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First published online September 14, 2007
Journal of Experimental Biology 210, 3344-3355 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.008730
To what extent might N2 limit dive performance in king penguins?
1 North Pacific Universities Marine Mammal Research Consortium, UBC Marine
Mammal Research Unit, ROOM 247, AERL, 2202 Main Mall, Vancouver, BC, V6T 1Z4,
Canada
2 Department of Zoology, The University of British Columbia, 6270 University
Blvd., Vancouver, BC, V6T 1Z4, Canada
3 Centre d'Ecologie et Physiologie Energétiques, C.N.R.S., 23 rue
Becquerel, 67087, Strasbourg, Cedex 02, France
* Author for correspondence (e-mail: andreas_fahlman{at}yahoo.com)
Accepted 17 July 2007
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Key words: breath-hold diving, decompression sickness, mathematical modeling, aerobic dive limit
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). In fact, maximum calculated ADL (cADL, O2
stores/rate of oxygen consumption
O2) is
5.4–7.0 min if
O2 during diving
is at resting levels (Fahlman et al.,
2005; Froget et al.,
2004) and O2 storage capacity between 45 ml
O2 kg–1
(Ponganis et al., 1999) and 58
ml O2 kg–1
(Kooyman and Ponganis, 1998).
This estimate suggests that >95% of all dives are performed aerobically
(Froget et al., 2004). In the
king penguin, a surface interval exceeding 15 min has been considered to mark
the end of a dive bout (A.S., J.-P. Gendner, C. A. Bost and Y.H., manuscript
submitted for publication). Extended surface intervals, or interbout periods,
occur more frequently during the night but there are also regular terminations
of dive bouts during daylight. Therefore, an important question to pose is why
do king penguins stop foraging, sometimes for hours, during a period when food
may be readily available? If king penguins seldom exceed their ADL, are there
other plausible reasons for dive bout termination besides elevated lactate
levels? Could it simply be that the birds are satiated, have lost track of the
prey patch, have a gut full of cold prey causing a thermal burden that cannot
sustain diving or that they are exhausted? There are probably many reasons
causing dive bout termination but what are some of the physiological
constraints that may limit extended bouts of repeated dives?
King penguins decrease their body temperatures during diving bouts,
returning to normothermic temperatures during the interbout period
(Fahlman et al., 2005;
Handrich et al., 1997) (A.S.,
J.-P. Gendner, C. A. Bost and Y.H., manuscript submitted for publication).
These re-warming events involve perfusing peripheral tissues with warm blood
from the core of the body so long intervals at the surface may be necessary
for this thermal process. This would also enable the birds to lay down
subcutaneous fat accumulated from prey ingestion
(Fahlman et al., 2005).
Another possibility is that these surface intervals serve to remove
accumulated N2, which might otherwise limit dive performance.
Boycott et al. (Boycott et al.,
1908), using empirical data from studies on goats weighing around
20 kg, suggested that decompression sickness (DCS) risk is negligible unless
the difference between the ambient pressure (Pamb) and
tissue tension exceeds a critical threshold. When extended to human divers,
the observations suggested that safe decompressions can be made as long as the
ratio between tissue tension and Pamb, the
supersaturation, never exceeds 2. In other words, a human diver fully
equilibrated with N2 at 2 atmospheres absolute (ATA; 1 ATA=101 kPa;
2 ATA=10 m depth) can safely return to 1 ATA
(Boycott et al., 1908). Air
contains 
79% N2, so safe N2 levels would be below
1.6 ATA when decompression is made directly to the water surface. Above 1.6
ATA, DCS risk in humans is expected to increase rapidly with increasing tissue
and blood N2 tension (PN2). In pigs
weighing between 17 and 24 kg, none of the animals showed DCS symptoms upon
decompression to 1 ATA (0.79 ATA N2) after being fully equilibrated
in an atmosphere containing 2.4 ATA N2 (3 ATA total pressure),
while 50% showed symptoms at 3.1 ATA N2 (4 ATA total pressure)
(Dromsky et al., 2000). As
there is a direct relationship between DCS susceptibility and body mass in
terrestrial animals it would be expected that a bird of 12 kg would able to
withstand a slightly higher pressure reduction before DCS symptoms. However,
mixed venous PN2 values above 3 ATA should
evince a considerable proportion of symptoms in a 12 kg bird unless it has
adaptations that reduce supersaturation and bubble formation or can otherwise
tolerate an elevated bubble load.
The aim of this paper is to estimate blood and tissue PN2 in king penguins during extended foraging trips to determine if, after repeated foraging dives, PN2 can reach levels that could cause DCS. If so, we wish to determine possible behavioural or physiological mechanisms that could be used to moderate tissue PN2 and thereby decrease the risk of DCS.
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;
Olszowka and Rahn, 1987). A
brief outline of the assumptions and physiological structure of the model are
given here and a detailed description can be found elsewhere
(Fahlman et al., 2006). Inert
gas uptake and removal are regulated by the following equation:
 | (1) |
tiss) that determines the time it takes to reach a new
equilibrium after a change in the external pressure.
Pblood is assumed to follow lung
PN2 as long as there is no pulmonary shunt.
Thus, N2 added to blood and tissues during a dive comes from the
lungs. tiss can be used to compute time to 50% completion
(tiss1/2) of inert gas uptake or removal for a specific tissue
since tiss1/2=ln2xtiss
(Fahlman et al., 2006). Also,
1/2 describes the time to 50% completion of inert gas uptake
or removal. When Ptiss reaches Pblood,
a new steady state is achieved and the tissue is considered saturated.
tiss is made up of several terms regulating uptake and
removal:
 | (2) |
tiss is rate of blood
flow through the tissue, Vtiss is tissue volume and
Stiss and Sblood are the solubilities of inert gas of
the tissue and blood (Fahlman et al.,
2006; Fahlman et al.,
2001; Kety, 1951).
Consequently, inert gas uptake and removal from a tissue are governed by the
volume of the tissue, the solubility of inert gas and the local rate of blood
flow. The time it takes for the whole animal to reach a new steady state, or
saturation, after an increase in external pressure is determined by cardiac
output (tot), the
distribution of blood flow and the proportion of tissues with different inert
gas solubilities. An animal with a respiratory system that does not collapse
during diving only has two ways of altering inert gas uptake and removal:
changing tot, or changing
its distribution. Consequently, a realistic model to estimate blood and tissue
PN2 must have accurate values for blood flow
and blood flow distribution.
Measuring PN2 in a diving animal is
extremely complex and has only been done successfully in a few studies. In
king penguins, heart rate and mixed venous PN2
were measured during forced dives to depth between 34 and 102 m
(Ponganis et al., 1999).
Despite great differences in the magnitude of cardiovascular change between
forced and voluntary dives (Kooyman,
1989) the data reported by Ponganis et al.
(Ponganis et al., 1999) make
it possible to validate assumptions used in the model. In addition, the
physiological description of inert gas flux enables us to identify variables
which have a large impact on PN2 levels and
that deserve further research.
For the model, the body of the penguin was partitioned into five different
compartments: blood (arterial and venous) and four tissues (central
circulation, brain, fat and muscle). The central circulation compartment
included heart, kidney and liver while the fat compartment included
subcutaneous and abdominal fat, skin, bone, alimentary tract and connective
tissue (Fahlman et al., 2006).
This separation divides the body into tissues with a fast (central
circulation), intermediate (brain and muscle) or slow (fat) rate of inert gas
uptake or removal and makes it possible to look at temporal differences in
their contribution to mixed venous PN2
(Fahlman et al., 2006).
The proportion of muscle mass (35.0%) was taken from non-fasted king
penguins (Cherel et al., 1994a;
Cherel et al., 1994b). Central
circulation (heart, liver and kidney) was assumed to be 5.4% of total body
mass. Mass proportions for heart (1.3–1.6%) and liver (3.6 %) were taken
from non-fasted penguins (Cherel et al.,
1994a; Cherel et al.,
1994b) and the proportional mass of the kidney (0.4%) was assumed
to be equal to the Weddell seal (Davis and
Kanatous, 1999). The size of the brain compartment was taken as 26
g (from Ponganis et al.,
1999). The mass proportion of the fat compartment was 50.7%. Blood
volume (83 ml kg–1) and volume of the respiratory system
(lung + trachea + air sacs, 69 ml kg–1) were assumed to be
similar to those previously reported for this species
(Ponganis et al., 1999). We
assumed that the average resting heart rate for king penguins on land (87
beats min–1) (Froget et
al., 2004) represented a
tot of 2.4 ml
s–1 kg–1, which is similar to that of
resting emperor penguins on sea ice
(Kooyman et al., 1992). In
king penguins, average heart rates while diving and at the water surface
between dives were 101 beats min–1 and 186 beats
min–1, respectively
(Froget et al., 2004). Diving
and post-dive tot were
scaled directly according to changes in heart rate from resting levels on land
for king penguins (Table 1).
Therefore, diving tot was
16% higher and post-diving was 114% higher than the resting value
(Table 1). Thus,
tot while diving was
assumed to be 50% of the surface value.
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Stephenson et al., 1994) and
voluntarily (Bevan and Butler,
1992) diving ducks and in force dived Weddell seals
(Zapol et al., 1979). In the
Pekin duck and Weddell seal, blood flow to the brain was approximately 1% of
tot at rest. With an
approximate fivefold decrease in heart rate and
tot during diving, brain
blood flow increased to 10% of
tot during forced dives in
the duck (Jones et al., 1979).
We therefore assumed that blood flow to the brain at the surface was 1% of
tot and 10% during forced
dives (Table 1). In foraging
birds, we assumed that the blood flow rate to the brain increased by a similar
amount as during forced dives. Due to the smaller cardiovascular changes in
freely diving birds, the proportion of
tot was therefore initially
set to 4% (Table 1). Muscle
blood flow at the surface was assumed to be 0.35 ml min–1 g
tissue–1 in both forced trials and during a foraging trip,
which is similar to those measured in resting ducks
(Table 1)
(Grubb, 1982;
Jones et al., 1979). During
forced diving, little or no muscle blood flow was detected in the Pekin duck
(Jones et al., 1979), Macaroni
(Eudyptes chrysolophus) or Gentoo penguin [Pygoscelis papua
(Scholander, 1940)]. It was
therefore assumed that blood flow to the muscle during forced dives decreased
tenfold. As a result, 26% of
tot was directed to the
muscle during forced diving. This is similar to the assumptions used for the
Weddell seal (Davis and Kanatous,
1999). Deep diving penguins, on the other hand, swim actively
during portions of the dive (Sato et al.,
2002). Therefore, blood flow to muscle cannot be reduced to the
same extent as those measured in forced diving birds. However, the reduced
work by alternating periods of active swimming with periods of gliding
(Sato et al., 2002) reduces
the rate of O2 utilization and myoglobin desaturation and thereby
prolongs aerobic metabolism of the muscle. For this reason, the proportion of
tot directed to the muscle
was reduced to 13% (Table 1).
For central circulation, blood flow at the surface during forced trials was
assumed to be similar in proportion to organ mass specific metabolic rate of
heart, liver and kidney (43% of total metabolic rate) in the Weddell seal
at rest (Davis and Kanatous,
1999). Heart rate at the surface was 33% higher in foraging as
compared with force dived birds. As
tot was directly scaled to
heart rate, this led to a 33% increase in
tot for foraging birds at
the surface as compared with force dived birds, and we assumed that most of
this was directed to the central circulation. Thus, the proportion of
tot directed to central
circulation while birds were at the surface during the foraging trip was 56%
(Table 1). Blood flow to kidney
and liver was significantly reduced while flow to the heart was maintained
during forced dives in the Pekin duck
(Jones et al., 1979). The
proportion of tot directed
to central circulation during forced dives increased slightly with an overall
72% reduction in the local blood flow rate
(Table 1). In foraging birds, a
28% reduction in the local blood flow rate to central circulation was the
result of a 50% decrease in
tot and a 45% increase in
the proportion of tot
directed to this compartment (Table
1). Blood flow to the fat compartment was assumed to be 4% of
tot at the surface and was
unchanged in one case during forced dives (see below) or allowed to decrease
to 2% during diving in both forced trials and while foraging
(Table 1).
Validation of mathematical model using data from forced dives in penguins
Measured venous PN2 data in king penguins
reported by Ponganis et al. (Ponganis et
al., 1999) for forced dives in a water filled hyperbaric chamber
were used to validate the model. Estimated venous
PN2 from the model was compared with measured
data for dives to three different pressures (11.2 ATA, 7.8 ATA and 4.4 ATA,
equal to depths of 102 m, 68 m and 34 m, respectively), assuming a symmetric
compression and decompression rate of 1 m s–1
(Ponganis et al., 1999). Dive
duration, including descent, bottom and ascent duration, was 270 s to a depth
of 102 m, 200 s to a depth of 68 m and 134 s to a depth of 34 m. The reported
mean diving and post-surface heart rates from forced dives were 30 beats
min–1 and 141 beats min–1, respectively
(Ponganis et al., 1999).
Changes in heart rate were assumed to be directly proportional to adjustments
in tot from the resting
heart rate on land [87 beats min–1
(Froget et al., 2004)].
tot during forced diving
and during the post-dive surface period were, respectively, modelled as 33%
and 162% of the resting value of 2.4 ml s–1
kg–1. Consequently,
tot during forced diving
was 0.8 ml s–1 kg–1 and the post-diving
surface value 3.9 ml s–1 kg–1. We assumed
body mass (Mb) to be 12 kg, which was within the range of
values reported by Ponganis et al.
(Ponganis et al., 1999).
Estimated data from foraging penguins
We used time–depth recordings published elsewhere (A.S., J.-P.
Gendner, C. A. Bost and Y.H., manuscript submitted for publication) from four
king penguins during a complete foraging trip
(Table 2). The time–depth
recorder measured dive depth every 2 s and allowed detection of pressure
changes as small as 0.02 ATA (0.2 m). To correct for baseline noise, only
dives deeper than 0.6 m for at least 6 s were considered to be dives. A dive
bout was defined as a minimum of three repeated deep dives (
50 m)
followed by a surface interval of less than 15 min.
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Sensitivity analysis for foraging birds
The model variables of cardiac output, regional blood flow tissue
distribution and parabronchial shunt were varied and the model run with each
new set of variables for each bird and for each foraging trip
(Table 3). Tissue and mixed
venous PN2 as the bird surfaced after deep and
shallow dives and from the last dive of a dive bout was compared between
models with different cardiovascular variables
(Table 4). This allowed an
assessment of the initial conditions of the model and enabled determination of
the sensitivity of estimated blood and tissue
PN2 values to changes in physiological
variables (Table 4).
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Model simulation details
Mb was assumed to be 12 kg during the entire foraging
trip, which was the average Mb of the four birds before
and after the foraging trip (Table
2). Forced diving birds show a more pronounced diving bradycardia
and presumably greater changes in
tot than freely diving
birds. As tot was scaled to
heart rate, we adjusted tot
for a free-ranging bird.
tot while diving was
assumed to be 50% of its value at the surface (2.6 vs 5.2 ml
s–1 kg–1,
Table 1).
We looked at the N2 flux during an interbout period to evaluate if the short (<60 s) and shallow (<30 m) dives that commonly occur between diving bouts can help to remove N2 while concurrently protecting against DCS. We ran the model twice, once with the complete data set and the other with short shallow interbout dives removed.
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). The
resulting N2 uptake or removal tiss1/2 for central
circulation, muscle, brain and fat were 0.35, 1.88, 3.46 and 204 min while at
the surface and 1.26, 18.8, 1.73 and 1022 min while diving (Model 0,
Table 3). In
Fig. 1, each observed mixed
venous PN2 value at depth was obtained in a
separate trial. The solid black line represents estimated mixed venous
PN2 when assuming a regional blood flow
distribution during diving as in Model 0 in
Table 3. The dotted black line
represents estimated mixed venous PN2 when the
regional blood flow to central circulation, muscle and fat were changed to
36%, 52%, and 2%, respectively, of
tot. Each experiment varied
in compression and decompression sequences and the average profile for each
dive depth is given in the figure. In all trials, maximum venous
PN2 occurred after the return to the surface
(Fig. 1). The immediate drop in
mixed venous PN2 occurring as the bird returned
to the surface, is caused by the sudden change in blood flow distribution to
the various tissues upon surfacing. An immediate change in tissue-specific
blood flow affects the amount of N2 removed from each tissue and
pooling into the mixed venous blood, thereby initiating the decline. Blood
perfusion changes upon reaching the surface are immediate in some species
(Butler and Jones, 1982), and
this characteristic could therefore be a physiological reality. For Model 0
(Table 3), maximum estimated
venous PN2 was 4.2 ATA during a compression to
11.2 ATA, 3.0 ATA for a compression to 7.8 ATA and 1.7 ATA for a compression
to 4.4 ATA.
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Sensitivity analysis
Cardiovascular variables were altered sequentially and the model simulation
repeated for each of the four birds (Table
3, Table 4). For
models A–G, the distribution of
tot was 56% to central
circulation, 39% to muscle, 1% to brain and 4% to the fat compartment while
the bird was at the surface. Model A was the same as that used for foraging
birds in Table 1 and was used
as our initial model, to which we compared all other models. The effect of
diving bradycardia was explored in model B. The effect of a 100% parabronchial
shunt, i.e. no gas exchange, established at 100 m of depth, was explored in
model C. Models D–F and H explored the effect of regional changes in
blood flow distribution. In model G we determined how the pre-surface
tachycardia that is reported to occur in king penguins would affect tissue and
blood PN2
(Table 3). The results from
models A–G were used to select blood flow distributions for a final
model used in the remainder of the analysis (Model I,
Table 3).
Without a diving bradycardia, PN2 decreased
in tissues where tiss1/2<1.3 min (central circulation and
brain) and also by as much as 15% for mixed venous
PN2 during deep dives
(Table 3,
Table 4, models A vs
B). In other words, increasing
tot reduced
PN2 at the end of the dive for fast tissues
while it increased PN2 in slow tissues.
Termination of gas exchange at 100 m reduced N2 levels in all
compartments. Brain decreased by as much as 17% while mixed venous
PN2 decreased by 8%
(Table 4, models A vs
C). Central circulation PN2 increased by 4% at
the end of dive bouts and by 8% at the end of deep dives when blood flow
decreased by 31% (models A vs D). A further 39% decrease in blood
flow increased PN2 an additional 3% (1.61 ATA,
model D vs model E). Brain PN2, on the
other hand, decreased by 1–26% with a 75% decrease in blood flow while
fat PN2 increased by 20–33% with a 100%
increase in blood flow (models A vs D). With a 200% increase in blood
flow, muscle PN2 increased by 15–54%
(models A vs D). There were no apparent trends in the data and under
certain conditions an increase or reduction in blood flow had similar effects
on tissue and blood PN2 levels as the bird
surfaced. To explore this further, end bout or end dive
PN2 was estimated by sequentially varying
tiss1/2 for each tissue either while diving
(Fig. 2) or while at the
surface (Fig. 3). The results
suggested that very high or very low blood flows during diving reduced
PN2. A reduction in blood flow at the surface,
on the other hand, reduced N2 removal and increased
PN2 at the end of dive bouts and dives
(Fig. 3). The data in
Fig. 2 was used to adjust blood
flow distribution to minimize tissue PN2 (model
I, Table 3,
Table 4). In particular, blood
flow to brain was reduced to 25% of its surface value, which reduced
PN2 by 8–43%. Similarly, a reduction in
fat blood flow by 50% reduced PN2 by
17–21% (Table 4, models A
vs I).
Estimated PN2 levels during foraging
In the remainder of the analysis, the cardiovascular variables detailed in
model I were used. Fig. 4 shows
changes occurring in estimated venous N2 levels during and after a
dive by a king penguin. Central circulation PN2
rapidly increased leading to a concomitant increase in mixed venous
PN2 (Fig.
4). At 101 s, 7 s after the start of ascent, mixed venous
PN2 exceeded lung
PN2. At this time N2 flux was
reversed and re-distribution of available N2 continued according to
PN2 gradients within the body. Central
circulation PN2 exceeded lung and arterial
PN2 3 s after ascent was initiated. Despite
this, central circulation PN2 continued to
increase until 11 s after the start of the ascent. This delay is caused by
blood transit time (11 s arterial transit time during diving). Similarly,
PN2 in muscle and fat continued to increase
throughout the entire dive and even after the bird had returned to the surface
(Fig. 4). At the end of the 46
s surface interval, 96% of N2 taken up was removed from the central
circulation (max PN2=4.45 ATA,
PN2 at end of surface interval=0.884 ATA).
Thus, central circulation PN2 was still higher
than surface PN2, i.e. ambient lung
PN2=0.741 ATA after correction for water
vapour. Likewise, PN2 in muscle (1.03 ATA) and
brain (1.06 ATA) at the end of the surface interval were still higher than the
pre-dive ambient values by 39% and 44%, respectively. Fat
PN2 increased only by 0.5% during the dive to
0.745 ATA and decreased insignificantly (<0.01%) during the surface
interval. A surface interval duration exceeding dive duration by at least
fivefold would be required to remove excess N2 from the mixed
venous blood (data not shown). The fact that no tissue returned to ambient
PN2 levels indicates that repeated diving will
lead to a build-up of PN2.
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Estimated tissue and blood PN2 using model I
(Table 3) for a diving bout for
bird 3 (Table 2) are shown in
Fig. 5, consisting of 92 dives
with an average duration of 180 s (range 6–254 s), an average surface
interval of 69 s (range 10–452 s), an average depth for each dive of 52
m (range 0.2–85 m) and an average maximum depth of 87 m (0.5–143
m). During the bout, estimated PN2 increased in
all tissues. For a fast tissue (central circulation) the pattern of change in
PN2 more or less followed
Pamb (Fig. 5A
vs B). For tissues with an intermediate time constant
(brain and muscle), an initial rapid increase was followed by a slow decline
to values that became more or less stable
(Fig. 5C). For a slow tissue
(fat), there was a continuous increase throughout the entire bout
(Fig. 5D). Maximum estimated
PN2 at bout termination was 3.81 ATA for
central circulation, 2.24 ATA for muscle, 2.56 ATA for brain, 1.23 ATA for fat
and 3.54 ATA for mixed venous blood (Fig.
5, model I, Table
3A). Average estimated mixed venous
PN2 for all birds when surfacing at the end of
a dive bout was 1.54±0.07 ATA (range 1.47–1.62 ATA) with maximum
values ranging between 3.26 ATA and 3.62 ATA (model I,
Table 4). During the extended
surface interval following a dive bout, venous
PN2 initially decreased as N2 was
removed from the fast tissue (central circulation).
PN2 then followed removal of N2 from
the intermediate tissues and finally was held at a supersaturated state for an
extended period as fat PN2 slowly decreased
(Fig. 5D). Note that at the end
of the 2.3 h (160 min) interbout period, subcutaneous fat
PN2 was still higher than ambient surface
PN2.
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Estimated fat PN2 levels for each animal throughout an entire foraging trip are shown in Fig. 6. Average estimated fat PN2 (1.13±0.06 ATA; range: 1.05–1.23 ATA, Table 4, model I) at the end of a dive bout did not vary significantly between birds (P>0.1). In addition, fat PN2 very seldom reached levels higher than 2.0 ATA (Fig. 6). For the brain, average estimated PN2 at the end of a dive bout was 1.81±0.15 ATA (range: 1.67–1.98 ATA, Table 4, model I). The amount of N2 taken up by adipose tissue was positively correlated with the duration of the dive bout (P<0.01, Fig. 6).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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).
However, changes in heart rate during diving are very different in freely
diving birds (Froget et al.,
2004) compared with those that are forced to dive
(Ponganis et al., 1999).
Assuming no pulmonary diffusion limitation, the most important variable
affecting rate of N2 uptake and removal is
tot and regional blood
flow. When 26% of tot was
directed to muscle, mixed venous PN2 during a
dive to 34 m or 67 m showed reasonable agreement with observed values.
However, during a dive to 102 m mixed venous
PN2 was overestimated by 22% and 38% at 120 s
and 166 s into the dive, respectively (Fig.
1, solid black lines). With a 100% increase in muscle blood flow
during diving, or 52% of
tot directed to the muscle,
there was good agreement between measured and observed
PN2 for the dive to 102 m
(Fig. 1, dotted lines). The
reasonable fit between observed and estimated mixed venous
PN2 suggests that cardiovascular changes
throughout each dive could explain deviations between predicted and observed
PN2. For example, a stressed animal exhibiting
tachycardia during the initial stages of the dive explains the one outlying
data point during simulated dives to 68 m
(Fig. 1B). Parabronchial shunt,
caused by engorgement of lung capillaries
(Ponganis et al., 1999), could
be another explanation for the slight deviation between observed and predicted
mixed venous PN2 during the dive to 102 m
(Fig. 1A). However, as mixed
venous PN2 increased during the bottom phase of
the dive a certain level of gas exchange must occur even at 100 m. Therefore,
assuming that gas exchange is prevented at 100 m, this would provide the most
conservative estimate of tissue and blood
PN2.
This modeling approach allows prediction of tissue and blood
PN2 based on different initial conditions.
Admittedly, any selected initial conditions are likely to be wrong, at least
during parts of the foraging trip, and this could affect our conclusions. In
addition, no information exists on
tot and regional blood flow
distribution in freely diving birds. It was therefore important to assess how
changes in tot, regional
blood flow distribution and parabronchial shunt affected blood and tissue
PN2. The slight deviance in observed
versus predicted mixed venous PN2
during a forced dive to 102 m indicate either that we chose an incorrect
tot or regional blood flow
distribution, or that there was a certain level of parabronchial shunt. The
geometry and size of the air tubule makes it unlikely that it would be able to
collapse without structural damage and thereby be able to re-expand as the
pressure is reduced. Thus, the respiratory system of a diving bird is the
opposite of the mammalian respiratory system, where the parabronchi (or lung)
is a rigid structure and the air sacs are highly compliant. We assumed that
the parabronchi are at least 5 times as rigid as the air sacs and that the
parabronchial volume is 10% of the total volume of the respiratory system
(Powell and Hopkins, 2004).
Using this model of the respiratory system, complete collapse of the air sacs
occurs at 100 m (Denison and Kooyman,
1973; Stephenson,
2005). Increasing the ambient pressure at the time the air sacs
have collapsed could produce relatively negative pressures in the parabronchi
[the squeeze (Francis and Denison,
1999)], possibly leading to barotrauma. It has been suggested that
engorgement of the capillaries reduces parabronchial volume, thereby
preventing barotrauma. However, engorgement of the capillaries could impair
gas exchange by reducing the diffusion rate. As this question is still
unresolved, we decided to test how tissue and blood
PN2 would be affected if gas exchange ceased at
100 m. We therefore ran the model assuming a 100% pulmonary shunt for depths
exceeding 100 m. For the four birds, maximum
PN2 in muscle decreased by 28%, brain by 40%,
fat by 20% and central circulation by 45% (models A vs C,
Table 3,
Table 4). However, mean
PN2 upon reaching the surface at the end of a
dive bout only decreased by 8% for muscle, 10% for brain, 10% for fat, 3% for
central circulation and 5% for mixed venous
(Table 4, models A vs
C). Thus, even if gas exchange terminates at depths beyond 100 m, tissue and
blood PN2 levels approach those causing DCS
symptoms in terrestrial animals of similar size.
It has previously been suggested that the dive response may be a useful
mechanism to reduce N2 uptake during diving and thereby minimize
DCS risk (Fahlman et al.,
2006; Ponganis et al.,
1999). It was therefore surprising when an increase in blood flow
resulted in an increase in end bout PN2 in some
tissues and a decrease in others. For example, diving bradycardia caused a
substantial reduction in brain and central circulation
PN2, while muscle and fat
PN2 increased
(Table 4, models A vs
B). These data suggested that an increase in the regional blood flow when
tiss1/2
1.30 min results in a reduction in
PN2 as the bird returns to the surface
(Table 3,
Table 4). In contrast,
PN2 increased with a reduction in blood flow
when tiss1/2>11.3 min. In addition,
PN2 increased in both central circulation and
muscle when the regional flow to the muscle was increased and the flow to
central circulation reduced. This shows that the diving bradycardia does not
simply reduce N2 levels during repeated diving, as previously
suggested (Fahlman et al.,
2006; Ponganis et al.,
1999). To investigate these unexpected results further we plotted
diving tiss1/2 (Fig.
2) or surface tiss1/2
(Fig. 3) for each tissue
against end bout or end dive PN2, for a series
of different regional blood flow distributions. At the surface, an increase in
tissue blood flow, or a reduction in surface tiss1/2, reduced
PN2 at the end of the dive
(Fig. 3). For blood flow during
diving, on the other hand, the data suggested that end dive
PN2 increases to a maximum and then decreases
with increasing diving tiss1/2. Maximum
PN2 occurred at a diving
tiss1/2 around 1–1.5 min for all compartments. The
relationship was particularly pronounced for dives >50 m. Consequently, to
reduce blood and tissue PN2 a diving animal can
either increase or decrease tiss1/2 below this maximum.
However, the circulatory system delivers O2 and removes
CO2, so blood flow changes to each specific tissue is a trade-off
between the need to exchange metabolic gases and reducing DCS risk. Due to the
predicted extremely high brain PN2 at the end
of a bout or a dive for models A–H, regional blood flow was adjusted in
an attempt to minimize tissue and blood PN2.
The distributions were chosen to agree with the re-distribution of blood flow
during diving according to the dive response. Compared with model A, blood
flow was slightly increased to central circulation and muscle and reduced to
brain and fat (Table 3). This
resulted in an 87.5% decrease in brain blood flow during diving. This is
contrary to the common belief that brain blood flow is maintained in freely
diving mammals and birds (Butler and Jones,
1982) as the brain is believed to be hypoxia intolerant. The
cardiovascular values used for Model I substantially reduced brain and fat
PN2 but had little effect on central
circulation, muscle or mixed venous PN2.
Despite this marked reduction in brain PN2, end
of dive and bout PN2 remained above 1.6 ATA
(Table 4, models A–H
vs I). Consequently, models A–I provide us with reasonable
estimates of the range of blood and tissue PN2
that these birds experience during a foraging trip. The question is to what
extent deep diving mammals and birds can reduce blood flow to hypoxia
sensitive organs to reduce extreme PN2 without
ischemic injury. This will certainly be an intriguing area of research in the
future.
Our simulations showed that the average surface interval after a
representative dive is too short to remove all the N2 taken up
(Fig. 4). For all birds, end
bout mixed venous PN2 averaged 1.54 ATA with
values exceeding 3.68 ATA (Table
4, model I). These PN2 values
exceed those that cause a predicted 15% DCS rate in mammals of similar size
(Dromsky et al., 2000). The
maximum PN2 values are dependent on
N2 uptake and removal from fast tissues (central circulation, brain
and muscle). The magnitude of mixed venous PN2
upon surfacing depends on the behaviour of the bird during the ascent phase,
as N2 is rapidly removed from tissues with high blood flow.
Consequently, these tissues contribute only transiently to DCS risk. Removal
of N2 from fat, on the other hand, is much slower and leads to
prolonged elevated mixed venous PN2
(Fig. 5C). As fat
PN2 rises throughout the dive bout it
increasingly contributes to DCS risk as compared with fast tissues. Average
fat PN2 values when surfacing at the end of a
dive bout ranged between 1.05 ATA to 1.20 ATA (model I,
Table 4) while average maximum
end bout values were between 1.43 ATA to 1.65 ATA
(Fig. 6). Consequently, during
an extended surface interval between two dive bouts (interbout interval) the
likelihood of bubble formation and growth may be dependent on delayed
N2 removal from tissues with poor circulation and the extent to
which they have reached complete pressure equilibration (saturation). To avoid
DCS the bird may be forced to end a dive bout and stay at the surface for an
extended surface interval to remove N2 from the adipose tissues.
This could explain why these birds sometimes end dive bouts during daylight
hours when food should be plentiful and why they re-warm the periphery during
the interbout interval (A.S., J.-P. Gendner, C. A. Bost and Y.H., manuscript
submitted for publication). If so, this suggests that during prolonged diving
adipose tissues may become a liability and could contribute more to the risk
of decompression sickness as compared with other tissues
(Tikuisis and Gerth, 2003).
Interestingly, bout duration increased for each bird throughout the foraging
trip, causing an increase in end bout fat PN2
throughout the foraging trip (Fig.
6). The increase in bout duration could be due to increased
aerobic fitness or foraging efficiency. Alternatively, as subcutaneous fat
stores increase throughout the trip so does the N2 buffering
capacity, allowing longer bouts before dangerous N2 levels are
reached.
The high N2 capacitance of adipose tissues was suggested to act
as a N2 absorbent and reduce bubble formation during deep and short
duration dives (Behnke et al.,
1935). During these dives, PN2 in
fast tissues are elevated while PN2 in slow
tissues remain low. Supersaturation of mixed venous blood during decompression
from such a dive is therefore minimal and of short duration. Consequently, the
likelihood of bubble formation and growth is unlikely. In king penguins, this
resembles PN2 distribution during dives
performed early during a dive bout. This is in contrast to the elevated
adipose PN2 at the end of a bout that would
force the bird to undertake a long surface interval. Consequently, adipose
tissue could help buffer PN2 at the beginning
of a dive bout but be a liability after a long bout.
If dive bout terminations during the day are, at least in part, caused by elevated tissue PN2 levels, it would be expected that PN2 levels would be higher than those during bout termination events at night. There were no differences in tissue PN2 levels during interbout intervals occurring at day or night, suggesting that elevated N2 is not the prime reason that birds stop deep diving. It is possible that the diurnal vertical distance migrated through the water column is particularly extensive on clear days and that prey descend too deep and it becomes too energetically costly for birds to continue foraging. However, this is a complex subject that depends on light availability, the time available for travel to the prey patch and the horizontal and vertical abundance of prey. In any case, it is clear that king penguins may experience extremely high levels of N2 in blood and tissues and it is likely that they live with tissue and blood PN2 levels that would cause DCS in similarly sized terrestrial animals. While slow tissues may become a liability over the course of an extended dive bout, dive behaviour may significantly alter mixed venous PN2 at the end of individual dives due to its important effect on gas exchange in fast tissues.
A large proportion of dives by king penguins are performed to depths that
are probably too shallow to be foraging dives. The function of these dives is
currently unexplained. One suggestion is that these dives represent travel
between prey patches. Another possibility postulated
(Kooyman, 1989) is that these
dives help remove accumulated anaerobic by-products after a series of deep and
long dives that have exceeded the ADL. Gas exchange in general would benefit
from these short duration dives. During these dives, as compared with staying
at the surface, parabronchial and arterial PO2
would increase, enhancing diffusion of O2 into depleted blood and
tissues and aiding in removal of CO2 by the Haldane effect. Thus,
these dives would improve uptake of O2 and removal of
CO2 and help remove anaerobic by-products
(Castellini et al., 1988). The
amount of N2 removed from the tissues during these shallow dives
depends on the depth (ambient pressure), duration and
tot. As compared with
staying at the surface, these dives reduce the pressure difference between
tissue and lung PN2 and therefore the rate of
N2 removal. However, staying at the surface increases
supersaturation
[(PN2tiss–PN2amb)/PN2amb]
and therefore the probability of bubble formation and growth
(Tikuisis and Gerth, 2003). To
reduce DCS risk, the shallow decompression dives need to be deep enough to
reduce supersaturation but shallow enough to allow removal of N2.
According to the estimated PN2 of approximately
1.5–4.0 ATA, this depth would be between 10 and 30 m
(Pamb
2–4 ATA). This is close to the actual depth
observed for shallow dives that occur between deep foraging dives of king
penguins. Fig. 7 shows the
effect on mixed venous supersaturation in a bird either performing a series of
these short, shallow (<30 m) decompression dives between two dive bouts or
resting at the surface. In the case where the bird performs short and shallow
interbout dives, supersaturation seldom exceeds 0.2. For a bird resting at the
surface, on the other hand, supersaturation during the initial 5 min after the
last dive is as much as 300% higher. These initial high levels may increase
the likelihood of bubble formation and growth and could increase the risk of
DCS in a bird resting at the surface.
If birds end a dive bout due to elevated tissue and blood
PN2 how do they sense or detect risky levels of
N2? It is possible that the animals can sense a low amount of
bubbles without serious symptoms, e.g. `niggles'. By diving to a shallow
depth, bubble size and numbers are reduced and the symptoms are alleviated.
During repeated dives, the depth becomes shallower as more N2 is
removed during each dive, until there are no more symptoms at the surface (see
Fig. 7). Thus, if the short and
shallow dives are used to safely remove N2 we would expect them to
decrease in depth throughout the interbout period. Even if birds become aware
that a certain bubble load has been reached, we cannot exclude that
termination of a dive bout is nothing but a behaviour that occurs when the
bird is exhausted or when the prey patch has scattered. Regardless of the
mechanism for bout termination, the data presented in the present paper
suggest that tissue and blood PN2 at the end of
a dive is a complex function of the need to supply O2 to central
organs while at the same time reducing uptake of N2. The seminal
work by Ponganis et al. (Ponganis et al.,
1999), suggests that gas exchange does occur to some extent at 102
m or more in king penguins. We lack important information about
tot and blood flow
distribution in freely diving penguins and these variables are vital for
accurately determining tissue and blood PN2
levels in breath-hold diving animals. However, our mathematical model is a
useful tool that can be used to create alternative explanations for some of
the unusual behaviours seen in deep diving birds. The data presented here
provide a range of tissue and blood PN2
estimates that can be expected during foraging in king penguins. It is clear
that king penguins may experience extremely high levels of N2 in
blood and tissues and it is difficult to see how they avoid symptoms of DCS.
The results also raise the question as to what extent gas exchange continues
during deep diving in penguins, and does PN2
affect diving marine mammals?
List of symbols and abbreviations
tot
tiss
O2
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Acknowledgments |
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Behnke, A. R., Thomson, R. M. and Shaw, L. A.
(1935). The rate of elimination of dissolved nitrogen in man in
relation to the fat and water content of the body. Am. J.
Physiol. 114,137
-146.
Berne, R. M. and Levy, M. N. (1997). Cardiovascular Physiology. St Louis, MI: Mosby-Year Book.
Bevan, R. M. and Butler, P. J. (1992).
Cardiac-output and blood-flow distribution during swimming and voluntary
diving of the tufted duck (Aythya fuligula). J. Exp.
Biol. 168,199
-217.
Boycott, A. E., Damant, G. C. C. and Haldane, J. S. (1908). The prevention of decompression-air illness. J. Hyg. Lond. 8,342 -443.
Butler, P. J. and Jones, D. R. (1982). The comparative physiology of diving in vertebrates. Adv. Comp. Physiol. Biochem. 8,179 -364.[Medline]
Castellini, M. A., Davis, R. W. and Kooyman, G. L. (1988). Blood chemistry regulation during repetitive diving in Weddell seals. Physiol. Zool. 61,379 -386.
Cherel, Y., Charrassin, J. B. and Challet, E. (1994a). Energy and protein requirements for molt in the king penguin Aptenodytes patagonicus. Am. J. Physiol. 266,R1182 -R1188.[Medline]
Cherel, Y., Gilles, J., Handrich, Y. and Le Maho, Y. (1994b). Nutrient reserves dynamics and energetics during long-term fasting in the king penguin (Aptenodytes patagonicus). J. Zool. Lond. 234,1 -12.
Davis, R. W. and Kanatous, S. B. (1999). Convective oxygen transport and tissue oxygen consumption in Weddell seals during aerobic dives. J. Exp. Biol. 202,1091 -1113.[Abstract]
Denison, D. M. and Kooyman, G. L. (1973). The structure and function of the small airways in pinniped and sea otter lungs. Respir. Physiol. 17,1 -10.[Medline]
Dromsky, D. M., Toner, C. B., Survanshi, S., Fahlman, A.,
Parker, E. and Weathersby, P. (2000). Natural history of
severe decompression sickness after rapid ascent from air saturation in a
porcine model. J. Appl. Physiol.
89,791
-798.
Fahlman, A., Tikuisis, P., Himm, J. F., Weathersby, P. K. and
Kayar, S. R. (2001). On the likelihood of decompression
sickness during H(2) biochemical decompression in pigs. J. Appl.
Physiol. 91,2720
-2729.
Fahlman, A., Schmidt, A., Handrich, Y., Woakes, A. J. and Butler, P. J. (2005). Metabolism and thermoregulation during fasting in king penguins, Aptenodytes patagonicus, in air and water. Am. J. Physiol. 289,R670 -R679.
Fahlman, A., Olszowka, A., Bostrom, B. and Jones, D. R. (2006). Deep diving mammals: dive behavior and circulatory adjustments contribute to bends avoidance. Respir. Physiol. Neurobiol. 153,66 -77.[CrossRef][Medline]
Francis, T. J. R. and Denison, D. M. (1999). Pulmonary barotrauma. In The Lung at Depth (ed. C. E. G. Lundgren and J. N. Miller), pp. 295-374. New York: Marcel Dekker.
Froget, G., Butler, P. J., Woakes, A. J., Fahlman, A., Kuntz,
G., Le Maho, Y. and Handrich, Y. (2004). Heart rate and
energetics of free-ranging king penguins (Aptenodytes patagonicus).
J. Exp. Biol. 207,3917
-3926.
Grubb, B. R. (1982). Cardiac output and stroke
volume in exercising ducks and pigeons. J. Appl.
Physiol. 53,207
-211.
Handrich, Y., Bevan, R. M., Charrassin, J. B., Butler, P. J., Putz, K., Woakes, A. J., Lage, J. and Le Maho, Y. (1997). Hypothermia in foraging king penguins. Nature 388, 64-67.[CrossRef]
Jones, D. R., Bryan, R. M. J., West, N. H., Lord, R. M. and Clark, B. (1979). Regional distribution of blood flow during diving in the duck (Anas platyrhynchos). Can. J. Zool. 57,995 -1002.
Kayar, S. R., Parker, E. C. and Harabin, A. L. (1997). Metabolism and thermoregulation in guinea pigs in hyperbaric hydrogen: effects of pressure. J. Therm. Biol. 22,31 -41.[CrossRef]
Kety, S. S. (1951). The theory and applications of the exchange of inert gas at the lungs and tissues. Pharmacol. Rev. 3,1 -41.[Medline]
Kooyman, G. L. (1989). Diverse Divers. New York: Springer-Verlag.
Kooyman, G. L. and Ponganis, P. J. (1998). The physiological basis of diving to depth: birds and mammals. Annu. Rev. Physiol. 60,19 -32.[CrossRef][Medline]
Kooyman, G. L., Ponganis, P. J., Castellini, M. A., Ponganis, E.
P., Ponganis, K. V., Thorson, P. H., Eckert, S. A. and LeMaho, Y.
(1992). Heart rates and swim speeds of emperor penguins diving
under sea ice. J. Exp. Biol.
165,161
-180.
Olszowka, A. J. and Rahn, H. (1987). Gas store changes during repetitive breath-hold diving. In Man in Stressful Environment-Diving, Hyperbaric and Hypobaric Physiology (ed. K. S. Shiraki and M. K. Yousef), pp. 417-428. Springfield: Charles C. Thomas Publisher.
Ponganis, P. J., Kooyman, G. L., VanDam, R. and Le Maho, Y. (1999). Physiological responses of king penguins during simulated diving to 136 m depth. J. Exp. Biol. 202,2819 -2822.[Abstract]
Powell, F. L. and Hopkins, S. R. (2004).
Comparative physiology of lung complexity: implications for gas exchange.
News Physiol. Sci. 19,55
-60.
Sato, K., Naito, Y., Kato, A., Niizuma, Y., Watanuki, Y.,
Charrassin, J. B., Bost, C. A., Handrich, Y. and Le Maho, Y.
(2002). Buoyancy and maximal diving depth in penguins: do they
control inhaling air volume? J. Exp. Biol.
205,1189
-1197.
Scholander, P. F. (1940). Experimental investigations on the respiratory function in diving mammals and birds. Hvalrådets Skrifter 22, 1-131.
Stephenson, R. (2005). A theoretical analysis of diving performance in the Weddell seal (Leptonychotes weddelli). Physiol. Biochem. Zool. 78,782 -800.[CrossRef][Medline]
Stephenson, R., Jones, D. R. and Bryan, R. M., Jr (1994). Regional cerebral blood flow during submergence asphyxia in Pekin duck. Am. J. Physiol. 266,R1162 -R1168.[Medline]
Tikuisis, P. and Gerth, W. A. (2003). Decompression theory. In Bennett and Elliott's Physiology and Medicine of Diving (ed. A. O. Brubakk and T. S. Neuman), pp.416 -452. Edinburgh: W. B. Saunders.
Zapol, W. M., Liggins, G. C., Schneider, R. C., Qvist, J.,
Snider, M. T., Creasy, R. K. and Hochachka, P. W. (1979).
Regional blood flow during simulated diving in the conscious Weddell seal.
J. Appl. Physiol. 47,968
-973.
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