Air sac PO2 and oxygen depletion during dives of emperor penguins
1 Center for Marine Biotechnology and Biomedicine, Scripps Institution of
Oceanography, University of California San Diego, La Jolla, CA 92093-0204,
USA
2 Anesthesiology Department, US Naval Medical Center, Balboa Hospital, San
Diego, CA 92134, USA
3 International Coastal Research Center, The Ocean Research Institute,
University of Tokyo, 2-106-1 Akahama, Ostuchi Iwate 028-1102,
Japan
* Author for correspondence (e-mail: pponganis{at}ucsd.edu)
Accepted 12 May 2005
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: air sac, Aptenodytes forsteri, dive, electrode, emperor penguin, hypoxia, metabolic rate, oxygen
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
A PO2 electrode (Licox C1 Revoxode; Integra
LifeSciences, Plainsboro, NJ, USA) and thermistor (model 554; Yellow Springs
Instruments, Yellow Springs, OH, USA) were inserted percutaneously 1014
cm through a peel-away catheter (a slit 14 g Angiocath catheter; Becton
Dickinson, Sandy, UT, USA) into the posterior thoracic air sac while birds
were under general isoflurane anesthesia
(Ponganis et al., 2001). The
probes were secured to the feathers with TesaTM tape and LoctiteTM
glue as previously described (Ponganis et
al., 2001
). The insertion site was along the lateral body wall,
approximately 20 cm below the axilla, and between two ribs overlying the
posterior thoracic air sac. The probes were connected via a
waterproof cable to a custom-built microprocessor recorder (UFI, Morro Bay,
CA, USA), which was attached to feathers of the mid-back with 5-min epoxy glue
(Devcon; Danvers, MA, USA), a VelcroTM patch and cable ties. After
overnight recovery, the birds were provided access to the dive hole for one
day. On the morning following the dive day, the recorder and probes were
removed under general anesthesia.
Air sac PO2 and temperature were recorded at
15-s intervals. In addition to the
PO2/temperature recorder (250 g,
15x6x3.5 cm), a Mk9 time depth recorder (TDR; Wildlife Computers,
Redmond, WA, USA; sensitive to 0.5 m, 30 g, 6.7x1.7x1.7 cm) was
attached with 5-min epoxy glue, VelcroTM and cable ties to
feathers along the mid-line back just above the tail. Depth was recorded at
1-s intervals. The TDR pressure output was verified in a pressure chamber at
Scripps Institution of Oceanography. The temperature probes (sensitive to
0.05°C, 0.2-s 60% response time) were calibrated as previously described
(Ponganis et al., 2001).
The manufacturer's specifications for the PO2 electrode include a zero offset of <1 mmHg, a linear response, probe-sensitivity error of <1%, a probe drift of <2% day1, a 1-min 90% response time, and a temperature correction factor for probe output of <5% deg.1. PO2 electrode responses were evaluated in 0.9% saline-filled (8 ml) test tubes in a water bath (ThermoNESLAB RTE 7; Portsmouth, NH, USA) at 38°C by bubbling the saline with appropriate gases: 100% N2 (ultra high purity grade 5.0; minimum purity 99.999%; WestAir Gases, San Diego, CA, USA) for a 0% O2 value, 3% O2 (primary standard grade; actual purity 2.99%; WestAir Gases), room air (21% O2) or 100% O2 (ultra high purity grade 4.4; minimum purity 99.994%; WestAir Gases).
For probe evaluation, the PO2 electrode output was recorded at 5-s intervals for the first 45 s, 15-s intervals from 45 s to 2 min, and 30-s intervals from 2 min until a stable output was reached. Upon stabilization of output, the probe was transferred to the next tube, progressing through a series that allowed for the recording of each possible transition among the varying oxygen concentrations. This allowed calculation of response time, calculation of regression calibration equations over different ranges of % O2 and determination of drift over 48 h of continuous use. The temperature correction factor was determined by recording the electrode output at 21% O2 between 37 and 42°C.
The effect of pressure on electrode output was evaluated with compression in a water-filled pressure chamber. In addition, the electrode response in air was also evaluated in the McMurdo Station recompression chamber with 10-m step compressions to a final depth of 50 m.
For deployment in the field, the PO2 electrode was calibrated with 100% N2 and room air at 38°C in a sterile, saline-filled test tube. Percentage O2 was converted to PO2 (mmHg) with the use of the local barometric pressure (available from the McMurdo Station weather service) after subtraction of the vapor pressure of water. All PO2 values are therefore expressed in mmHg; in figures, the corresponding values in kPa are also expressed, assuming 1 mmHg=0.133 kPa.
After removal from the bird, TDR and PO2/temperature recorder outputs were downloaded to a laptop PC. Recorder output was converted to data in Excel with the use of appropriate calibration equations; PO2 probe output was first corrected to 38°C with a 4% deg.1 temperature correction factor (see Results). Data were analyzed and illustrated graphically using Excel, Origin and SPSS software. Statistical significance was assumed at P<0.05. All data are expressed as means ± S.D. unless otherwise stated.
The final PO2 was recorded during the final 15 s of the dive. End-of-dive PO2 was calculated from the final PO2 recorded during a dive by first calculating the O2 fraction at the depth at which the final PO2 was recorded [i.e. final PO2/(ambient pressure vapor pressure of water)] and by then using that fraction to calculate the equivalent PO2 at the surface [O2 fraction x (barometric pressure vapor pressure of water)]. These calculated variables were considered the closest possible approximation of end-of-dive PO2 and O2 fraction available from the data. In O2 fraction calculations, 100% humidity was assumed in the air sac.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
|
Output of the PO2 electrode was relatively stable over 48 h at 0, 3 and 21% O2; however, at 100% O2, electrode output drifted significantly over time from the initial reading (Fig. 2). Percentage changes in output of four electrodes at 0, 21 and 100% O2 at 24 and 48 h were 0, 7.3±5.1 and 30.8±7.3% and 0, 10.5±5.8 and 35.6±7.7%, respectively. This drift resulted in a decrease in calculated PO2 with time (calculated with the original linear regression equation for initial data points at 0 and 21% O2 at time 0; see Table 2). The magnitudes of these decreases were: 0 mmHg PO2 at 0% O2, 1115 mmHg PO2 at 21% O2 and 199229 mmHg PO2 at 100% O2 at 24 and 48 h.
|
|
The 90% response times from 0 to 21% O2 in four electrodes were 0.8±0.1, 0.8±0.2 and 1.0±0.1 min at 0, 24 and 48 h, respectively. See typical responses to step changes in O2 concentration in Fig. 1. Detailed analysis of probe 1 for 12 step changes between 0, 3, 21 and 100% O2 revealed mean 90% response times of 1.1±0.1 min at 0 h, 1.3±0.2 min at 24 h and 1.3±0.4 min at 48 h.
PO2 electrode output of four probes at 21% O2 changed by 4.2±0.4% deg.1 between temperatures of 37 and 42°C. Electrode output did not change during compression in a water-filled pressure chamber to 51 atmospheres absolute (ATA; 500 m depth). Output of an electrode in air in a recompression chamber increased during compression and returned to baseline with decompression to ambient, surface pressure (Fig. 3). Response time, calibration equations and drift of PO2 electrodes suspended in the gas phase above the saline in the stoppered test tubes were similar to those parameters of the same electrodes immersed in saline.
|
|
Mean air sac PO2 ranged from 114 to 130 mmHg during 3-h periods when the penguins were resting overnight in the corral (Table 3). Start-of-dive PO2 (the last surface value prior to the start of a dive) was 136±8 mmHg, corresponding to 19.6±1.2% O2. Start-of-dive PO2 did not correlate with either dive duration or maximum depth of dive (r=0.09 and 0.12, respectively, P>0.05). Air sac PO2 typically increased during descent and then gradually decreased during the latter portion of the dive (Fig. 5). The final PO2 during a dive (the last recorded value during the dive) ranged from 0 to 90 mmHg (Fig. 6). The end-of-dive PO2 (the final PO2 of a dive corrected to 0-m depth) ranged from 0 to 80 mmHg, corresponding to a 011.7% air sac O2 fraction (Fig. 7). End-of-dive PO2 and O2 fraction decreased exponentially with increasing dive duration (Fig. 7). The mean net change in air sac O2 fraction during a dive was 16.5±2.8%; the percentage of available air sac O2 depleted during a dive ranged from 42 to 100% (Fig. 8).
|
|
|
|
|
Mean air sac temperature during rest periods at night ranged from 37.1 to 38.3°C (Table 3). Mean air sac temperatures during individual dives ranged from 36.1 to 38.7°C in all birds. Mean temperature during dives of individual birds did not correlate with diving duration (r<0.02, P>0.05). Typically, air sac temperature increased slightly during dives (Fig. 9).
|
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The major limitation of the electrode was its response to 100% O2. During initial calibration, the magnitude of the electrode's output at 100% O2 was, on average, about 8% less than expected in comparison with the outputs at <21% O2. In addition, there was a large drift (a decrease as great as 30%) in the electrode's 100% O2 response over 2448 h (Fig. 2). Both the decreased sensitivity at 100% O2 and the drift of that response over time made it impossible to either construct an accurate linear regression calibration over the entire range of 0100% O2 or use a second calibration equation between 21% and 100% O2 for high PO2 values.
We conclude from this evaluation that the PO2 electrode should allow us to achieve the primary goal in this project, namely to determine the initial and end-of-dive PO2. Use of a 021% O2, or 0321% O2 calibration equation for each electrode yields accurate calculations of PO2 between 0 and 21% O2, the range of O2 concentration expected prior to and at the end of a dive. The primary limitations in interpretation of the data in this range are the small amount of drift in the electrode response over time and the 1-min response time of the electrode. The electrode should also provide a qualitative record for PO2 values above the calibration range, such as might occur due to air sac compression at depth. However, such hyperoxic values will not be quantifiable because of the less-than-expected electrode output and the drift of the electrode response at higher PO2 values. Finally, because instantaneous air sac PO2 may change quickly with rapid changes in depth, the response time of the electrode may create a lag between the instantaneous air sac PO2 and the electrode reading.
PO2 electrode location
The posterior thoracic air sac was chosen as the location for insertion of
the PO2 electrode because of its anatomical
access, the safety of the procedure at this site, the lack of effects of the
probe at this site on behavior and the use of this air sac in prior studies of
penguins (Kooyman et al.,
1973; Scholander,
1940
). Although gas composition of the cervical air sacs is
considered to most closely represent end-parabronchial gas
(Powell et al., 1981
), the
electrode was not placed in those air sacs because of concern over (1) safety,
(2) disturbance of behavior due to interference with neck movements and (3)
the potential for electrode damage due to body movement and preening.
Placement of the O2 electrode in the posterior thoracic air sac,
or indeed in any air sac, might be considered a limitation in trying to
estimate O2 depletion of the entire respiratory system of a diving
penguin. This is because air flow and gas mixing within the avian respiratory
system, even during routine respiration, are complex and incompletely
understood (Powell and Hempelman,
1985; Scheid,
1979
; Torre-Bueno et al.,
1980
). However, in swimming penguins, interclavicular-air-sac and
posterior-thoracic-air-sac pressure oscillations are associated with wing
beats and have been considered a mechanism to enhance gas mixing and gas
exchange (Boggs et al., 2001
).
Such pressure differentials within the air sacs may also contribute to air sac
gas mixing and movement of air through the lung in emperors diving at the
isolated dive hole since these birds stroke continuously in this situation
(Van Dam et al., 2002
).
Therefore, despite incomplete knowledge of air flow patterns in the
respiratory system during a dive, we feel that the posterior-thoracic-air-sac
PO2 data are a reasonable estimate of the
overall, average PO2 of the respiratory
system.
Dive behavior
The dive behavior of the birds in this experiment was typical of emperors
foraging at an isolated dive hole. The dives were less than 100 m in depth and
ranged to almost 11 min induration. Although similar in duration to many dives
at sea, dive depths were only in the shallow range of the depths reached by
emperors at sea (Kooyman and Kooyman,
1995). 55% of dives were greater than the 5.6-min ADL previously
measured in emperors diving at an isolated dive hole
(Ponganis et al., 1997
). This
type of diving pattern is similar to that in prior studies in which heart rate
and swim speed (Kooyman et al.,
1992
), FMR (Nagy et al.,
2001
), stroke frequency (Van
Dam et al., 2002
) and feeding behavior (primary prey;
Pagothenia borchgrevinkii;
Ponganis et al., 2000
) have
been documented in penguins diving at the isolated dive hole.
Air sac temperature
Air sac temperature at rest was within the range of temperatures measured
previously at multiple body sites in emperor penguins (Ponganis et al.,
2001,
2003b
). Only minor
fluctuations occurred during and between dives
(Fig. 9), and mean dive
temperature did not correlate with diving duration. As in past studies of
temperature regulation during diving of emperor penguins at the isolated dive
hole, there was no evidence for a hypothermic extension of aerobic dive
time.
Air sac PO2
Compression hyperoxia and O2 depletion
Air sac PO2 during rest periods and prior to
diving was similar to that previously reported in other penguins (measured as
% O2; Kooyman et al.,
1973; Scholander,
1940
). There was no correlation between start-of-dive
PO2 and dive duration.
PO2 profiles during dives demonstrated the net
effect of both ambient pressure changes and continued O2
consumption during a dive (Fig.
5). The peak PO2 values in these
profiles are probably an underestimate of the actual peak air sac
PO2 because of the decreased electrode
sensitivity at high PO2 values and because of
the lag time of the electrode response. Nonetheless, the profiles provide an
excellent example of compression hyperoxia and O2 depletion during
diving. Continued oxygen depletion from the respiratory system of these
penguins should be expected since (1) these dives are shallow, (2) gas
exchange continues during simulated dives in other penguin species to depths
as great as 136 m (Kooyman et al.,
1973
; Ponganis et al.,
1999
) and (3) a continuous strokeglide swim pattern
(Van Dam et al., 2002
) should
maintain movement of air through the lungs and enhance gas exchange
(Boggs et al., 2001
).
Hypoxic tolerance
The final PO2 values of dives
(Fig. 6) were recorded at depth
during the last 15 s of diving, ranged from 0 to 90 mmHg and are the closest
available approximation of the instantaneous air sac
PO2 during the latter phases of ascent. The
final air sac PO2 was less than 20 mmHg in 42%
of all dives. As such, these data demonstrate significant hypoxic tolerance in
the emperor penguin. For, if air sac PO2 is
representative of the PO2 in the parabronchial
air capillary of the penguin lung, these values are the maximum arterial
PO2 values near the ends of these dives.
Depending on the degree of shunt through the lung, the actual arterial
PO2 value may be even lower. For example, in
bar-headed geese (Anser indicus) exposed to 5% inspired
O2, arterial PO2 was 29 mmHg, which
is 5 mmHg less than the inspired PO2 of 34 mmHg
(Black and Tenney, 1980).
How emperors avoid shallow water blackout under such conditions remains a
mystery. The final PO2 values in 42% of all
dives were less than air sac and intravascular
PO2 values in maximally force-submerged ducks
(Hudson and Jones, 1986). Since
the P50 of emperor penguin hemoglobin (Hb) is similar to
those of the Hbs of high-altitude birds
(Black and Tenney, 1980
;
Tamburrini et al., 1994
), Hb
saturation at a given PO2 should not be
exceptional. It is conceivable that venous PO2
might be greater than the extremely low air sac values during long dives and
that a 100% pulmonary shunt would avoid gas exchange and preserve available
O2 for delivery to the brain. However, there is no evidence,
especially at shallow depth, for this mechanism of cessation of gas exchange
(Kooyman et al., 1973
).
Oxygenation of carotid blood via the avian ophthalmic rete
(Bernstein et al., 1984
;
Pinshow et al., 1982
) is
unlikely since continued passage of fresh air over nasal and oral mucosa will
not occur during a dive. On the other hand, adaptations in the brain may also
contribute to increased cerebral hypoxemic tolerance. For instance, increased
capillary density in the brains of harbor seals (Phoca vitulina) may
account for the harbor seal's tolerance of arterial
PO2 as low as 10 mmHg
(Kerem and Elsner, 1973
). In
this regard, birds, in general, have high brain capillary densities
(Faraci, 1986
). Elevated
concentrations of neuroglobin, the recently discovered O2-binding
protein in the brain (Burmester et al.,
2000
), may also represent another potential mechanism for
increased cerebral hypoxemic tolerance.
Respiratory O2 store depletion
End-of-dive PO2 values (final
PO2 during a dive corrected to 0-m depth) were
calculated to provide an estimate of the end-of-dive respiratory O2
fraction (% O2) and examine the magnitude and rate of respiratory
O2 depletion during diving. The end-of-dive air sac O2
fraction decreased exponentially with dive duration
(Fig. 7). Assuming that these
air sac O2 fractions are representative of the entire respiratory
system, these calculations indicate that, depending on the duration of the
dive, 42100% of available air sac O2 is consumed during the
dive (Fig. 8). In dives with
durations greater than the ADL, the end-of-dive air sac O2 fraction
ranged from 0 to 4%, corresponding to PO2
values of 028 mmHg. Although an absolute value of 0% O2 may
be secondary to sampling or measurement artifact, these low values are
consistent with significant depletion of the respiratory O2 store
during diving. The data from these long dives also demonstrate, as has been
previously emphasized (Kooyman and
Ponganis, 1998), that the onset of post-dive lactate accumulation
in emperors is not associated with the complete depletion of all O2
stores.
|
The DRV and O2 fraction calculations resulted in a mean
respiratory O2 store depletion rate of 2.1±0.8 ml
O2 kg1 min1
(Fig. 10). This value is about
one-third the measured and predicted resting metabolic rate for a penguin of
this body mass (Kooyman and Ponganis,
1994; LeMaho et al.,
1976
; Pinshow et al.,
1977
) and is much less than the 511 ml O2
kg1 min1 respiratory O2
depletion rates previously measured during forced submersions and simulated
dives of other penguin species (Kooyman et
al., 1973
; Scholander,
1940
). This supports the concept that respiratory O2
consumption is low during diving, most likely regulated by reductions in heart
rate and peripheral blood flow (Kooyman et
al., 1992
; Scholander,
1940
). In addition, the respiratory O2 store depletion
rates of dives of emperor penguins decreased exponentially with diving
duration and ranged from 1 to 5 ml O2 kg1
min1 (Fig.
10), demonstrating that the rates of respiratory O2
store depletion of individual dives were variable and dependent on the
duration of the dive and probably also on dive behavior.
These calculations represent the first estimation of one component of the
total O2 store depletion rate and metabolic rate during the dive of
an emperor penguin. They are consistent with hypothesized low diving metabolic
rates, which were based on oxygen consumption during flume swimming, and on
observed differences between wing beat frequency during flume swimming
versus diving (Kooyman and
Ponganis, 1994). These values also suggest that the O2
consumption rate during a dive is much less than the FMR of emperors at the
isolated dive hole (21 ml O2 kg1
min1; Nagy et al.,
2001
). Such a low diving metabolic rate would be consistent with
the inability to distinguish differences in the Nagy et al.
(2001
) study between FMR of
hand-fed penguins and FMR of birds that foraged for food.
![]() |
Acknowledgments |
---|
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Bernstein, M. H., Duran, H. L. and Pinshow, B. (1984). Extrapulmonary gas exchange enhances brain oxygen in pigeons. Science 226,564 -566.[Medline]
Black, C. P. and Tenney, S. M. (1980). Oxygen transport during progressive hypoxia in high-altitude and sea-level waterfowl. Res. Physiol. 39,217 -239.[CrossRef][Medline]
Boggs, D. F., Baudinette, R. V., Frappell, P. B. and Butler, P. (2001). The influence of locomotion on air-sac pressures in little penguins. J. Exp. Biol. 204,3581 -3586.[Medline]
Burmester, T., Weich, B., Reinhardt, S. and Hankein, T. (2000). A vertebrate globin expressed in the brain. Nature 407,520 -523.[CrossRef][Medline]
Butler, P. J. and Jones, D. R. (1997). The
physiology of diving of birds and mammals. Physiol.
Rev. 77,837
-899.
Faraci, F. M. (1986). Circulation during hypoxia in birds. Comp. Biochem. Physiol. A 85,613 -620.[CrossRef][Medline]
Hudson, D. M. and Jones, D. R. (1986). The influence of body mass on the endurance to restrained submergence in the Pekin duck. J. Exp. Biol. 120,351 -367.
Kerem, D. and Elsner, R. W. (1973). Cerebral tolerance to asphyxial hypoxia in the harbor seal. Res. Physiol. 19,188 -200.[CrossRef][Medline]
Kooyman, G. L. and Kooyman, T. G. (1995). Diving behavior of emperor penguins nurturing chicks at Coulman Island, Antarctica. Condor 97,536 -549.
Kooyman, G. L. and Ponganis, P. J. (1994).
Emperor penguin oxygen consumption, heart rate and plasma lactate levels
druing graded swimming exercise. J. Exp. Biol.
195,199
-209.
Kooyman, G. L. and Ponganis, P. J. (1998). The physiological basis of diving to depth: birds and mammals. Ann. Rev. Physiol. 60,19 -32.[CrossRef][Medline]
Kooyman, G. L., Schroeder, J. P., Greene, D. G. and Smith, V.
A. (1973). Gas exchange in penguins during simulated dives to
30 and 68 m. Am. J. Physiol.
225,1467
-1471.
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.[Abstract]
LeMaho, Y., Delclitte, P. and Chatonnet, J.
(1976). Thermoregulation in fasting emperor penguins under
natural conditions. Am. J. Physiol.
231,913
-922.
Nagy, K. A., Kooyman, G. L. and Ponganis, P. J. (2001). Energetic cost of foraging in free-diving emperor penguins. Physiol. Biochem. Zool. 74,541 -547.[CrossRef][Medline]
Pinshow, B., Fedak, M. A. and Schmidt-Nielsen, K. (1977). Terrestrial locomotion in penguins: it costs more to waddle. Science 195,592 -594.[Medline]
Pinshow, B., Bernstein, M. H., Lopez, G. E. and Kleinhaus, S. (1982). Regulation of brain temperature in pigeons: effects of corneal convection. Am. J. Physiol. 1982,R577 -R581.
Ponganis, P. J. and Kooyman, G. L. (2000). Diving physiology of birds: a history of studies on polar species. Comp. Biochem. Physiol. A 126,143 -151.
Ponganis, P. J., Kooyman, G. L., Starke, L. N., Kooyman, C. A.
and Kooyman, T. G. (1997). Post-dive blood lactate
concentrations in emperor penguins, Aptenodytes forsteri. J. Exp.
Biol. 200,1623
-1626.
Ponganis, P. J., Kooyman, G. L., Van Dam, R. and Le Maho, Y.
(1999). Physiological responses of king penguins during simulated
diving to 136m depth. J. Exp. Biol.
202,2819
-2822.
Ponganis, P. J., Van Dam, R. P., Marshall, G., Knower, T. and
Levenson, D. H. (2000). Sub-ice foraging behavior of
emperor penguins. J. Exp. Biol.
203,3275
-3278.
Ponganis, P. J., Van Dam, R. P., Knower, T. and Levenson, D. H. (2001). Temperature regulation in emperor penguins foraging under sea ice. Comp. Biochem. Physiol. A 129,811 -820.
Ponganis, P., Kooyman, G. L. and Ridgway, S. H. (2003a). Comparative Diving Physiology. In Physiology and Medicine of Diving (ed. A. O. Brubakk and T. S. Neuman), pp.211 -226. Edinburgh: Saunders.
Ponganis, P. J., Van Dam, R. P., Levenson, D. H., Knower, T., Ponganis, K. V. and Marshall, G. (2003b). Regional heterothermy and conservation of core temperature in emperor penguins diving under sea ice. Comp. Biochem. Physiol. A 135,477 -487.
Powell, F. L. and Hempelman, S. C. (1985). Sources of carbon dioxide in penguin air sacs. Am. J. Physiol. 248,R748 -R752.[Medline]
Powell, F. L., Geiser, J., Gratz, R. K. and Scheid, P. (1981). Airflow in the avian respiratory tract: variations of O2 and CO concentrations in the bronchi of the duck. Res. Physiol. 44,195 -213.[CrossRef][Medline]
Sato, K., Naito, Y., Kato, A., Niizuma, Y., Watanuki, Y.,
Charassin, 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.
Scheid, P. (1979). Mechanisms of gas exchange in bird lungs. Rev. Physiol. Biochem. Pharmacol. 86,137 -186.[Medline]
Scholander, P. F. (1940). Experimental investigations on the respiratory function in diving mammals and birds. Hvalradets skrifter 22,1 -131.
Tamburrini, M., Condo, S. G., di Prisco, G. and Giardina, B. (1994). Adaptation to extreme environments: structure-function relationships in emperor penguin hemoglobin. J. Mol. Biol. 237,615 -621.[CrossRef][Medline]
Torre-Bueno, J. R., Geiser, J. and Scheid, P. (1980). Incomplete gas mixing in the air sacs of the duck. Res. Physiol. 42,109 -122.[CrossRef][Medline]
Van Dam, R. P., Ponganis, P. J., Ponganis, K. V., Levenson, D. H. and Marshall, G. (2002). Stroke frequencies of emperor penguins diving under sea ice. J. Exp. Biol. 205,3769 -3774.[Medline]