Patterns of respiration in diving penguins: is the last gasp an inspired tactic?
1 Institut für Meereskunde, Düsternbrooker Weg 20, D-24105 Kiel,
Germany
2 Depto. de Biología Marina, Universidad Católica del Norte,
Larrondo 1281, Coquimbo, Chile
3 Human and Animal Physiology, Stellenbosch University, Private Bag X1,
Matieland 7602, South Africa
* Author for correspondence
Accepted 24 February 2003
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Summary |
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Key words: respiration, tidal volume, penguin, Spheniscus humboldti, Spheniscus magellanicus, surface interval between dives, breathing
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Introduction |
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Although a great deal is known about the process of gas exchange in diving
marine endotherms (e.g. Butler and Jones,
1997), there are few data that might illuminate the utility of
different gas-exchange strategies on genuinely free-living animals (but see
Le Boeuf et al., 2000
), due to
the logistic difficulties of this type of study. We used a new type of logger
(Wilson et al., 2002
) to
quantify voluntary breathing patterns in captive Humboldt penguins
Spheniscus humboldti and free-living, foraging Magellanic penguins
S. magellanicus, in order to improve our understanding of respiration
during surface intervals between dives. Acquired data were examined using a
simple model to determine the extent to which rates of gas exchange might be
affected and enhanced by observed breath frequency and derived tidal volume
data.
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Materials and methods |
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Measurement of beak angle
Individual penguins were removed from the group and fitted with the
Inter-Mandibular Sensor (IMASEN) (Wilson
et al., 2002). This consisted of a small Hall sensor (0.8
mmx2.5 mm diameter), highly sensitive to magnetic field strength, which
was glued with two-component epoxy resin to the upper beak of the bird close
to the tomium, approximately 30 mm from the rictus. This sensor was linked by
a thin (0.95 mm diameter), teflon-coated cable to a logging unit placed on the
bird's back and held in place by tape, following details given in Wilson et
al. (1997
). Attachment of the
device took approximately 10 min, primarily determined by the drying time of
the glue. The dimensions of the logger were 12.5 cmx2 cm. The logger
itself consisted of electronics potted in resin powered by a lithium 3.6 V
battery (DK Log-IM; Driesen und Kern GmbH, Am Hasselt 25, D-24576 Bad
Bramstedt, Germany). The unit had a memory of 4 Mb and was set to store data
on magnetic field strength (with 16 bit resolution) at a frequency of 5 Hz.
Increasing the distance between the Hall sensor on one beak half and the
magnet on the other beak half (as the beak opened) resulted in a corresponding
decrease in magnetic field strength that was sensed by the Hall device. Thus,
the Hall sensor output was related to the beak angle. The Hall sensor output
was calibrated to allow conversion into beak angle by setting the IMASEN to
record and then allowing the penguin to bite wooden rods of known diameter at
defined positions along the beak. The distance between the articulation and
the point on the beak at which the rod was bitten was measured and the beak
angle calculated via simple trigonometry. The Hall sensor output was
then plotted against beak angle and curve-fitted to derive a general equation
for the relationship between recorded output and beak angle.
Measurement of rates of inspiration and expiration
The rates of air flow in breathing penguins were determined using a
specially constructed blown-plastic mask, fashioned to fit snugly over a
Humboldt penguin head. The joins between bird and mask were sealed with
neoprene. With this arrangement the volume of air in the mask was
approximately 350 ml, although free access to outside air was possible
via a 60 mm long tube of initial i.d. 23 mm. A tiny plastic door (7
mmx5 mm) was located within this tube. This door was joined at its base
to a finely turned stainless steel tube (0.6 mm e.d., 0.3 mm i.d.) pivoted on
a nylon line to allow it to move freely, and hinged about its base. It was
held nominally in the vertical position using the magnetic fields of three
different neodinium boron magnets. One magnet (2 mmx2 mmx1 mm) was
glued to the top of the door with the NorthSouth fields facing parallel
to the main surface of the door perpendicular to the long axis of the
breathing tube. The two other magnets (each 7 mmx1.5 mm diameter) were
placed longitudinally along the floor of the breathing tube, one on each side
of the door, and so orientated that the closest poles to the door were the
same as the adjacent pole on the door-associated magnet. This configuration
held the door in a stable, central position irrespective of the orientation of
the mask, without having to incur the vagaries of mechanical spring systems.
However, air movement resulting from slight pressure differences on one side
of the door caused it to lean to one side, the door position being relative to
the direction and rate of air flow along the tube. The door position was
recorded using a Hall sensor placed next to the door on the outside of the
breathing tube. This sensor was connected to a DK Log-IM logger identical, in
principle, to that used to measure penguin beak angle. Here, door position
resulted in particular magnetic fields being produced in the vicinity of the
sensor. Door position via the Hall sensor output relative to air flow
rate and direction was calibrated by pumping air through the breathing tube
(in the absence of a penguin) at known rates (0.2518 l
min1) in the laboratory (0.05 l min1).
Nine birds were equipped with IMASENs and fitted with the mask for periods of 930 min (some penguins tended to bite the mask and thus proved unsuitable for measuring beak opening solely as a function of breathing see below) while rates of air in- and out-flow were logged with the Hall sensor at a frequency of 5 Hz. IMASENS were also set to record at the same frequency, both devices being perfectly synchronized and double checked for time using external magnets brought into close contact with both Hall sensors simultaneously. The results obtained on the door positions within the mask during breathing were converted into air flow rates using the calibration data (see above). The point at which inspiration or expiration began was clear as a swing in the door position. Flow rates, starting at the beginning of each inspiration or expiration, were summed so as to derive the total amount of air inspired or expired, respectively, representing the tidal volume.
Field work
Field work was conducted on Magellanic penguins Spheniscus
magellanicus Forster between 24 November and 15 December 2000 and between
25 November and 3 December 2001 at Cabo Vírgenes (52°24'S,
68°26'W), Santa Cruz, Argentina, with the approval of the Consejo
Agrario de Santa Cruz. Five individuals brooding chicks were removed from the
nest and equipped with IMASENs, set to record at 10 Hz, as described for the
captive birds. Here, however, the cable linking the logger to the sensor was
secured at two sites on the head (the top of the head and the nape of the
neck) using a spot of epoxy resin enclosing the cable and binding it to the
feathers (Wilson et al.,
2002). In addition, birds were equipped with Lotek LTD 100 loggers
(Lotek Marine Technologies, 114 Cabot Street, St John's, NF, A1C1Z8 Canada).
These units recorded, among other things, depth (12 bit resolution) at 1 s
intervals. The units were 57 mm long and 18 mm diameter, weighed 16 g in air
(1.8 g in seawater) and were attached to the birds by neoprene-backed plastic
leg rings. Birds were left to go on a single foraging trip before the devices
were removed and the data downloaded.
Beak and depth data were treated simultaneously using the software MT-beak (Jensen Software Systems, Laboe, Germany). This software displayed the data on the screen in the form of two graphs against a time axis. The program identified deviations in beak opening events (with a threshold set by the user) and determined the start and end time of the events and maximum values within the defined periods. These values were stored in a separate file together with data on depth.
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Results |
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Air was inhaled just after the beak began its opening movement and continued until just before the beak closed (Fig. 1A). Here, the rate at which air was inhaled was dependent on beak angle, with the best fit being inspiration rate=51.6+139.7ln(beak angle) (r=0.80, F=150.0, P<0.001) (Fig. 2A). Air was expired at the time the beak angle was minimal and there was no relationship between beak angle and the rate at which air was exhaled (Fig. 2B).
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The result of the movements of air meant that the peak in beak angle was offset from the peak corresponding to the moment of maximum volume of air inspired (Fig. 1). However, there was a clear relationship between the tidal volume of any one breath and the maximum beak angle for the beak motion associated with that breath, as well as between the tidal volume of any one breath and the change in beak angle devoted to that breath (here the minimum beak angle is taken as zero) (Fig. 3). This relationship was not the same between individuals (Table 2).
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Field work
All five Magellanic penguins fitted with IMASENs in the wild were recovered
in good health with the units having logged data for the full duration of the
foraging trip. The birds executed 3661707 dives, in total, during which
they fed extensively (cf. Wilson et al.,
2002). All the birds showed remarkably similar patterns of
respiration, although individual differences in absolute beak angles were
apparent (see below).
Two major types of beak movement were apparent when the birds were at the
surface: (i) irregular beak openings and closing, considered to be due to
preening and calling (see Wilson et al.,
2002), which will not be further discussed here, and (ii) a highly
regular series of beak opening and closing cycles
(Fig. 4). In the surface
intervals during normal dive bouts, however, beak angle amplitude changed
systematically; immediately on surfacing beak angle amplitude was high, but
this decreased to a minimum before increasing again to a maximum just before
the bird dived (Fig. 4). This
pattern was apparent irrespective of the number of breaths taken by the birds
during the surface period, although the initial and final beak angle
amplitudes increased with increasing number of breaths taken during the
surface pause (Fig. 5).
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Beak amplitudes during extended pauses at the surface
The U-shaped pattern of maximum beak angle per breath (see Figs
4,
5) was not apparent immediately
prior to dives that occurred after a long pause at the surface, where beak
amplitude per breath increased from a minimum to a maximum before the dive
commenced, nor in surface pauses that followed dives but which were extended
for some minutes or more, where the initial high beak amplitude was apparent
but no second peak occurred. In other words, the initial high values decreased
to a minimum immediately following a dive and appeared to be associated with
recovery from the dive (Fig.
4C), whereas the minimum increasing to a maximum just prior to a
dive appeared to be associated with dive preparation
(Fig. 4B).
Breath cycle time and breath number during the surface pause
Breath cycle time changed systematically over the duration of the surface
interval; cycle times were initially short, increasing to a maximum (that
corresponded to the minimum in beak angle) before decreasing again to a
minimum immediately prior to diving. As a consequence of the systematic
changes in beak angle amplitude and breath cycle time over the surface
interval, there was a clear relationship between breath cycle time and maximum
beak angle for that breath, with higher beak angle amplitudes being associated
with short breath cycle times (Fig.
6, Table 3). In
addition, the effect of the changing breath cycle time with breath number led
to a roughly exponential relationship between the total number of breaths
taken during the surface pause and time
(Fig. 7,
Table 3). Finally, the number
of breaths taken during any surface interval within a dive bout (i.e. this
does not include long periods of rest at the surface cf.
Kooyman, 1989) was positively
correlated with the duration of the preceding dive
(Table 3).
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Discussion |
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Breathing cycle of penguins on land
The anatomy of the avian respiratory system is complex. Birds may breathe
through either the nares or mouth, and have complicated oro-nasal structures
that tend to filter out large particles
(Powell, 2000); the oro-nasal
structures are separated from the trachea by the larynx, which opens into the
trachea through the slit-like glottis
(McLelland, 1989
). The
laryngeal muscles contract during breathing so as to open the glottis during
inspiration and decrease resistance to inspiratory air flow
(Powell, 2000
). The complexity
of the air passages in the upper airways tends to increase the resistance to
air flow through them. The rate of air flow can be approximated by
Poiseuille's equation, whereby the volume of air per unit time
dV/dt is given by:
![]() | (1) |
In order to minimize the energy needed for the act of inspiration, and the
time taken for the air to be inspired, the resistance of air being drawn in
through the beak must therefore also be minimized. This can be presumably
achieved by opening the beak and breathing in through the mouth rather than
the nares. However, the appropriate degree of opening is also dependent on the
energy expended in the opening process (see below for an explanation of why
the beak needs to be opened and closed with each respiratory cycle) and the
extent of the desired tidal volume per unit time; greater flow rates require
wider breathing apertures (see Equation 1 above). This interpretation is at
least loosely supported by our results
(Fig. 2A), although we believe
that it is naive to assume that beak angle might be the sole factor in
determining the width of the respiratory aperture. Inside a penguin's beak is
highly complex, consisting of a large spiny tongue and numerous spiny and
fleshy sections (Zusi, 1975;
Wilson and Duffy, 1986
), so
that the relative position of these features is likely to prove critical in
determining the resistance offered to the air during inspiration, particularly
when the beak angle is small.
During rest, both inspiration and expiration are reported to require active
contraction of the respiratory muscles, and the relaxed resting volume of the
avian respiratory system is midway between the inspiratory and expiratory
volumes (Seifert, 1896). An
increase in ventilatory volume is probably achieved by recruiting more motor
units in active muscles and additional respiratory muscles, both in
inspiration and expiration (e.g. Kadono et
al., 1963
; Fedde et al.,
1964
). Exhalation in little penguins Eudyptula minor does
not involve the abdominal muscles (Boggs et
al., 2001
). This, plus the fact that in penguins the
interclavicular air sac is larger than the posterior air sac and undergoes
greater pressure fluctuations which are coordinated with flipper movements
during swimming, suggests that exhalation may be passive, or at least aided by
swimming movements, in this and other species of penguins. We propose that
when Humboldt penguins are breathing during periods of elevated metabolic
rate, beak closure serves to regulate the flow of air, based on the principles
covered by Poiseuille's equation (Equation 1). Were expiration to be active,
beak closure, by reducing the effective radius of the exhalatory passage,
would necessitate that birds work harder to achieve an appropriate rate of air
flow which, in turn, would require an investment of energy. This is
counter-intuitive, suggesting that exhalation may indeed be passive in this
species. Our observations that penguins in the laboratory invariably exhaled
with the beak minimally open and that the wave form of the beak angle in the
breathing cycle deviated from a true sine wave by having long, low troughs,
may reflect control of the speed of exhalation. Slow ventilation in the little
penguin probably increases the efficiency of oxygen extraction
(Stahel and Nicol, 1988
), and
slowing exhalation may prevent reflex inhibition of ventilation by
intrapulmonary chemoreceptors that are stimulated when airway CO2
levels are reduced, as by rapid air passage
(Furilla and Bernstein, 1995
).
Finally, partial beak closure during exhalation when tidal volumes are high
may also reduce water and heat losses substantially by forcing air to exit
through the nasal turbinates, reclaiming both water and heat that would
otherwise be lost (Geist,
2000
). In herring gulls Larus argentatus, comparison of
respiratory evaporative water loss between birds breathing oropharyngeally and
through the nares has led to estimates of water savings by narial breathing as
high as 71% and heat savings of 5.6%
(Geist, 2000
). The lack of a
relationship between beak angle and expiration rate may be due to the
r4 term in Poiseuille's equation, because when the
respiratory aperture is very small, as was the case during expiration, minute
changes can affect air flow rate substantially. This would further be
compounded by small changes in, for instance, tongue orientation (see
above).
The fact that, in Humboldt penguins at least, beak angle is related to, and probably determines, inspiration rate, and therefore tidal volume, means that respiration can be assessed in free-living birds. It is unfortunate, though not unexpected, that the relationship between tidal volume and beak angle shows such considerable individual variability (Fig. 3, Table 2), necessitating that all free-living penguins to be studied using this methodology need be subject to the mask calibration procedure in order to determine absolute values. Despite this, the linear relationship between beak angle and tidal volume in all individuals studied means that the situation for birds in the wild can at least be modelled using an appropriate equation.
Breathing cycle of penguins at sea
The most obvious difference between the patterns of breathing demonstrated
by the free-living Magellanic penguins and the captive Humboldt penguins was
one of degree. In general, the range of beak angles of the foraging birds was
much higher (cf. Figs 3,
5). In that the change in beak
angles of the Magellanic penguins on land was also very small, it seems likely
that this is due to a difference in metabolic rates (or apparent metabolic
rates, due to gas exchange occurring during the reduced surface interval
corresponding to a relatively long period underwater) rather than some
fundamental difference in bill construction or breathing apparatus between
Magellanic and Humboldt penguins. In fact, the species are congeneric and
remarkably similar in morphology and behaviour
(Williams, 1995) so, although
it would be unwise to use derived values inter-specifically, trends in
measured parameters are likely to be the same.
Can we allude to oxygen acquisition over the surface pause
period?
We have shown that there are a number of relationships between the
parameters measured in the free-living birds (see above) which suggest causal
links between them. In addition, data from captive Humboldt penguins show that
tidal volume can be approximated by examining at maximum beak angle. If we
assume that maximum beak angle in Magellanic penguins is also related to tidal
volume, we can qualitatively examine the tidal volumes in sequential breaths
for the whole of the surface pause in these free-living birds. Furthermore,
the time that each inspiration is allowed to remain within the respiratory
system can be determined for the whole of the surface pause. If this
information is coupled with a few assumptions based on what is known about gas
diffusion rates under defined circumstances, we can even attempt to examine
the rate at which oxygen might be expected to be acquired by the birds over
the surface pause. The steps involved in this are described below.
Firstly, we need to know the maximum beak angle per breath (BAmax) in relation to breath number within the sequence of breaths taken in the surface pause (n) and the total number of breaths taken in the surface pause (Nmax). These values can be taken directly from means derived from the birds (e.g. Fig. 5).
The actual number of sequential breaths (Nmax)
following dives of a particular duration (Dd) can be
predicted from the linear relationship between these two variables
(Table 3), duration being a
proxy for energy expenditure and therefore oxygen debt:
![]() | (2) |
![]() | (3) |
Assuming that the linear relationship between tidal volume
(VT) and maximum beak angle observed in Humboldt penguins
(Table 2) holds good for
Magellanic penguins, so that:
![]() | (4) |
![]() | (5) |
The rate of air passage can also be described by the individual terms
within this form because tidal volume is related to breath cycle time.
Furthermore, if we assume that the oxygen and carbon dioxide levels in the
bird's body at the end of the surface pause always have particular values, as
must be the case during `steady state' diving where dive durations are
relatively constant and the bird does not exceed its aerobic dive limit (cf.
Butler and Woakes, 1984;
Butler and Jones, 1997
), we can
allude to potential rates of oxygen absorption and carbon dioxide elimination
over time.
At any one time, and assuming that blood flow to the lungs is constant, the
rate of oxygen uptake into the body tissues
(bO2) is
dependent on the difference in the partial pressure of oxygen between body
tissues and lungs (Butler and Jones,
1997
) so that:
![]() | (6) |
![]() | (7) |
![]() | (8) |
The overall increase in total oxygen O2,tot within the body, therefore,
over Nmax breaths during a surface pause can be given by:
![]() | (9) |
The pattern of the change in body oxygen incurred, therefore, by a
Magellanic penguin during a surface pause consisting of a particular number of
breaths can be derived by considering the energy expended during the dive and
the amount of oxygen corresponding to this. For example, during normal
swimming at a speed resulting in the lowest cost of transport, Humboldt
penguins expend energy at a rate of 10.8 W kg1
(Luna-Jorquera and Culik,
2000). The respiratory quotient is 0.78 for Humboldt penguins
(Luna-Jorquera and Culik,
2000
) and a conversion factor of 20 J ml1
O2 is appropriate for deriving W kg1
(Eckert, 1993
;
Schmidt-Nielsen, 1993
).
Assuming this to be typical for the genus, a 4 kg Spheniscus penguin
expends approximately 2.2 ml O2 s1 swimming
underwater. Thus, during a typical dive of approximately 74 s, a Magellanic
penguin operating according to the patterns displayed in our results will
expend approximately 163 ml O2 and then take 14 breaths
(Table 3; e.g. bird 5) during a
surface pause of 22 s (Fig. 7)
to pay back this debt (plus the debt incurred for the metabolism at the
surface during this time, which is likely to be of the order of 1.1 ml
s1; Luna-Jorquera and
Culik, 2000
). Reference to mean beak angles associated with each
breath over the pause period and Fig.
7, above, allows calculation of breath cycle times so that tidal
volume and hence the volume of oxygen (V; see Equation 4 above)
inhaled per breath (for convenience we shall ignore the relatively small
amount of oxygen used for metabolic purposes during the surface pause).
Assuming that the oxygen debt of the dive of 163 ml is paid back during the
surface pause, we can present a scenario for the rate of uptake of oxygen
during the surface pause using Equations 8 and 9
(Fig. 8). Note, however, that
if the bird's oxygen deficit following the dive is only that incurred during
the dive (163 ml in our example), this deficit can never be made good in the
time available at the surface, irrespective of the value of the constant k1.
This is due to the perpetually reducing difference in oxygen partial pressures
between lungs and blood. In fact, for the bird to be able to dive and rest in
a steady state, it must always dive with an oxygen deficit
(Fig. 8). Kramer
(1988
) pointed out that this
is a desirable state of affairs in a slightly different context because, in
order to minimize time at the surface and increase foraging efficiency, diving
animals should only submerge with enough oxygen to cover their needs for the
duration of the dive; substantial (non-anaerobic) oxygen debts subsequent to a
dive result in a rapid rate of oxygen uptake. In this general context, greater
oxygen deficits result in faster oxygen uptake rates, which allows birds to
have a highly variable pause duration (cf.
Wanless et al., 1993
) yet
still operate effectively. Shorter pauses result in a greater deficit, which
is automatically and iteratively corrected during the next surface pause due
to the higher rate of transfer of oxygen from the air to the tissues.
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Why is the breathing pattern during the surface pause so shaped?
The breathing pattern apparent during the surface pause, with an initially
high tidal volume and rapid breathing rate followed by a reduction in both
these parameters before rising again until the subsequent dive
(Fig. 5), is not the pattern
that should be observed if the penguin were only trying to maximize rate of
oxygen gain into the tissues. For example, taking the model used to derive
Fig. 8A, to simulate the rate
of oxygen uptake in the tissues during consistently high breathing frequencies
and high tidal volumes (Fig.
8C), the overall rate of oxygen transfer is higher. Apparently,
therefore, penguins could reduce time spent at the surface by deep, fast
breathing. Why do they not do this instead of consistently showing the
characteristic double modality in tidal volumes with reduced ventilation rates
between (Fig. 5)?
In order to explain this we need to invoke another factor, the most likely
candidate being CO2 elimination. If the rate of CO2
elimination is directly proportional to the partial pressure difference
between body CO2 and inspired CO2, in a manner similar
to that postulated for oxygen, there can be no real advantage in the breathing
pattern observed since the amount of CO2 in the body decreases over
the surface pause in a manner approximating to exponential decay
(Fig. 9). However, two things
make this scenario unlikely. Firstly, haemoglobin oxygen saturation is a major
factor affecting the position of the CO2 equilibrium curve (the
Haldane effect) (Scheipers et al.,
1975; Powell,
2000
). The physiological effect of this is to promote
CO2 unloading into the lungs when the blood is oxygenated.
Secondly, the CO2 contained within the body exists in the form of a
bicarbonate ion, or combined with terminal amine groups in haemoglobin or in
solution. Release of CO2 is complicated, being partly catalysed by
carbonic anhydrase (Maren,
1967
), and certainly incurs a greater time lag than does the
release of oxygen. Since CO2 can only be released when the blood is
associated with the lungs, we postulate that at any one time the oxygen
entering blood via the lungs does not induce CO2 release
fast enough for it to enter the lungs immediately, but that the more
oxygenated blood circulates, during which time the processes releasing the
CO2 take place so that this gas is then finally liberated the next
time the unit of blood containing it passes the vicinity of the lungs
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During the course of the surface pause between dives, the breathing
patterns exhibited by Magellanic penguins will tend to lead to initial
log-type, followed by linear, increases in blood oxygen concentrations
(Fig. 8). However, if
CO2 loss is proportional to the degree of oxygenation of the
tissues, high rates of CO2 elimination may only occur after a
substantial amount of the oxygen debt has been repaid. As in the case of
O2 uptake, high tidal volumes coupled with high breathing
frequencies will tend to increase rates of gaseous diffusion so that the
second peak in beak angle, which occurs just before the dive, might be
primarily devoted to elimination of CO2, whose liberation is
facilitated by the previous increment in blood oxygen
(Fig. 9). This possibility is
supported by pre-dive increases in respiratory exchange ratios that were
reported recently for captive freely diving grey seals
(Boutilier et al., 2001),
reflecting elevated end-tidal PCO2 and
supplying evidence for the `flushing out' of CO2 immediately before
dives. These authors emphasised that readjustment of body CO2
stores is slower than that of O2 stores, and may govern inter-dive
intervals. Earlier work on captive Humboldt penguins likewise showed increased
ventilation just before dives (Butler and
Woakes, 1984
).
Note that, in a steady state situation, the bird must balance both O2 and CO2 losses with gains and it would seem, superficially, that only one of these parameters may dictate the length of the surface pause. This may be achieved, in part, as a result of the iterative and automatic balancing of O2 and CO2 according to concentration; the rate of O2 replacement increases with increasing difference between lungs and tissues and CO2 exchange is favoured by high blood O2 levels. Any bird that does not equilibrate its gas levels appropriately during a particular surface pause following a dive is more likely to manage at the next due to the change in body gas concentrations, which affect the subsequent rate of gas exchange accordingly.
Overall, therefore, we reason that diving penguins should attempt to
minimize surface time (Schoener,
1971,
1986
) although the energetic
consequences of so doing should also be considered
(Perry and Pianka, 1997
). With
this as a basis, and since simple replacement of oxygen cannot account for the
patterns we see (Fig. 9), we
propose that carbon dioxide release, operating under particular time- and
blood oxygen saturation-dependent factors, is a major factor in determining
the length and form of penguin inter-dive ventilation behaviour. High
breathing frequencies and tidal volumes, typical of the initial and final
breaths in a surface pause, are presumably coupled with increased energy
expenditure due to the physical process of shunting air around the respiratory
system as defined by Poiseuille's formulation, and will result in an
appreciable quantity of the oxygen gained per unit time having to be used to
operate the respiratory mechanism. In a complete formulation, patterns
observed by us must also incorporate this in the solution so that where high
respiration rates occur, the gain in oxygen (for example at the beginning of
the pause) or loss of carbon dioxide (at the end of the pause) can act to
justify the increase in both oxygen usage and carbon dioxide production that
this respiratory pattern entails. Reduced tidal volumes and respiratory
frequencies, such as occur in the middle of the surface pause, would auger for
the execution of some time-dependent process. However, the increase in the
length of this relatively relaxed period with increasing number of breaths in
any particular surface pause (Figs
5,
6), which appears to be coupled
with initial and final tidal volumes and ultimately with oxygen use during the
dive (Fig. 8), would appear to
be linked to body oxygen and carbon dioxide levels both pre- and post-dive. We
have no information on this and thus, despite a relatively complex analysis,
still cannot equate our observations with the predictions made by Kramer
(1988
). Miniaturization of
appropriate sensors will allow us to resolve this key element in the question
of time optimization in diving endotherms.
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Acknowledgments |
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