19–131% of
resting levels [(see Davis and Kanatous,
1999), table 2]. For brevity, we hereafter refer to these
percentages of resting, predive b as
percent b (e.g.
19%b). When
b was below resting levels, most of
the reduction resulted from a decrease in fH (i.e.
bradycardia). However, based on studies of seals during forced submergence and
voluntary dives (Blix and Folkow,
1983; Kjekshus et al.,
1982; Ponganis et al.,
1990; Sinnet et al., 1978;
Zapol et al., 1979),
VS was also reduced as fH declined.
The maximum reduction in VS in the model was 25% of the
resting value and was proportionate to the reduction in
fH. The reduction in cardiac output (i.e. the severity of
the dive response) was immediate and remained constant throughout a dive. An
`anticipatory' increase in b toward
the end of a dive was not included in the model. Except for the brain, where
circulation was always maintained at resting levels, we assumed that blood
flow to the rest of the body decreased proportionately with
b during a dive due to reduced
b and peripheral vasoconstriction
(Blix et al., 1976;
Elsner et al., 1964).
Peripheral vasoconstriction was assumed to occur in the large arteries (e.g.
the renal artery), making it independent of tissue level metabolic dilators
that affect arterioles (White et al.,
1973). Because vasoconstriction was assumed to occur high in the
vascular tree, blood flow was not adjusted independently to individual tissue
beds.
Body oxygen stores were confined to the blood and skeletal muscle in this
model, since no oxygen storage capability exists in the splanchnic organs
(Dodd et al., 1987) and the
heart represents less than 2% of the total muscle mass. We assumed that lung
oxygen was not available during a dive due to the complete functional
pulmonary shunt that occurs in Weddell seals at pressures greater than
3–5 atmospheres (2280–3800 mmHg; 1 mmHg=0.133 kPa; approximately
30–50 m deep) (Falke et al.,
1985; Reed et al.,
1994). Even if lung oxygen were available during a dive, it
represents only 5% of the total body oxygen store in Weddell seals
(Kooyman and Ponganis,
1998).
To calculate total oxygen stores in the blood, we assumed that the blood
volume for a 450 kg Weddell seal was 96 liters (Ponganis et al., 1993a) and
that 33% of this volume was arterial blood and 67% was venous blood (i.e.
venules, small and large veins, hepatic sinus and spleen)
(Hurford et al., 1996;
Rowell, 1986). The blood
hemoglobin (Hb) concentration (assuming complete splenic contraction) was 260
g l–1, and the oxygen binding capacity of Hb was 1.34 ml
O2 g–1 Hb
(Kooyman et al., 1980;
Ponganis et al., 1993a; Qvist et al.,
1986). This gave a capacitance coefficient of oxygen in blood
(ßBO2) of 348 ml O2 l–1
(260 g Hb l–1 blood x 1.34 ml O2
g–1 Hb). At the beginning of a dive, we assumed that the
arterial blood was 100% saturated with oxygen as a result of predive
hyperventilation (Kooyman et al.,
1980; Qvist et al.,
1986; Ponganis et al., 1993a). Mixed venous blood was calculated
from Eqn 2 to be 86% saturated at the beginning of a dive assuming an oxygen
content that was 5% by volume less (Ponganis et al., 1993a) than an initial
CaO2 of 348 ml O2
l–1 blood.
 | (2) |
O2 is
the oxygen saturation of mixed venous blood. Arterial and venous blood oxygen
stores were calculated as:
 | (3) |
 | (4) |
). We assumed an
oxygen binding capacity of 1.34 ml O2 g–1 Mb, and
complete saturation at the beginning of a dive
(Gayeski et al., 1987;
Schenkman et al., 1997).
Muscle oxygen stores were calculated as:
 | (5) |
).
As blood circulates through the four vascular beds
(Fig. 1), the organs and
tissues extract oxygen from the blood to meet their respective
O2 requirements.
CvO2 was calculated for each circulatory bed
according to Fick's Principle:
 | (6) |
 | (7) |
 | (8) |
 | (9) |
is blood flow rate,
is the rate of oxygen consumption,
the letters B, H, M indicate brain, heart and skeletal muscle respectively,
and SRC indicates splanchnic, renal and cutaneous organs and other peripheral
tissues. However, the extraction coefficient of oxygen from the blood
(EBO2), where
EBO2=(CaO2–CvO2)/CaO2,
could never exceed 0.8 (i.e. maximum EBO2 at
critical oxygen delivery) during a single pass of the blood through an organ
or tissue (Samsel and Schumacker,
1994; Torrance and Wittnich,
1994; Nelson et al.,
1988). The mixed venous blood oxygen concentration
(CO2) was
calculated for the four vascular beds as the difference between the
CaO2 and the total oxygen extracted per ml of
blood:
 | (10) |
The arterial blood oxygen saturation (SaO2)
and venous blood oxygen saturation (SvO2) were
calculated for the blood of each vascular bed as the quotient of their
respective oxygen concentrations (Eqn 6–9) and a
ßBO2 of 348 ml O2 l–1
blood. The arterial (PaO2) and venous
(PvO2) blood oxygen partial pressures were
calculated from their respective SaO2 and
SvO2 using two polynomial equations fitted to
the oxy-hemoglobin dissociation curve (P50=26.9 mmHg=0.133
kPa) for adult Weddell seals (Qvist et
al., 1981).
Evidence obtained during the forced submergence of harbor seals and Weddell
seals indicates that B is
generally maintained and
BO2 does not
decline (Blix and Folkow, 1983;
Kerem and Elsner, 1973;
Zapol et al., 1979). In this
model, we assumed that B
and BO2 remained
at resting levels during a dive and were independent of
b. We also assumed that the minimum
PaO2 and
PO2 for normal
cerebral metabolism and function were 22 mmHg
(SaO2=38%) and 18 mmHg
(SO2=27%),
respectively. This is comparable to the average
PaO2 (24.5±2.86 mmHg; mean ±
s.d., N=7) in Weddell seals 2 min before surfacing and to the end
tidal PO2 (24 mmHg) of the first exhalation
(assuming that this approximates arterial PO2)
after 17 min aerobic dives (Ponganis et al., 1993a;
Qvist et al., 1986). As a
result, the model terminated a dive if PaO2
decreased below 22 mmHg in the model. However, the
PaO2 of blood perfusing the brain was generally
not a consideration in determining ADL.
We assumed that H and
HO2 changed
proportionately with b
(Blix and Folkow, 1983;
Blix et al., 1976;
Kjekshus et al., 1982). When
convective oxygen transport to the myocardium changed during a dive, it was
proportional to the change in heart work, and the myocardium always received
sufficient blood oxygen to maintain aerobic metabolism.
M was also assumed to
change proportionately with b. Oxygen
transported to the muscles in the blood was always used (up to a maximum
EBO2 of 0.8) before oxygen bound to Mb because
of the lower affinity of Hb for oxygen
(Schenkman et al., 1997).
Oxygen not provided by the blood was obtained from oxymyoglobin stores to meet
MO2
requirements.
MO2 was assumed
to be independent of M as
long as the combination of convective oxygen transport and oxymyoglobin stores
was sufficient to meet metabolic demand. If at any time the combination of
these two were no longer sufficient to maintain aerobic muscle metabolism, the
dive was terminated.
Postabsorptive
O2
(3.73±0.88 ml O2 min–1
kg–1) and postprandial
O2
(5.24±0.88 ml O2 min–1
kg–1) during aerobic dives were based on indirect calorimetry
measurements by Williams et al. for foraging and non-foraging Weddell seals
(Williams et al., 2004). We
assumed that the average difference in
O2 (1.51 ml
O2 min–1 kg–1 or 680 ml
O2 min–1 for a 450 kg seal) between postabsorptive
and postprandial dives of 7–23 min in duration resulted from the
metabolic cost of prey warming, digestion, absorption and assimilation, which
we refer to as the Heat Increment of Feeding (HIF). This increase in
O2 was added to
the postabsorptive
SRCO2 to give a
postprandial
SRCO2 of 1234 ml
O2 min–1 (a 2.2-fold increase). We assumed that
the SRCO2 was
maintained as long as: (1) convective oxygen transport was sufficient to
support oxygen demand, (2) EBO2 did not exceed
0.8 and (3) PaO2 was greater than 22 mmHg
(Kvietys and Granger, 1982;
Schlichtig et al., 1992).
Computations
The model was run on a standard spreadsheet program (Quattro Pro for
Windows Version 6.0, Novell Applications Group, Orem, UT, USA) for eight
levels of b, sixteen levels of
MO2 up to a
maximum whole-body
O2 of 10.7 ml
O2 min–1 kg–1 and four different
Mb concentrations under postabsorptive conditions, which produced 512
combinations. These were then compared to postprandial conditions for the
normal and elevated Mb concentration adding an additional 256 combinations.
The general procedure was to select a Mb concentration, set the
b at a particular level (e.g. 37% of
the resting level) and then vary the
MO2 from 1 to 16
times the resting level. This process was then repeated for each Mb
concentration and b.
O2 for the four
vascular beds and the entire body were calculated for each combination. The
ADL was reached and the dive terminated when: (1) any non-muscle organ or
tissue did not receive sufficient oxygen through convective oxygen transport
to maintain aerobic metabolism, (2) convective oxygen transport and
oxymyoglobin stores were no longer sufficient to maintain aerobic muscle
metabolism, or (3) when the PaO2 fell below 22
mmHg.
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b in optimizing the ADL at different levels of muscle metabolismb in optimizing the ADL
at different levels of muscle metabolism has been described
(Davis and Kanatous, 1999).
Briefly, the ADL decreases in a non-linear fashion with increasing
MO2 for
different levels of b
(range=19–131% of resting levels)
(Davis and Kanatous, 1999;
Davis et al., 2004) (Figs
2,
3). For each level of
MO2, there is an
optimal b that gives a maximum ADL,
and this optimal b increases (i.e. the
dive response is less pronounced) as
MO2 increases
[(see Davis and Kanatous,
1999), fig. 4 and table 4]. Since the ADL is inversely
proportional to
MO2 (assuming a
constant level of blood and muscle oxygen depletion), the optimal
b decreases as the ADL increases [(see
Davis and Kanatous, 1999), fig.
5].
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The effect of Mb concentration on the postabsorptive ADL
In the postabsorptive state, the resting ADL (28 min) was independent of Mb
concentration (Fig. 2). At a
resting level of
MO2, the lowest
level of convective oxygen transport
(b=19%) was still sufficient to supply
97% of the oxygen needed by the skeletal muscle. As a result, very little Mb
oxygen (ranging from 21% to 1% of endogenous oxymyoglobin for concentrations
from 5 to 108 mg g–1, respectively) was used while resting
submerged, and it was not a factor that limited the ADL (Tables
1,
2,
3,
4). The only way to increase
the use of Mb oxygen at rest was to decrease convective oxygen transport even
further (i.e. b<19%). However, when
we ran the model at a b of 9%, the ADL
decreased because convective oxygen transport to the splanchnic organs and
kidneys was insufficient. Hence, at rest there was no optimal
b that provided sufficient oxygen
delivery for the kidneys and splanchnic organs while utilizing more Mb-bound
oxygen, regardless of the Mb concentration. As a result, there was no
difference in ADL for Mb concentrations of 54 and 108 mg g–1
until MO2
exceeded 3-times resting.
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At muscle Mb concentrations of 5 and 27 mg g–1, the
postabsorptive ADL decreased in a curvilinear fashion with increasing
MO2 and whole
body O2. At
normal and elevated Mb concentrations, the ADL decreased in a curvilinear
fashion with the exception of a common plateau at 24 min for
MO2 of 2- to
3-times resting and 2- to 5-times resting for these two Mb concentrations,
respectively (Fig. 2). At these
low levels of
MO2, the ADL was
limited by blood oxygen stores, and Mb oxygen was not a limiting factor
(Tables 3 and
4). These two curves diverge at
higher levels of exertion as muscle oxygen stores are consumed and contribute
significantly to setting the ADL. Only when
MO2 exceeded
3-times resting did an increase in the Mb concentration above 54 mg
g–1 increase the ADL.
Based on the findings of Williams et al.
(Williams et al., 2004), we
assumed an average postabsorptive diving
O2 of 3.8 ml
O2 min–1 kg–1, which was
equivalent to a
MO2 of 5-times
resting in our model. At this routine level of diving metabolism, a reduction
of Mb concentration from 54 mg g–1 to 27 mg
g–1 and 5 mg g–1 reduced the ADL from 18 min
to 12.7 min (29% reduction) and 11.0 min (39% reduction), respectively.
Doubling the normal Mb concentration increased the ADL 33% from 18 to 24 min
(Fig. 2).
For all four Mb concentrations, the optimal
b (i.e. the
b that gave the maximum ADL) increased
as muscular exertion increased (Fig.
3). The optimal b
increased more quickly with increasing levels of exertion (i.e. the slope of
the trend line was greater) for low muscle Mb concentrations compared to
normal and elevated Mb concentrations. As Mb increased, the optimum
b for each level of
MO2 decreased.
For example, at the average diving
MO2 of 5-times
resting, the optimal b at Mb
concentrations of 5, 27, 54 and 108 g Mb kg–1 were 75%, 56%,
37% and 19% of resting levels, respectively. As Mb increases,
b and muscle blood flow must decrease
(i.e. more pronounced dive response) for the muscle to fully use this Mb bound
oxygen.
At a MO2 of
5-times resting for normal and elevated Mb concentrations, convective oxygen
transport at the optimal b was
insufficient to support the aerobic metabolic needs of the muscle. As a
result, muscle Mb oxygen stores were used from the beginning and throughout
the dive (Fig. 4). In contrast,
the optimal b for reduced Mb
concentrations was greater (i.e. less pronounced dive response), resulting in
increased convective oxygen transport to the muscles and a delay in the use of
Mb oxygen until well into the dive (7 min and 1.33 min for Mb concentrations
of 5 and 27 mg g–1, respectively). With optimal matching of
b to
MO2, almost all
myoglobin oxygen was consumed at this routine level of exertion regardless of
myoglobin concentration.
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The effect of Mb concentration on the postprandial ADL
Under postprandial conditions, the ADL decreased at all levels of exertion
because of the increased oxygen consumption of the splanchnic organs
associated with prey warming, digestion and assimilation. At a routine
MO2 of 5-times
resting and normal Mb concentration, the postprandial ADL (12 min) was 33%
less than under postabsorptive conditions
(Fig. 5). The convective oxygen
transport needed by the splanchnic organs required a
b that was not optimal for the
complete use of muscle oxygen at a routine diving
MO2 of 5-times
resting. Not until
MO2 exceeded
7-times resting did this level of perfusion allow for complete utilization of
muscle oxygen stores, and Mb oxygen became limiting to the ADL
(Fig. 5 and
Table 5). As a result, doubling
the Mb concentration did not increase the ADL until the level of muscular
exertion exceeded 7-times resting. Diving at routine levels of muscular
exertion in a postprandial state resulted in convective oxygen transport and
not oxy-myoglobin limiting the ADL. Based on the results from our model,
digesting and assimilating food while diving decreased the ADL for two
reasons: (1) increased splanchnic consumption of blood oxygen and (2) the
increased convective oxygen transport needed by the splanchnic organs resulted
in a b that was not optimal for the
complete use of muscle oxygen. As a result, the model indicated that there was
no advantage in having a higher than normal myoglobin concentration during
postprandial dives at routine levels of
MO2.
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)
compared to Hb (p50=27 mmHg) (Qvist et
al., 1981), it is an endogenous oxygen store for muscle only. To
use this source of oxygen, the muscle must become hypoxic by reducing
convective oxygen transport. This not only decreases the muscle
PO2 so that the oxygen dissociates from
myoglobin, but also reserves more blood oxygen for other tissues. The first
publication using this model (Davis and
Kanatous, 1999) showed the importance of adjusting cardiac output
and convective oxygen transport to muscle according to the level of exertion,
so that the total oxygen available in the muscle and blood was used by the end
of a dive. As the level of muscular exertion increased, the dive response was
less pronounced and convective oxygen transport to skeletal muscle (and other
peripheral organs and tissues) increased. To maximize the ADL, both oxygen
stores had to be depleted simultaneously so that neither was singly
responsible for limiting aerobic dive duration.
In a postabsorptive resting state, the ADL was independent of Mb
concentration from 5–108 mg myoglobin g–1 muscle
(Fig. 2). The model showed that
the b needed to maintain resting
metabolism in the splanchnic organs (19%) resulted in an over-perfusion of the
skeletal muscle so that almost all (97%) of the oxygen used by the muscles at
rest was supplied by convective oxygen transport in the blood. Greater
utilization of Mb oxygen would require less convective oxygen transport to
skeletal muscle. However, further reduction in
b (9%) resulted in insufficient
convective oxygen transport to the splanchnic organs and reduced the ADL.
At a routine diving
MO2 of 5-times
resting, the postabsorptive ADL increased with higher Mb concentrations
(Fig. 2). In addition, Mb
concentration was negatively correlated with optimal
b for a dive
(Fig. 3). Higher Mb
concentrations (54 and 108 mg g–1) required a greater
reduction in cardiac output (more profound dive response). The resultant
reduction in convective oxygen transport to muscles decreased the muscle
PO2 (i.e. made the muscle hypoxic) so that
myoglobin oxygen was used throughout the dive
(Fig. 4).
At a MO2 of 1
to 7-times resting in a postprandial state, the
b required to maintain the elevated
aerobic metabolism in the splanchnic organs resulted in an over-perfusion of
the skeletal muscle, which caused the incomplete use of Mb oxygen stores
(Table 5). Inefficient use of
muscle oxygen stores as well as increased use of blood oxygen for digestion
and assimilation resulted in blood oxygen limiting the ADL in the postprandial
state until MO2
exceeded 7-times resting (Fig.
5 and Table 5). As
a result, the doubling of Mb concentration did not increase the ADL under
postprandial conditions until the level of
MO2 exceeded
7-times resting, which is 40% higher than the routine level of exertion.
Behavioral considerations
The results of this model showed that an increase in the Mb concentration
increased the ADL at a routine diving
MO2 under
postabsorptive conditions (Fig.
2). However, for the same
MO2 under
postprandial conditions, the convective oxygen transport needed for digestion
and assimilation required a b which
resulted in an over-perfusion of the muscle and incomplete use of muscle
oxygen stores at routine levels of exertion (i.e. <7 times resting
MO2)
(Fig. 5 and Tables
5,
6). Castellini et al. stressed
the importance of integrating physiology and behavior in considering the
biology of diving (Castellini et al.,
1992a). To determine what selective pressures might affect
myoglobin concentration, it is important to consider the way Weddell seals
routinely dive.
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Davis et al. classified Weddell seal dives into four types
(Davis et al., 2003). Type 1
were feeding dives with a mean duration of 15.0 min, and these accounted for
14% of all dives made and 29% of total time submerged. Given the assumptions
regarding HIF, the postprandial ADL (12 min) at a routine level of exertion
calculated by our model agrees well with average duration of feeding dives
reported (Davis et al., 2003).
Types 2 and 3 dives were relatively short in duration (mean=3.6 min and 7.9
min, respectively) and were rarely associated with feeding. Together these
dives accounted for 72% of dives being made. The average duration of these
dive types are well below our estimated postabsorptive ADL of 18 min and are
not limited by the physiological constraints of the oxygen stores, but by
behavior.
Type 4 dives were long in duration (average=24.7 min), appeared to be exploratory (non-feeding) dives, and accounted for 14% of all dives. This dive type exceeds our estimated postabsorptive ADL of 18 min and relies significantly on anaerobic metabolism. Our model indicates that an increased myoglobin concentration would prolong aerobic metabolism for this type of dive. However, these long duration dives rarely occur in free-diving Weddell seals (Kooyman, 1980).
Factors determining myoglobin concentration
It appears that dives of the type and duration in which an increase in
myoglobin concentration would increase the ADL are rare under normal diving
behavior. While an increase in myoglobin would prolong aerobic metabolism
during some long duration, postabsorptive dives, it does not appear to limit
the ADL in the majority of natural dives (i.e. Types 1, 2 and 3). Weddell
seals make the majority of their feeding dives in bouts of many dives with
short recovery periods on the surface
(Castellini et al., 1992a;
Kooyman et al., 1980). As a
result, many of these feeding dives probably occur in the postprandial
condition. Davis et al. observed (Davis et
al., 1983) that the plasma of Weddell seals became very lipemic
during deep foraging dives, indicating that the digestion and intestinal
absorption of fat was occurring during the 5–6 h foraging session.
Increased energy expenditure for digestion during diving is added to the
metabolic costs for locomotion and basal metabolism
(Williams et al., 2004). This
increased metabolism for digestion and assimilation is also thought to reduce
the ADL of southern elephant seals during foraging bouts
(McConnell et al., 1992).
Digestion not only increases oxygen consumption, but also influences the
optimal management of the muscle and blood oxygen stores. Our model indicated
that diving with the additional metabolic cost of HIF causes blood oxygen to
limit the ADL rather than myoglobin oxygen (i.e. myoglobin stores may not be
completely used). We hypothesize that myoglobin concentration is optimized for
the type and duration of dives routinely made by Weddell seals, and that a
further increase may not increase the ADL of most free-ranging dives. Whether
physiological constraints associated with the dive response and convective
oxygen transport have limited the concentration of myoglobin in muscles
remains uncertain, but our model does suggest a possible influence during the
evolution of Weddell seals and other long duration divers. In addition, the
model indicates that the calculated ADL is more complex than simply the
quotient of the available oxygen stores and estimated metabolic rate.
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionList of symbols and...References |
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O2
B
H
M
O2
SRC
O2
b
BO2
CRSO2
HO2
MO2
O2
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Acknowledgments |
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References |
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