Pharmacological blockade of the dive response: effects on heart rate and diving behaviour in the harbour seal (Phoca vitulina)
1 Department of Zoology, University of British Columbia, Vancouver, British
Columbia, Canada V6T 1Z4
2 Peter-Wall Institute for Advanced Studies, University of British Columbia,
Vancouver, British Columbia, Canada V6T 1Z2
* Present address: Institute of Marine Science, University of Alaska Fairbanks
and Alaska SeaLife Center, Seward, AK 99664, USA
Author for correspondence (e-mail:
jones{at}zoology.ubc.ca)
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Summary |
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Key words: diving, diving physiology, dive response, diving behaviour, heart rate, bradycardia, harbour seal, Phoca vitulina, methoctramine, metoprolol, prazosin, sympathetic system, parasympathetic system
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Introduction |
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While the cardiovascular responses to submergence are clearly necessary
during extended dives to conserve finite O2 stores for the
hypoxia-sensitive brain and heart, the role of these responses during routine
diving is not as obvious. For instance, Signore and Jones
(1995) found that in muskrats
(Ondatra zibethica), when bradycardia and vasoconstriction were
pharmacologically inhibited, maximum underwater survival time significantly
decreased, yet the muskrats still dived voluntarily for periods that are as
long as their routine dives. Furthermore, the cardiovascular responses to
short dives are highly variable in seals. Jones et al.
(1973
) found that harbour
seals did not always exhibit bradycardia during feeding dives that were <40
s. There is also evidence that bradycardia during short dives is not
necessarily related to swimming speed or muscular work in seals
(Kooyman and Campbell, 1972
;
Fedak, 1986
;
Williams et al., 1991
).
Because it is unclear whether the cardiovascular components of the diving response are necessary during routine diving and, given that harbor seals meet their ecological needs through repetitive short aerobic dives, we were interested in the functional role, if any, of the dive response during short dives. In the present study, we used pharmacological blockers to investigate the necessity of diving bradycardia, vasoconstriction and surface tachycardia in the performance of short dives and short surface intervals in harbour seals. We also investigated whether these adjustments were necessary to maintain a high percentage of time spent underwater during diving bouts.
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Materials and methods |
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Instrumentation
Each seal was anaesthetized using 5% isoflurane (Janssen, Toronto, ON,
Canada; induction by mask) and, after endotracheal intubation, the seal was
maintained on 1-2% isoflurane and 98-99% O2. Two electrocardiogram
(ECG) electrodes were placed on the dorsal surface of the seal, one above the
shoulder blade and one above the pelvis, on opposite sides of the animal. Hair
was shaved from the areas where incisions were to be made, and the exposed
skin was cleaned with 70% alcohol and an iodine-based solution (polyvinyl
pyrolidine-iodine complex 10%, Iodovet, Rougier Pharma, Mirabel, QC, Canada).
Thin-wire ECG electrodes (28 gauge, shielded, Cooner Wire Company, Chatsworth,
CA, USA) were tunnelled subcutaneously 9 cm from the insertion site (one
cranially and one caudally) with a 14 gauge hypodermic needle. Each ECG
electrode was connected to an externalized waterproof lead and an underwater
connector (USI square miniconn, Underwater Systems, Stanton, CA, USA) that was
glued to a neoprene base with 5-min epoxy (Devcon, Acklands, Vancouver, BC,
Canada). After electrode insertion, the amplified ECG was displayed on an
oscilloscope to verify that the electrode placement resulted in a clear
signal. The underwater connector/neoprene base was then glued to the seal's
hair using cyanoacrylate adhesive (ZapAGap, Richmond RC Supply Ltd, Delta, BC,
Canada). The electrode insertion sites were bathed with 1 ml bupivacaine
hydrochloride 25% (Abbott Laboratories Ltd, Montreal, QC, Canada) to provide
post-operative analgesia. A colored neoprene patch was glued (ZapAGap) to the
hair on each seal's head for identification on videotape. Two buckles were
glued to the seal's hair mid-way between the two electrodes using 10-min epoxy
(Evercoat Ten Set Epoxy; Fibreglass-Evercoat Co. Inc., Cincinnati, OH, USA)
for the attachment of an ECG-recording instrument. Seals were allowed at least
48 h to recover before diving experiments. All procedures were approved by the
Animal Care Committee at the University of British Columbia.
Pharmacological antagonists
Preliminary experiments with three seals established the appropriate doses
of the pharmacological blockers used in the diving experiments, as well as the
time frame in which the durgs were most effective. Specific pharmacological
agonists were used to induce the cardiovascular responses seen during diving
in order to assess the doses of the blockers and the effectiveness of
blockade. Before drug testing, a catheter [PE micro-renathane tubing, 0.050
units x 0.025 units o.d. x i.d. (Braintree Scientific Inc.,
Braintree, MA, USA) attached to a 21 gauge winged needle infusion set
(Venisystems Abbott Laboratories Inc., Abbott Park, IL, USA)] was inserted
into the extradural intravertebral vein under anaesthesia (see above
protocol). The catheter was kept open by filling it with heparinized PVP
[polyvinyl pyrolidine (Sigma-Aldrich Canada Ltd); 1 g PVP:12 ml saline,
heparin 20 U ml-1]. Each seal was restricted to a dry enclosure,
the PVP was withdrawn from the catheter, and the catheter was attached to a
saline-filled intravenous line (1.9 m; Interlink System, Baxter Corp.,
Toronto, ON, Canada). Heart rate was monitored after intravenous injection of
each agonist alone (into the catheter extension), and then the effects of the
agonists were monitored following administration of the appropriate
antagonist. The ß-adrenergic agonist isoproterenol hydrochloride (0.01
µg kg-1; Sigma-Aldrich Canada Ltd) was used to induce
tachycardia and therefore assess the efficacy of the
ß1-adrenergic antagonist metoprolol (Novartis Pharmaceuticals
Canada Inc., East Hanover, NJ, USA). The -adrenergic agonist
1-phenylephrine hydrochloride (0.06 µg kg-1; Sigma-Aldrich
Canada Ltd) was used to induce both vasoconstriction and bradycardia in order
to assess the efficacy of the
1-adrenergic antagonist
prazosin (Pfizer Inc., New York, NY, USA) and the muscarinic antagonist
methoctramine (Sigma-Aldrich Canada Ltd), respectively.
In one seal, several different doses of each blocker were tested for blockade of the agonist-induced response and for unwanted side effects. The specific doses to be used in diving experiments were ultimately chosen based on the maximum drug dose causing the desired blockade (as indicated by heartrate analysis) without any obvious side effects such as excitement or lethargy. These doses were then confirmed in two other seals. In all three seals, the selected doses were tested for blockade of the agonist-induced responses at different time intervals after administration of the antagonist (15 min to 2 h intervals for up to 6 h post dose). Based on these results, we estimated the time frame during which diving experiments would be conducted.
Diving experiments
Diving experiments with five harbour seals were conducted in a 4.5 m
x 11 m diameter x depth freshwater tank. Seals were allowed to
acclimate to the tank over a period of 1-2 months. Water temperature ranged
from 12°C to 16°C. All five seals received each of the following
treatments, once, in randomized order: (1) subcutaneous (S.C.) injection of
the cardio-selective muscarinic antagonist methoctramine (0.23 mg
kg-1); (2) oral administration (in a fish) of the
1-adrenergic antagonist prazosin (three doses, 0.24 mg
kg-1 each); (3) oral administration of the
ß1-adrenergic antagonist metoprolol (two doses, 4 mg
kg-1 each); (4) a combination of S.C. methoctramine and oral
prazosin; (5) a combination of S.C. methoctramine and oral metoprolol; (6)
S.C. injection of saline (control for all methoctramine injections); and (7)
oral administration of a fish without pills (control for prazosin and
metoprolol). Treatments were done on separate days with at least 24 h between
drugs (48 h following metoprolol). Injections were given just before diving
sessions while seals were at the surface platform of the dive tank. Oral pills
(prazosin, metoprolol, or control fish) were given on the evening before and
the morning of diving experiments.
Heart rate (fH) was recorded using a custom-designed
data logger that consisted of a high-memory ECG recorder based on a computer
board (model 8; Onset Computer Corp., Bourne, MA, USA) interfaced to a
compact-flash memory expansion board (model CF8; Peripheral Issues, Mashpee,
MA, USA) (for details, see Andrews,
1998; Southwood et al.,
1999
). The data logger was programmed to sample the amplified ECG
signal at 50 Hz and, with a memory of 15 Mb, recorded fH
for 84 h. Before diving sessions, the data logger was attached to the buckles
on the seal and connected to the ECG electrodes via underwater
connectors. During experiments, voluntary diving behaviour was recorded using
a video camera (Lorex, Strategic Vista Corp., Markham, ON, Canada) suspended
over the breathing hole (2.4 m2) in which the seals surfaced.
Statistics and analysis
Data were downloaded to a computer from the data logger, and inter-beat
intervals were calculated by detecting the R waves of the ventricular QRS
complexes of the ECG. Instantaneous heart rate was determined by converting
RR intervals to beats min-1, and mean fH
for dives and surface intervals was calculated by averaging these values. The
first and last 10 s of each dive and the last 3 s of each surface interval
were excluded from the calculation of means to reduce variability in
fH caused by the initial bradycardia that is below the
fH established during the rest of the dive, cardiac
acceleration before surfacing (anticipatory tachycardia), and cardiac
deceleration before submergence (anticipatory bradycardia). Therefore, only
dives of >20 s and surface intervals of >3 s were analyzed. For each
treatment, diving behaviour (dive and surface interval durations) was analyzed
from the videotapes for the hour during which the blockade was maximal. This
hour of analysis was initially estimated during preliminary drug testing and
ultimately determined by analysis of fH during diving
sessions. For methoctraminetreated groups, dive behaviour was analyzed
approximately 1-2 h after injections; for prazosin, 1.25-2.25 h after the
third oral dose; and for metoprolol, 4-5 h after the second oral dose.
Controls for each group were analyzed to match these time periods. Values for
fH and dive behaviour given in the text represent grand
means ± S.E.M. (N=5) for each treatment.
The means for each group were compared using one-way repeated measures analysis of variance (ANOVA). Multiple comparisons were performed using Tukey tests. Differences were considered significant when P<0.05. All statistics were calcualted with SigmaStat software (Jandel Scientific, San Rafael, CA, USA).
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Results |
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The effects of the pharmacological blockers on dive and post-dive surface
interval fH are presented in
Fig. 2, and diving
fH profiles are shown in
Fig. 3. In the control groups,
mean dive fH ranged from 47±3 beats
min-1 to 49±4 beats min-1, and mean surface
interval fH ranged from 133±3 beats
min-1 to 138±4 beats min-1
(Fig. 2). During a typical dive
bout in control seals, fH dropped immediately upon diving
to approximately 17% of the pre-dive surface rate within 5-10 s of the dive.
fH then increased to approximately 35% of the predive rate
within 30-40 s of the initiation of the dive and remained at this level until
approximately 10-20 s before surfacing, when it increased rapidly so that
pre-dive levels were reached upon or within 5 s of surfacing
(Fig. 3). In the -and
ß-adrenergic-blocked groups, the fH profiles followed
a similar pattern to those in the control group (an initial drop, a slight
increase to a steady level and then a pre-surfacing increase to surface
levels). In the three muscarinic-injected groups, fH
decreased to a lesser degree such that the extreme initial drop and steep
increase 10-20 s before surfacing were not pronounced
(Fig. 3).
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In the muscarinic-blocked group, mean dive fH was
significantly higher (P<0.001, N=5) than in the control
group (110±3 beats min-1 versus 49±4 beats
min-1), while mean surface fH was not
significantly different from the control group (137±3 beats
min-1 versus 138±4 beats min-1)
(Fig. 2). Dive
fH in -adrenergic-blocked animals was significantly
higher (P<0.001, N=5) than in control seals (64±3
beats min-1 versus 47±3 beats min-1),
but surface rates were not significantly different (121±5 beats
min-1 versus 133±3 beats min-1)
(Fig. 2). After
ß-adrenergic blockade, dive fH was not significantly
different from that of the control group (42±3 beats min-1
versus 48±3 beats min-1), but surface
fH was significantly lower (P<0.001,
N=5) (98±1 beats min-1 versus 137±3
beats min-1) (Fig.
2). In the muscarinic- plus
-adrenergic-blocked group, dive
fH was significantly higher (P<0.001,
N=5) than in control seals (109±3 beats min-1
versus 49±4 beats min-1), but surface rates were
not significantly different (136±3 beats min-1
versus 133±3 beats min-1)
(Fig. 2). Dive
fH after muscarinic- plus ß-adrenergic blockade was
significantly higher (P<0.001, N=5) than in the control
(88±1 beats min-1 versus 49±4 beats
min-1), and surface fH was also significantly
lower (P<0.001, N=5) (111±2 beats min-1
versus 138±4 beats min-1)
(Fig. 2). In each treatment
condition, the dive fH was significantly lower
(P<0.001, N=5) than the surface fH
(Fig. 2).
Fig. 4 shows the effect of
pharmacological blockade on mean dive and post-dive surface interval duration.
Mean dive duration in control seals ranged from 2.61±0.32 min to
2.83±0.49 min, and mean surface-interval duration ranged from
0.40±0.04 min to 0.43±0.04 min
(Fig. 4). None of the
treatments had any significant effect on mean dive duration (2.34±0.47
min for the muscarinic group; 2.40±0.27 min for the -adrenergic
group; 2.80±0.39 min for the ß-adrenergic group; 2.67±0.45
min for the muscarinic plus
-adrenergic group; 2.67±0.47 min for
the muscarinic plus ß-adrenergic group;
Fig. 4). In fact, seals made
voluntary dives for as long as 8.12 min without a surface tachycardia, 6.72
min when bradycardia was blocked, 4.72 min when vasoconstriction was blocked,
and 4.93 min when both bradycardia and vasoconstriction were blocked.
Furthermore, there was no significant change in mean surface interval duration
after blockade (0.40±0.04 min for the muscarinic group;
0.47±0.04 min for the
-adrenergic group; 0.44±0.02 min
for the ß-adrenergic group; 0.48±0.02 min for the muscarinic plus
-adrenergic group; 0.44±0.04 min for the muscarinic plus
ß-adrenergic group; Fig.
4).
|
There was no effect of blockade on the percentage of time spent submerged during diving sessions. In control seals, mean percentage dive time ranged from 86±1% to 87±1%, and in treated seals, percentage dive time ranged from 83±2% to 85±2%.
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Discussion |
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The effects of the blockers on fH were in agreement
with their pharmacological action on the autonomic nervous system.
Methoctramine is a polymethylene tetra-amine compound that is highly selective
for M2-subtype muscarinic receptors that are predominantly found in
the heart in many terrestrial mammals
(Hammer and Giachetti, 1982;
Giraldo et al., 1988
;
Melchiorre, 1988
;
Hendrix and Robinson, 1997
).
Therefore, methoctramine reduced diving bradycardia by inhibiting the action
of acetylcholine on cardiac M2 receptors in the seals. Prazosin is
a highly selective
1-adrenergic antagonist with an affinity
for
1 receptors that is approximately 1000-fold greater than
for
2 receptors (Davey,
1980
; Hoffman,
2001
). In humans and other terrestrial mammals, blockade of
1 receptors inhibits vasoconstriction induced by
catecholamines so that vasodilation occurs in arterioles. The fall in
peripheral vascular resistance leads to decreases in arterial blood pressure
and, as a result of the barostatic reflex, slight increases in
fH and cardiac output
(Davey, 1980
;
Saeed et al., 1982
;
Hoffman, 2001
). Prazosin
caused a slight but significant increase in diving fH,
probably as a result of
-adrenergic blockade causing peripheral
vasodilation. Although we could not monitor blood flow and arterial blood
pressure during dives, the increase in fH after
administration of prazosin, as well as the lack of a marked effect of the
-adrenergic agonist phenylephrine in prazosin-treated animals, suggests
that
-adrenergic blockade was indeed effective in our seals. Metoprolol
is a ß1-selective adrenergic antagonist that blocks the action
of noradrenaline on ß1 receptors that are predominantly found
in the myocardium in humans (Prichard and
Tomlinson, 1986
; Hoffman,
2001
). Therefore, metoprolol inhibited post-dive surface
tachycardia by blocking sympathetic inputs to ß-adrenergic receptors on
the heart.
The effects of cardiovascular pharmacological blockade reveal the dynamic influence on fH of the two branches of the autonomic nervous system during diving. Because mean surface fH was unchanged by muscarinic blockade but significantly lower after ß-adrenergic blockade, post-dive tachycardia is attributed to increased sympathetic stimulation of the heart, as well as vagal withdrawal at the surface. Mean dive fH after muscarinic blockade was significantly higher than the dive fH in control seals, whereas dive fH following ß-adrenergic blockade was not significantly different; therefore, the parasympathetic nervous system is the primary modulator of bradycardia during diving. However, the role of the sympathetic system during diving is not as straightforward. The fH during dives was significantly lower than during surface intervals in muscarinic-blocked seals, suggesting that an increased level of sympathetic stimulation at the surface is withdrawn during submergence. Sympathetic inputs to the heart cannot be withdrawn completely though, because diving fH after ß-adrenergic plus muscarinic blockade was significantly lower than after muscarinic blockade alone. However, ß-adrenergic blockade alone did not significantly lower diving fH.
One possible explanation for these discrepancies in diving
fH is that the two divisions of the autonomic nervous
system interact asymmetrically such that the parasympathetic system dominates
the sympathetic system when vagal outflow to the heart is maximal. In other
words, sympathetic tone persists during diving but is not expressed because
the vagus modulates fH by means of an accentuated
antagonism. Accentuated antagonism has also been observed in diving muskrats
(Signore and Jones, 1995) and
is the result of a cholinergically mediated insensitivity of cardiac cells to
adrenergic stimulation (Kimura et al.,
1985
; Signore and Jones,
1995
). Such a response during diving would explain why harbour
seals develop a bradycardia despite increases in circulating catecholamines
(Hance et al., 1982
;
Hochachka et al., 1995
). It
would also facilitate the rapid switching between dive and surface states,
because the effective response to changes in sympathetic activation occurs
more slowly than changes resulting from parasympathetic activity
(Furilla and Jones, 1987
;
Japundzic et al., 1990
).
A puzzling result is that the dive fH was significantly
lower than the surface fH in muscarinic- plus
ß-adrenergic-blocked seals. Simultaneous blockade of parasympathetic and
sympathetic outflow to the heart should reveal the aneural or intrinsic
fH. In our double-blocked seals, dive
fH was 88 beats min-1, whereas surface
fH was 111 beats min-1. This finding suggests
that either blockade was not complete or that there is a non-muscarinic,
non-ß1-adrenergic factor affecting fH
during diving in harbour seals. One possibility is that the surface
tachycardia may be caused by stimulation of cardiac ß2
receptors by circulating adrenaline. We chose a ß1-selective
antagonist in order to avoid effects on ß2-adrenergic
receptors in vascular and bronchial smooth muscle. Also, sympathetic
stimulation of the heart in humans is known to occur primarily via
ß1 receptors, although it is uncertain as to what extent
activation of cardiac ß2 receptors contributes to increases in
fH (Hoffman,
2001). It is likely that ß2 receptors play a
larger role in cardiac responses in seals.
On several occasions, seals displayed a decrease in fH
1-3 s before submergence. Anticipatory bradycardia has previously been
observed in harbour seals (Jones et al.,
1973). Furthermore, pre-surfacing tachycardia was seen in all
control dives and was unaffected by
- or ß-adrenergic blockade but
was reduced in methoctramine-injected animals, which suggests that it is
caused by the withdrawal of vagal inputs. Cardiac acceleration before
surfacing has been reported in both seals
(Jones et al., 1973
;
Thompson and Fedak, 1993
;
Andrews et al., 1997
) and
muskrats (Signore and Jones,
1995
). By restoring circulation to tissues that may have been
hypoperfused during the dive, pre-surfacing tachycardia should further reduce
the O2 content of the blood, thereby maximizing O2
uptake at the beginning of the surface interval
(Thompson and Fedak,
1993
).
Previous studies reveal that harbour seals in the wild typically dive for
2-6 min, with surface intervals lasting <1 min, so they spend 75-85% of
their time at sea submerged (Fedak et al.,
1988; Eguchi and Harvey,
1995
; Bowen et al.,
1999
). Our data agree with literature values. In control seals,
dive duration ranged from 23s to 5.4 min, and the mean duration was 2.7 min;
surface intervals ranged from 4s to 1.4 min, and mean surface-interval
duration was 25s. During control diving sessions, seals spent 86% of their
time submerged.
Pharmacological blockade of diving bradycardia, vasoconstriction and
post-dive tachycardia did not significantly affect routine dive or
surface-interval duration. Evidently, our seals had enough onboard
O2 to maintain routine dives without the O2-conserving
dive response and also to prevent an O2 debt large enough to
require extra time at the surface. For Weddell seals (Leptonycotes
weddellii), dives that involve an increasing reliance on anaerobic
metabolism usually necessitate extended surface intervals to replenish
glycolytic fuel reserves, process anaerobic byproducts, and restore blood and
tissue pH (Kooyman et al.,
1980). Although we did not measure post-dive blood lactate levels,
the seals did not surface or haul out on the deck for extended recovery
periods, so it is likely that they avoided significant anaerobic energy
contributions to diving metabolism. Furthermore, assuming that ß-blocked
seals did not fully reload their O2 stores at the surface, their
O2 reservoir was still large enough to enable continuous diving
(and some dives as long as 8.1 min). Seals also maintained a high percentage
dive time (approximately 84%) in all treatments; thus, the cardiovascular dive
response was not necessary to maintain an `efficient' dive strategy during
short diving sessions.
The short dives made by our seals in the control and treatment groups were
all within estimates of their aerobic dive limit (ADL). This limit is defined
as the maximum amount of time a diver can remain submerged relying only on
aerobic biochemical pathways (Kooyman et
al., 1983). The ADL can be empirically determined by measuring
post-dive blood lactate, the main metabolite of anaerobiosis, or an estimate
of the ADL (cADL) can be calculated using the quotient of estimated values for
O2 stores and diving metabolic rate (DMR). Specifically, if total
body O2 stores in the harbour seal equal 57 ml kg-1
(assuming 50% desaturation of arterial blood and 85% desaturation of venous
blood; Davis et al., 1991
), and
if the DMR is equal to the resting metabolic rate (RMR) of 7.3 ml
O2 min-1 kg-1
(Davis et al., 1991
), then the
cADL should be 7.8 min. In fact, RMR is essentially the metabolic rate when no
O2-conserving mechanisms are being utilized; therefore, harbour
seals are theoretically capable of diving for up to 7.8 min without the dive
response (if they use all of their available O2 stores). It follows
that any O2-conserving mechanism could potentially increase this
aerobic limit, or, alternatively, any physiological response resulting in
higher O2 demands such as exercise or stress could potentially
decrease it. Although we did not measure DMR in this study, the activity level
of the seals during diving experiments was probably quite low compared with
that of seals foraging in nature. On the other hand, Davis et al.
(1985
) showed that harbour
seals swimming in a flume at 1.4m s-1 increased their O2
consumption two times above the resting rate. Even if the DMR is equal to
twice the RMR, the cADL should be 3.9 min. Because mean dive durations in
control and treated seals ranged from 2.3 min to 2.8 min, all dives were
probably aerobic in nature.
In a similar study, Signore and Jones
(1995) found that, after
pharmacological blockade of the dive response, muskrats still dived
voluntarily for periods as long as their cADL, but maximum underwater survival
time significantly decreased. Although we did not measure maximum underwater
survival times in our seals, we expect that blockade of the dive response
should limit dive duration and also extend recovery time at the surface for
dives beyond the cADL. Again, if seals are capable of diving for up to 7.8 min
without any O2-conserving mechanisms (depending on the DMR), then
it follows that any dives beyond that limit would either require some degree
of a cardiovascular dive response and some degree of metabolic suppression or,
alternatively, an increasing reliance upon anaerobic metabolism to meet energy
demands.
If estimates of the ADL are in fact correct, then the seals in this study,
and perhaps seals in the wild, often surface before they reach their aerobic
limits. Why not remain submerged until O2 stores are nearly
exhausted? Optimality models have been used to tackle this question, and
factors that limit time at the surface and thus the extent of preparation for
a subsequent dive may limit dive duration. Such factors might include
increased predation risk while at the surface or a reoxygenation rate that
declines with surface interval time so that O2 is gained with
diminishing returns (Kramer,
1988; Houston and Carbone,
1992
). Based on breath-by-breath measurements of end-tidal
O2 and CO2 concentrations during surface intervals in
harbour porpoises (Phocoena phocoena) and grey seals (Halichoerus
grypus), Boutilier et al.
(2001
) recently proposed that
surface-interval duration is governed by the readjustment of CO2
stores rather than O2 stores. Perhaps the accumulation of
CO2 and the resulting increase in tissue and blood pH could dictate
the end to an aerobic dive. Although seals can tolerate much higher arterial
CO2 tensions compared with terrestrial mammals
(Kerem and Elsner, 1973
), a
study of harp (Pagophilus groenlandicus) and hooded seals
(Cystophora cristata) indeed showed that dive duration decreased
significantly with increasing alveolar CO2 tension
(Påsche, 1976
).
Although the harbour seals in this study could perform a series of short
aerobic dives without the cardiovascular dive response, control seals
consistently displayed a cardiac response during routine diving, suggesting
that bradycardia has some utility. A relatively moderate degree of bradycardia
and peripheral vasoconstriction is probably utilized during such short dives
to limit the depletion of blood O2 by peripheral organs and
particularly by the muscles, thereby reserving O2 stores for the
brain and heart in case of emergencies (i.e. unplanned extension of
submergence). While some supplementation of the muscle O2 store
could delay the onset of anaerobic metabolism
(Davis and Kanatous, 1999;
Jobsis et al., 2001
),
unrestricted blood flow to the muscles would limit aerobic dive capacity.
Because of the greater affinity of myoglobin for O2 compared with
haemoglobin, blood-borne O2 would quickly diffuse into the active
muscles and render the local myoglobin-bound O2 store unavailable
for use. Davis and Kanatous
(1999
) developed a numerical
model that describes the potential importance of the dive response in
optimizing the use of blood and muscle O2 stores during dives
involving different levels of muscular exertion. They found that blood and
muscle O2 stores should be consumed simultaneously but that cardiac
output and muscle perfusion must be reduced below resting levels in order to
maximize the ADL over a range of diving metabolic rates (2-9 ml O2
min-1 kg-1). Furthermore, Jobsis et al.
(2001
) found that during
trained submersions of harbours seals, increased muscle blood flow was
accompanied by a reduction in myoglobin desaturation, suggesting a higher rate
of O2 extraction from the blood even though muscle perfusion during
submersion was significantly reduced from resting values.
Although post-dive tachycardia was also not necessary to sustain a series
of short aerobic dives punctuated by short surface intervals, control seals
consistently displayed high heart rates at the surface. In between short
dives, surface tachycardia facilitates the restoration of blood gases and
O2 stores to pre-dive levels
(Thompson and Fedak, 1993;
Andrews et al., 1997
). While
seals are able to dive continuously without this degree of tachycardia, diving
with a larger reservoir of O2 would allow for greater flexibility
in behaviour in that a `safety margin' would be available if the dive must be
extended.
In conclusion, our data indicate that harbour seals are able to maintain routine dive and post-dive surface-interval durations as well as a high percentage of time underwater when the O2-conserving dive response is pharmacologically inhibited. Nevertheless, our seals utilized the response during all control dives, regardless of dive duration. While they may not be necessary, cardiovascular adjustments are probably utilized during short dives in order to maximize aerobic dive capacity and to conserve O2 for emergencies. This study raises some fundamental questions as to why seals surface before they reach their ADL and also what the functional role of the dive response is during short routine dives.
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Acknowledgments |
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References |
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