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First published online November 30, 2007
Journal of Experimental Biology 210, 4279-4285 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.011221
Returning on empty: extreme blood O2 depletion underlies dive capacity of emperor penguins
Center for Marine Biotechnology and Biomedicine, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093-0204, USA
* Author for correspondence (e-mail: pponganis{at}ucsd.edu)
Accepted 30 September 2007
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Key words: aerobic dive limit, blood gases, dive, emperor penguin, hypoxemia, PO2
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Introduction |
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; Robertson,
1995). This breath-hold capacity is dependent, in part, on
utilization and depletion of the blood O2 store
(Scholander, 1940). Since
dissociation of all O2 from hemoglobin (Hb) requires a low
O2 partial pressure (PO2), effective
utilization of the blood O2 store implies exceptional hypoxemic
(low PO2) tolerance in these animals. Prior
investigations of the diving physiology and behavior of emperor penguins at
the corralled, isolated dive hole of our Penguin Ranch research camp on the
sea ice of McMurdo Sound, Antarctica, have made such diving activity an ideal
model in which to investigate blood O2 depletion and hypoxemic
tolerance.
While under the sea ice of McMurdo Sound, emperor penguins primarily feed
on the sub-ice fish, Pagothenia borchgrevinki
(Ponganis et al., 2000). Dive
durations of 5–12 min are common, and dive depths are usually less than
100 m. During these dives, the birds undergo variable bradycardias
(Kooyman et al., 1992),
maintain aortic and vena caval temperatures near 37–39°C
(Ponganis et al., 2001;
Ponganis et al., 2004;
Ponganis et al., 2003) and
have an aerobic dive limit (ADL; dive duration associated with post-dive blood
lactate accumulation) of 5.6 min (Ponganis
et al., 1997b).
Particularly relevant to the current investigation was the recent
successful application of an air sac PO2
electrode and backpack recorder to diving birds at the Penguin Ranch
(Stockard et al., 2005).
PO2 profiles obtained via the
O2 electrode revealed that 42% of these voluntary dives of emperor
penguins had end-of-dive air sac PO2 values
less than 20 mmHg (1 mmHg=133.3 Pa). Such low
PO2 values are significant in comparison with
other birds for several reasons. First, the lowest of these air sac values in
emperor penguins is less than inspired air values (23 mmHg) of birds at
altitudes as high as 11 580 m (Black and
Tenney, 1980). Second, these values in free-diving emperor
penguins are also lower than the air sac PO2
values (
30 mmHg) of pekin ducks (Anas platyrhynchos) forcibly
submerged to the point of `imminent cardiovascular collapse'
(Hudson and Jones, 1986).
Third, because air sac PO2 represents the
maximum arterial PO2 and, in fact, is usually
greater than the simultaneous arterial value
(Powell, 2000;
Weinstein et al., 1985), these
low air sac values in emperor penguins imply that blood
PO2 values are commonly less than 20 mmHg. This
is remarkable in that blood O2 content at a
PO2 of 22 mmHg is very low (less than 5 ml
O2 dl–1 blood) in the high-altitude bird, the
bar-headed goose (Anser indicus), and is even less in pekin ducks and
pigeons (Columbia livia) (Black
and Tenney, 1980; Hudson and
Jones, 1986; Weinstein et al.,
1985).
Therefore, in order to further investigate hypoxemic tolerance and blood O2 depletion during dives, we equipped emperor penguins that were diving at the Penguin Ranch research camp with intravascular PO2 electrodes and backpack recorders. In addition, we measured PO2, O2 content, pH, PCO2 and lactate concentrations in arterial and venous blood samples from birds at rest. Our goals were to determine (1) the baseline blood respiratory variables in birds at rest, (2) the relationship of the final blood PO2 of a dive to dive duration, (3) the relationship of final blood PO2 of a dive to the ADL, and (4) the hypoxemic tolerance of emperor penguins.
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;
Ponganis et al., 1997b), and
were then released at the McMurdo Sound ice edge. Blood-sampling catheters or
PO2 electrodes/thermistors were inserted
percutaneously into the aorta or vena cava of emperor penguins under general
isoflurane anesthesia as described previously
(Ponganis et al., 1997b;
Ponganis et al., 2001;
Ponganis et al., 2004) and
below. Catheterizations were confirmed as arterial or venous by observations
of obvious pulsatile flows from arteries, by transduction of intravascular
pressure and/or by PO2 values of >250 mmHg
in arteries and <100 mmHg in veins during anesthesia with 100%
O2 ventilation (Ponganis et
al., 2004). After overnight recovery from anesthesia, birds were
allowed to dive at the isolated dive hole. After 1–2 days of diving and
data collection, probes and recorders were removed under general anesthesia.
Data from the recorders were downloaded to a personal computer and analyzed
with Microsoft Excel (OriginLab Corp., Northampton, MA, USA) and SPSS (SPSS,
Inc., Chicago, IL, USA) software. Means are expressed ± standard
deviation (s.d.). All procedures were approved under a UCSD Animal Subjects
Committee protocol and US Antarctic Treaty Permit.
Catheterizations, blood samples at rest
For blood analyses in birds at rest, arterial samples were obtained
via the femoral artery in one case and via the brachial
artery in the wing in two cases. Venous samples were obtained from the femoral
or axillary vein. The femoral artery was cannulated percutaneously with a 20 g
epidural catheter (Perifix catheter; B. Braun Medical Inc., Bethlehem, PA,
USA) via a 19 g thin-wall needle. Brachial arteries were catheterized
percutaneously with 4.5 cm, 20 g catheters (RA-04020; Arrow International,
Reading, PA, USA). Only short arterial catheters could be inserted in the wing
secondary to the axillary arterial plexus in emperor penguins
(Trawa, 1970). The femoral
vein was catheterized percutaneously
(Ponganis et al., 1999) with
5-Fr nylon catheters (Cook, Bloomington, IN, USA) or the 20 g epidural
catheters via the same technique used for the femoral artery. In two
cases, the axillary vein was catheterized with an epidural catheter
via a 16 g catheter introducer (Becton Dickinson, Sandy, UT, USA) in
the brachial vein of the wing. The femoral artery catheter and all venous
catheters were inserted 15–30 cm into the aorta and vena cava,
respectively. Catheters were flushed with heparinized (4 U heparin
ml–1) 0.9% saline. The portion of the catheter and stopcock
external to the body was filled with a pre-measured volume of 40% ethanol/60%
heparinized saline to prevent freezing of the external catheter solution
(Ponganis et al., 1997b).
Blood samples from birds at rest were obtained between two and four hours after recovery from anesthesia. During this time, the birds were kept inside the penguin transport box (45x45x120 cm) near their corral at ambient Antarctic temperatures (–10 to –20°C). Distraction of the calm bird by one observer via the open lid of the box allowed the collection of the sample (after withdrawal of >3x the tubing deadspace) by a second researcher.
Blood gas (PO2,
PCO2 and pH) and lactate concentration analyses
were conducted with a Series 200 i-STAT Portable Clinical Analyzer (CG4+
cartridge; Abbott Point of Care Inc., East Windsor, NJ, USA) at 37°C.
O2 content was determined with a Tucker chamber technique (Models
SI 782 O2 meter and 1302 O2 electrode; Strathkelvin,
Motherwell, Scotland, UK) (Tucker,
1967). Samples were analyzed within 10 min after collection. Blood
gas, O2 content and [lactate] were stable in the blood gas syringes
(Model 4041, Sims Portex, Keene, NH, USA) for as long as 4 h at room
temperature.
PO2 electrode, thermistor, recorder
For PO2 studies, a
PO2 electrode (Licox C1.1 Revoxode; Integra
LifeSciences, Plainsboro, NJ, USA) (manufacturer's specifications: 90%
response time <1 min, temperature correction factor <5%
°C–1, sensitivity error of <1%, and probe drift <2%
day–1) and thermistor (model 554; Yellow Springs Instruments,
Yellow Springs, OH, USA) (60% response time 0.2 s, sensitivity 0.05°C),
evaluated and calibrated as previously described
(Ponganis et al., 2001;
Ponganis et al., 2004;
Stockard et al., 2005), were
inserted 11–20 cm percutaneously into the vena cava or aorta
via the femoral vein or artery with a peel-away introducer (PLIP 4.5
or 5.0-18-9-DENNY introducer; Cook)
(Ponganis et al., 2001;
Ponganis et al., 2004;
Stockard et al., 2005). Prior
to insertion, the PO2 electrode was
heparin-coated with an aseptic one-min immersion in 7% TDMAC heparin solution
(Polysciences, Warrington, PA, USA).
In order to evaluate the effect of O2 consumption by the electrode on O2 depletion and a decline in PO2 in stagnant blood, the output of two O2 electrodes, each immersed in 2 ml of saline equilibrated with air at 38°C, was monitored when the equilibration air supply was shut off.
The custom PO2/temperature recorder (UFI,
Morro Bay, CA, USA), protected in an underwater housing (250 g,
15x6x3.5 cm) and connected to the electrode and thermistor with
waterproof cables (Sea Con, El Cajon, CA, USA; Impulse Enterprise, San Diego,
CA, USA), was mounted with a VelcroTM patch and cable ties as previously
described (Stockard et al.,
2005) while the bird was under anesthesia. It recorded both
parameters at 15 s intervals. The bird was also equipped with a Mk9 time depth
recorder (TDR, Wildlife Computers, Redmond, WA, USA) (sensitive to 0.5 m, 30
g, 6.5x1.7x1.7 cm; sample rate, 1 Hz)
(Stockard et al., 2005).
Calibration and assay temperatures
In prior studies, mean aortic and vena caval temperatures during dives
ranged from 38.3 to 39°C and from 37.2 to 38.3°C, respectively
(Ponganis et al., 2004;
Ponganis et al., 2003).
Therefore, the output of the PO2 electrode was
temperature corrected to 38°C and all data in the
PO2 profiles are reported for a temperature of
38°C. For a PO2 of 60 mmHg, a
±1°C temperature difference between an in vivo temperature
and 38°C would result in a very minor ±4 mmHg difference between
the in vivo PO2 and the
PO2 profile reported at 38°C
(Ashwood et al., 1983). For a
PO2 of 4 mmHg, the difference would be less
than 0.3 mmHg.
Results of blood gas analyses are reported at 37°C because previously
measured mean aortic and vena caval temperatures of emperor penguins at rest
were 37.3–38.0°C and 36.3–38.7°C, respectively
(Ponganis et al., 2004;
Ponganis et al., 2003). For a
PO2 of 60 mmHg,
PCO2 of 40 mmHg and a pH of 7.40 reported at
37°C, an in vivo temperature of 38°C would again result in
minimal changes in the in vivo values
(Ashwood et al., 1983;
Kiley et al., 1979), i.e. 64
mmHg, 42 mmHg and 7.39 pH units.
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PO2 profiles and final PO2 values during dives
Arterial PO2 profiles during dives were
similar to those previously observed in the air sacs
(Stockard et al., 2005). The
rise and fall in air sac and arterial PO2
profiles are illustrated in shallow dives of similar duration from two birds
in Fig. 2. Final arterial
PO2 values, recorded during the last 15 s of
dives as long as 6.8 min, ranged from 44 to 92 mmHg. The sample size of
arterial PO2 profiles (12 dives in three birds)
was limited due to thrombus formation on the electrode, saltwater leaks into
underwater connections and the technical difficulty of arterial
catheterization.
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) in
relation to dive duration are compared in
Fig. 4B.
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Blood temperatures during dives were similar to those recorded in previous
studies (Ponganis et al.,
2004; Ponganis et al.,
2003). Final temperatures recorded during the last 15 s of dives
ranged from 36.3 to 39.4°C.
In the test-tube evaluation of the depletion of O2 in saline due to the O2 consumption of the electrode, the PO2 declined from 5 to 8 mmHg over the first 4 min after the equilibration air supply was shut off to the test tubes. It did not decline further over 20 min for either of the two PO2 electrodes tested.
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;
Ponganis et al., 2001) at the
isolated dive hole (Fig. 1).
Dives of >100 m in depth were rare, and 47% of dives were >5.6 min, the
previously measured ADL (Ponganis et al.,
1997b). In 2004, birds often performed long-duration dives of
>16 min; this included a 23.1 min dive
(Fig. 3), which is now the
longest reported dive in an emperor penguin. Dive profiles and lack of hunting
ascents to the undersurface of the sea ice during these exceptional dives
suggested that the birds were foraging at 50–80 m depth.
Blood analyses of emperor penguins at rest
In emperor penguins at rest, mean arterial
PO2 was 68±7 mmHg, less than two-thirds
the mean value in the air sac of birds at rest
(Stockard et al., 2005). Large
air-sac-to-arterial differences in PO2 in birds
at rest are considered primarily due to ventilation–perfusion mismatch
(Powell, 2000). It is unknown
if this air-sac-to-arterial difference in PO2
in emperor penguins at rest is also partially secondary to the thickened
parabronchial capillary blood-to-air barrier that has been reported in these
birds (Welsch and Aschauer,
1986).
Although these arterial PO2 values in
emperor penguins are in the lower range of values reported for birds at rest
(Powell, 2000), the arterial
O2 content of 22.5±1.3 ml O2
dl–1 still represented greater than 91% saturation of the
previously measured average [Hb] of 18 g dl–1
(Kooyman and Ponganis, 1998).
Arterial pH, PCO2 and [lactate] in emperor
penguins at rest were characteristic of other avian species
(Powell, 2000) and are
consistent with a lack of stress during the sampling procedure. Venous
PO2, O2 content, pH,
PCO2 and [lactate] were consistent with the
observed arterial values and resulted in an estimated 70% venous Hb
saturation.
PO2 profiles and final PO2 values during dives
Arterial PO2 profiles reflected the effects
of compression hyperoxia and O2-store depletion previously
documented in the air sacs during dives
(Stockard et al., 2005). For
example, during a 5.3-min, 60-m deep dive, arterial
PO2 increased from an initial value of 98 mmHg
to a peak value of 257 mmHg and then gradually decreased to a final value of
76 mmHg near the end of the dive. Fig.
2 demonstrates the similarity of arterial and air sac
PO2 profiles in two different birds during
shallow dives of short duration. Near the ends of some dives, the compression
hyperoxia resulted in arterial PO2 values that
were greater than the mean value (68±7 mmHg) of birds at rest.
Venous PO2 did not always simply decline during dives but sometimes increased (Fig. 2). This accounts for final dive values (Fig. 4A) that are greater than those of birds at rest. In addition, there was a wide range of pre-dive venous PO2 levels (Figs 2 and 3). Prior to a 23.1 min dive (Fig. 3), the blood O2 store was optimized with an elevated pre-dive venous PO2 of 63 mmHg. This value was not only greater than that of birds at rest but was nearly equivalent to arterial values of birds at rest. These findings support the concept that the blood O2 store of emperor penguins can be enhanced by `arterialization' of venous blood.
Although final venous PO2 declined in relation to dive duration, the relationship was variable; e.g. at a dive duration of 5.6 min (the ADL), final venous PO2 values spanned a range of 40 mmHg. These final venous PO2 data and the previously published final air sac PO2 data provide evidence that the total body O2 store is not depleted at the ADL. In fact, the body O2 store is still not depleted even after many minutes beyond the ADL (Fig. 4). The wide range of final values for a given dive duration was consistent with variations in the rates of decline of PO2 in the individual venous profiles and, presumably, was related to differences in rates of O2 consumption during dives. The minimum rate at which final venous PO2 declined in relation to dive duration of emperor penguins at the isolated dive hole is described by the exponential regression in Fig. 4A.
We also propose that venous PO2 profiles and
end-of-dive values, especially during the latter portions of long dives,
approximate arterial values. Comparison of final air sac
(Stockard et al., 2005) and
venous PO2 values from dives of emperor
penguins reveals that final air sac values become indistinguishable from final
venous values during longer dives (Fig.
4B). This is particularly apparent after dives beyond the ADL
(Fig. 4B). Arterial
PO2 data, available over a limited range of
relatively short dive durations, occupy the same range as air sac values and,
in some cases, overlap venous values. Given the similar distributions of
arterial, air sac and even some venous final
PO2 values for short dive durations, and the
assumption that air sac PO2 represents maximal
arterial PO2, we think that venous final
PO2 values approximate arterial final
PO2 values for long dives. Similar
equilibrations of venous and arterial PO2
values have also been reported in seals
(Elsner et al., 1964;
Stockard et al., 2007). Thus,
as indices of the entire blood O2 store, the venous
PO2 profiles from the longer dives in this
study demonstrate that emperor penguins clearly push the limits of hypoxemia
and, indeed, are capable of `returning on empty' to the dive hole. In 29% of
dives, final venous PO2 values were less than
20 mmHg; in some dives, PO2 reached values as
low as 1–6 mmHg. These final PO2 values
are well below the arterial and venous thresholds (20–25 mmHg) for
cardiovascular collapse in pekin ducks
(Hudson and Jones, 1986) and
are also less than arterial PO2 (22 mmHg) in
bar-headed geese at 11 580 m altitude
(Black and Tenney, 1980). In
the 23 min dive of an emperor penguin, PO2 was
less than 20 mmHg for 8 min and eventually reached 6 mmHg
(Fig. 3).
One might question whether the extremely low final venous
PO2 data could be secondary to O2
consumption by the electrode in blood made stagnant by the bradycardia and low
cardiac output of diving. We think this is unlikely for several reasons.
First, low PO2 values also occurred in the air
sacs, which should not be affected by stagnant blood. Second, given the stroke
volume and blood volume of emperor penguins
(Kooyman et al., 1992;
Ponganis et al., 1997a), even
if heart rate were 5 beats min–1 during the last 10 min of
the 23 min dive, the entire blood volume would circulate during that time
period. Presumably, there would still be some flow past the electrode in that
situation. Third, low final venous PO2 values
also occurred during short dives, which have higher heart rates
(Kooyman et al., 1992) that
should be associated with higher blood flows. Fourth, during the initial
post-dive portion of the surface interval, venous
PO2 often stayed the same
(Fig. 3) or even decreased
further (P.J.P., unpublished data). This lack of an immediate increase in
venous PO2 during the tachycardia
(Kooyman et al., 1992) and
presumed high blood flows of the initial surface period again support our
argument that the low values during dives are not secondary to the localized
depletion of O2 in a stagnant layer of blood around the electrode.
Fifth, in the test-tube evaluation of the potential effect of the
PO2 electrode itself on O2 depletion
in saline, there was only a minimal initial decline in
PO2 over 4 min, and then no change thereafter.
This change in PO2 in saline should be the
maximum potential effect of the electrode since localized O2
depletion in blood would be buffered by release of O2 from Hb.
Therefore, we expect that the localized depletion of O2 by the
electrode in blood would be even less and that the low venous
PO2 values in this study are not secondary to
O2 consumption by the electrode.
These low PO2 values in the blood and
respiratory systems of diving emperor penguins are also remarkable in
comparison to mammalian indices of hypoxemia, including (a) the typical
arterial PO2 criterion of 60 mmHg for treatment
of human patients (Nunn,
1977), (b) end-tidal PO2 values of
35 mmHg from climbers on ambient air at the top of Mount Everest
(West et al., 1983), (c) human
thresholds for shallow-water blackout near 25 mmHg
(Ferrigno and Lundgren, 1999),
(d) mixed venous PO2 values of 27–34 mmHg
in terrestrial mammals exercising at maximal O2 consumption
(Taylor et al., 1987), (e)
femoral venous PO2 values of 20 mmHg in humans
exercising at maximal O2 consumption
(Roca et al., 1992) and (f)
arterial and end-tidal PO2 values of
15–20 mmHg in free-diving Weddell seals (Leptonychotes
weddellii) and bottlenose dolphins (Tursiops truncatus)
(Ponganis et al., 1993;
Qvist et al., 1986;
Ridgway et al., 1969). The
only PO2 values equivalent to the extremes of
hypoxemia found in these free-diving emperor penguins are the arterial and
venous PO2 levels (10 and 3 mmHg, respectively)
found in harbor seals (Phoca vitulina) forcibly submerged to an
electroencephalographic threshold for hypoxemic brain damage
(Kerem and Elsner, 1973).
These findings of extreme hypoxemia in emperor penguins also suggest that,
in contrast to the Hb of the pekin duck or pigeon
(Hudson and Jones, 1986;
Weinstein et al., 1985), the
Hb of the emperor penguin is not stripped of all its O2 at a
PO2 of 20 mmHg. In other words, the
P50 (PO2 at 50%
O2 saturation of Hb) of whole blood in emperor penguins is probably
much lower than the P50 of pekin ducks (42–52 mmHg)
(Black and Tenney, 1980;
Lutz, 1980;
Powell, 2000) and perhaps even
lower than the P50 of isolated, reconstituted emperor
penguin Hb (36 mmHg) (Tamburrini et al.,
1994). Rather, it is probably closer to the lowest whole-blood
P50 values (30–34 mmHg) found in Adelie, gentoo and
chinstrap penguins (Pygoscelis adeliae, P. papua, P. antarctica) and
in high-altitude-adapted birds such as the bar-headed goose
(Black and Tenney, 1980;
Milsom et al., 1973;
Petschow et al., 1977). This
suggestion of a relatively low P50 in the emperor penguin
is supported by the blood gas and O2 content analyses of these
birds at rest. At a mean venous PO2 of 41 mmHg,
mean O2 content was 17.4 ml O2 dl–1,
which represents approximately 70% saturation of an average Hb concentration
of 18 g dl–1 (Kooyman and
Ponganis, 1998).
In comparison to the P50 of the pekin duck, a lower
P50 in the emperor penguin would not only increase blood
O2 content during hypoxemia but it would also enhance dive capacity
by allowing more complete depletion of the respiratory O2 store. In
the pekin duck forcibly submerged to the point of `imminent cardiovascular
collapse', 25% of the respiratory O2 store was still unused because
the blood contained almost no O2 at an air sac
PO2 near 30 mmHg
(Hudson and Jones, 1986).
In conclusion, intravascular/air sac PO2
profiles in diving emperor penguins have revealed that their dive capacity is
at least partially achieved through optimum management of the
blood/respiratory O2 stores and extreme hypoxemic tolerance. The
blood PO2 profiles provide insight into the
nature and magnitude of physiological responses during the dive as well as
into biochemical/molecular mechanisms underlying hypoxemic tolerance. In
particular, a Hb with high O2 affinity (low
P50) in penguins is essential not only to enhance blood
O2 content during hypoxemia but also to allow depletion of the
respiratory O2 store, which in emperor penguins constitutes 19% of
the total body O2 store (Kooyman
and Ponganis, 1998). Other mechanisms of such extreme hypoxemic
tolerance may include increased capillary densities, modifications in reactive
O2 species production and/or scavenging, and changes in the
concentration and function of neuroglobin and cytoglobin. In addition to their
relevance to the diving capacity and biology of emperor penguins, these
potential cellular adaptations may also serve as models for improved
understanding and treatment of human hypoxemic/ischemic pathologies.
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Acknowledgments |
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