Oxygen uptake during post dive recovery in a diving bird Aythya fuligula: implications for optimal foraging models
1 School of Biosciences, University of Birmingham, Edgbaston, Birmingham,
B15 2TT, UK
2 School of Mathematics and Statistics, University of Birmingham, Edgbaston,
Birmingham, B15 2TT, UK
* Author for correspondence (e-mail: lgh013{at}bham.ac.uk)
Accepted 16 September 2002
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Summary |
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Key words: tufted duck, Aythya fuligula, diving, oxygen uptake, optimal foraging, model
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Introduction |
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During foraging bouts, assuming that a diver wants to be under the water
acquiring food for as much time as possible, repeatedly returning to the
surface for oxygen is (generally) in direct competition with food gain
(Ydenberg and Clark, 1989).
Optimal foraging models, which are based on the marginal value theorem
(Charnov, 1976
), have been
developed to determine the optimal surface time for oxygen loading that
maximises the proportion of time spent foraging
(Kramer, 1988
;
Houston and Carbone, 1992
;
Carbone and Houston, 1996
).
These models are based on the physiological gains and losses of oxygen over
the dive cycle and therefore the postdive loading curve is an integral, but as
yet unquantified, part of many theoretical studies of optimal time allocation
(Thompson et al., 1993
;
Carbone and Houston, 1994
,
1996
;
Lea et al., 1996
;
Walton et al., 1998
; Mori,
1998
,
1999
).
Because the mammalian lung system rapidly collapses on immersion
(Kooyman and Ponganis, 1998),
the majority of the oxygen stores of marine mammals consist of haemoglobin and
myoglobin. Thus it is likely that the generic shape for the oxygen loading
curve proposed and used by Kramer
(1988
) in his optimal
breathing model (Fig. 1) may be
correct for most diving mammals. However, Walton et al.
(1998
) have argued that this
shape is not accurate for diving birds.
|
The respiratory system of birds differs from that of mammals and consists
mainly of large distended air sacs and a lung, which is comparatively small
and rigid (Scheid, 1979).
However, the estimated contribution of the air sacs to the total body oxygen
stores of diving birds ranges from 23% to 64%, e.g. tufted duck
(Keijer and Butler, 1982
),
thick-billed murre (Croll et al.,
1992
), lesser scaup
(Stephenson, 1995
),
Adélie penguin (Kooyman and
Ponganis, 1998
), king penguin
(Ponganis et al., 1999
).
Therefore, it has been suggested that the respiratory system will have a
profound influence on the dynamics of post-dive oxygen loading. The oxygen
stored within the air sacs of tufted ducks during a dive is made available for
consumption through locomotion, and associated abdominal activity. This
produces pressure differentials between the posterior and anterior air sacs,
which could reciprocally force the gas stored in the air sacs through the
lungs (Boggs et al., 1998
).
Walton et al. (1998
) suggest
that the gas in the air sacs at the end of a dive is therefore depleted of
oxygen. They argued that, at the start of a surface interval, fresh air must
be taken up into the respiratory tract before oxygen uptake by haemoglobin and
myoglobin can occur, since fresh air must enter the caudal air sacs before any
oxygen becomes available to the lungs.
Consequently, Walton et al.
(1998) predict that avian
divers will produce a `kinked' oxygen uptake curve, with the first phase
representing oxygen taken more rapidly into the air sacs and the second
representing the relatively slower replacement of haemoglobin and myoglobin
stores. In contrast to the smooth curve, this biphasic modification of the
oxygen resaturation curve results in the prediction that all dives shorter
than a certain duration will have identical optimal surface times
(Walton et al., 1998
)
(Fig. 2). In addition, these
dives will also achieve identical levels of oxygen resaturation during the
subsequent surface period (Walton et al.,
1998
).
|
Both the smooth oxygen uptake curves of earlier models as well as the
biphasic curve of Walton et al.
(1998) predict a number of
optimal behavioural patterns. These concern adjustments to surface time and
foraging time in response to changes in dive depth and energetic costs during
the dive. Some qualitative behavioural trends recorded in diving birds are
predicted by optimal time allocation models incorporating the smooth oxygen
replacement curve (Carbone and Houston,
1994
; Carbone et al.,
1996
; Lea et al.,
1996
), while trends reported by Walton et al.
(1998
) are predicted by their
model, which incorporates the biphasic curve. However, it is premature to
affirm the success of any of these models when key assumptions have not been
verified. It is likely that the details of oxygen uptake curves have a
critical effect on the gross predictions of optimal foraging models for divers
(Ruxton et al., 2000
). The
differing predictions of present models reveal the importance of empirical
study on oxygen uptake curves so that further progress can be made in
understanding observed diving behaviour.
The purpose of the present study was to test the hypothesis that the post-dive oxygen gain curve for tufted ducks Aythya fuligula is biphasic. The delineation of the loading curve for voluntarily diving birds was achieved using a fast-response respirometry system, which is able to measure small changes in oxygen concentration over a fairly fine time resolution given a repetitive measurement signal. This enabled the quantification of a critical aspect of optimal foraging models for diving vertebrates and the determination of the extent to which the biphasic adaptation for diving birds is apparent.
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Materials and methods |
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The experimental dive tank was located in a large outdoor aviary close to where the animals were housed. Two large metal fencing panels (1.75x3.45 m) were bolted together perpendicularly and placed in one corner of the dive tank, creating a 1.75x1.75 m cross-section area with a maximum depth of 2.7 m, in which the experiments were conducted. The metal panels stood 0.75 m above the water and, by using smaller fencing panels as a roof and additional side netting, a corral was formed above the water to prevent the birds from escaping.
The birds were trained to dive to a feeding platform (67x82 cm) positioned at a depth of 1.8 m. During the experiments the birds were fed corn and live mealworms. The latter was found to encourage diving behaviour. A false mesh floor was fitted to the bottom of the tank to prevent birds from diving for food that had spilt from the feeding platform. A submersible pool cleaner (Dolphin, Maytronics Ltd) was periodically used to clean fallen food from the floor of the tank. The water temperature varied between 10 and 15°C during the experimental period.
Respirometry experiments
The surface of the tank was covered in netting except for a small area over
which the open base of the small, clear acrylic respirometer chamber
(35x25x25 cm) was positioned and from which the individual birds
dived. The open base of the respirometer was placed 4 cm below the surface of
the water to form an airtight seal along its sides. This made the effective
volume of the respirometer 18 375 ml. The respirometer contained a fan that
ensured thorough mixing of the air within the chamber. A flow of 500 ml
s-1 was drawn through the respirometer by a fixed flow pump,
keeping CO2 below 0.2% at all times. Metabolic gas concentrations
were determined using a zirconia oxygen sensor (Ametek, Thermox Instruments,
model S3A-1/N.22) and an infrared carbon dioxide sensor (ADC Ltd, model
SS-100) connected in series. The sample pump in the CO2 sensor was
used to draw an air sample from an outlet in the respirometer and through the
gas sensors at a constant flow rate of 17 ml s-1. A 500 ml flask
was used just prior to the sample pump to reduce any flow oscillations (see
Fig. 3 for a diagram of the
experimental apparatus). Total flow through the respirometer was 517 ml
s-1. Tubing of 300 ml volume was attached to the holes in the
respirometer open to ambient air. This ensured that when the duck initially
surfaced into the respirometer after a dive, the small volume of air forced
out of the holes did not escape from the system and was subsequently sucked
back into the respirometer.
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All connecting tubing was impermeable to oxygen and was as short and as small bore as possible to reduce dead space. The response time of the oxygen analyser was less than 0.2 s and the lag time of the respirometer box and tubing was 2.5 s. The residual time constant of the system after deconvolution (see later) was 0.4 s and was determined by N2 injections at various points within the respirometer to simulate instantaneous changes in oxygen uptake. The effect of the residual time constant is a slight filtering of the VO2 data, which results in a slight blurring of the cumulative oxygen uptake curves.
The O2 and CO2 analysers were calibrated each day with known gas concentrations produced by a precision gas-mixing pump (Wösthoff Pumps, Bochum). Atmospheric pressure was recorded every hour (Digital Weather Barometer, Prosser Scientific Instruments Ltd, UK) and a relative humidity and temperature probe (Vaisala, Finland) was fixed inside the respirometer to allow airflow through the respirometer to be corrected for water vapour.
A LabVIEW program (National Instruments Corporation, USA) was written to record data on respirometer oxygen concentration during the experimental sessions. A subroutine of the program controlled a reference valve, which sampled ambient oxygen concentration for 10 s every 20 min. This allowed the detection and correction of baseline drift in the measuring system. 300 scans were averaged every 250 ms for humidity, temperature, %O2, %CO2 and reference valve position, and the data were then recorded onto the internal hard drive of the computer running the program (Dell Computers Dimensions XPS P60).
During the experimental sessions, the bird's behaviour was recorded onto video tape to determine time budget data by using a black and white video camera (JVC, model TK-S240) and video recorder (Mitsubishi, model Time Lapse HS-5424E[B]A). An additional small hole in the surface net was replaced with a clear perspex sheet, through which activity at the feeding platform could also be filmed. Two 500 W lamps were attached to the roof of the corral and used to illuminate the feeding platform. A light-emitting diode placed in the field of view of the video camera was turned on at the start of each data recording session. This allowed accurate synchrony between the video footage of behaviour and the respirometer oxygen composition data so that rates of oxygen uptake against time for each surface period could be determined. Preliminary data showed that the ducks first inspired when they were fully surfaced on the water.
Analysis of respirometry data
Percentage oxygen concentration data were converted into rate of oxygen
uptake using a modification of the formula given by Woakes and Butler
(1983), which allows accurate
determination of fast changes in gas concentrations (see Equation 1 below). By
treating the respirometer as both an open and a closed system, oxygen uptake
could be determined for 0.25 s intervals, despite the system having a much
longer response time (36 s). The changes in oxygen concentration in the
respirometer between t1 and t2 were
very small and often within the error of the oxygen analyser, creating a low
ratio of measurement signal against signal noise. However, the noise component
of each measurement was random and therefore equally likely to be negative or
positive. Thus, recording multiple data points for each value of t
allowed signal averaging to recover the measurement signal at each 0.25 s by
reducing the magnitude of the mean noise value
(Bentley, 1983
), i.e. averaging
maintained the root-mean-square (rms) value of the measurement signal while
reducing the rms value of the noise. Because a very large number of data
points (N=870 and 878) were collected and averaged, the
signal-to-noise ratio was greatly increased. A change of 1 ml O2 in
the respirometer could then be measured with an error of approximately
±0.03 ml:
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Oxygen data for the last 1 s surface interval were removed so that any
elevated pre-dive
O2 was not
included in the analysis (Butler and
Woakes, 1979
; Woakes and
Butler, 1983
). For analysis of oxygen uptake data, values are
means ± S.E.M. for four animals. To avoid animal bias, mean values were
obtained for each bird and these means were used to obtain the final mean. A
significant difference between means was tested with paired
t-tests.
Statistics for biphasic determination
Bout criterion interval analysis
(Slater and Lester, 1982) was
used to eliminate all (inter-bout) dives with a surface time greater than 35
s. Preliminary data suggested that longer dives had a more pronounced effect
on the oxygen loading dynamics, possibly due to the amount of oxygen used
while submerged, and so the dive data were split into two groups for analysis.
Dives were split at 16.0 s, which gave two dive duration bins, `short' and
`long', with N-values as equal as possible (short, dive duration
<16.0 s, N=870; long, dive duration
16.0 s, N=878).
The mean VO2 data were smoothed by taking a
running three-point average and then log-transformed to linearise the
exponentially decreasing oxygen uptake data. `Broken stick' analysis was then
performed to see if the biphasic regression line was statistically a better
fit than a linear one (Seber,
1977
). To construct a biphasic regression line, the logged mean
oxygen uptake data were split at a selected data point. A linear regression
line was then fitted to the data, which corresponded from the start of the
surface time up to and including the chosen break point. Similarly, another
linear regression line was fitted just after the chosen break point to the
remainder of the data. The uptake data during the surface recovery had
therefore been split into two phases around a chosen data point. The linear
equations for each of these phases allowed the intersecting point of
inflection, C, to be calculated (see Equation 5) and an overall
biphasic regression equation to be determined (see Equations 6, 7).
An illustration of this technique can be seen in Fig. 4. For this worked example the break point in the data was arbitrarily chosen at 6 s. Regression analysis was conducted on the data up to and including this break point (Linear phase 1) and again on all remaining data points (Linear phase 2). The point of intersection for these two regression lines also represents the point of inflection, C, of the biphasic regression line. Equation 5 can therefore be used with parameters determined by the linear regression analysis to calculate this point of inflection. A generalised regression equation for a biphasic line can then be produced using Equations 6 and 7. It is at this point that the `broken stick' analysis is conducted to see if the biphasic regression line is statistically a better description of the data than a linear regression line (Fig. 4B).
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Locating inflection points for biphasic regression
Least-squares regression was performed on the uptake data with the break
point at 6 s post dive, as given in the example
(Fig. 4). An iterative sequence
of least-squares regression with the chosen break point decreasing by 0.25 s
every execution was then completed. The biphasic regression line that had a
break point with the lowest residual variance, and so represented the best
description of the data, was used as the biphasic regression solution to the
uptake data.
For the biphasic regression, both phases of the broken stick model were calculated by linear regression and so can be defined as follows:
Linear phase 1 (before the break):
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![]() | (3) |
![]() | (4) |
![]() | (5) |
![]() | (6) |
![]() | (7) |
To test the significance of the biphasic regression equation, least-squares
regression was performed using both the biphasic construct and simple linear
regression. An F-test was then performed on the residual mean sum of
squares for both equations to determine statistically whether the biphasic
regression was a significant improvement. Degrees of freedom (d.f.) for linear
regression is N-1 whereas d.f. for biphasic uptake is N-4 as
a1, a2, b1 and
C have been calculated to define the biphasic equation. Other
methodologies are available to determine whether biphasic relationships exist
within the data. These are more complex as they allow for a smoother
transition between the two phases of the biphasic construct
(Koops and Grossman,
1993).
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Results |
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Oxygen uptake
The mean rate of oxygen uptake
(O2) for all
dives, over the first 15 s, was 1.14±0.33 ml s-1. However,
the rate of oxygen uptake was not constant
(Fig. 5). The
VO2 data for all dives show that upon surfacing
there was a more rapid phase of oxygen uptake for approximately the first 3 s,
during which
O2
was 2.45±0.09 ml s-1.
|
O2 was
significantly higher for the first 3 s of surface time after both short and
long dives (short dives, 2.22±0.13 ml s-1; long dives,
2.67±0.12 ml s-1) than for the rest of the surface period,
up to 15 s (short dives, 0.72±0.28 ml s-1,
P<0.001; long dives, 0.82±0.37 ml s-1,
P<0.001).
O2 significantly
differed between short and long dives during the first 3 s
(P<0.01) but did not significantly differ between short and long
dives for the rest of the surface period up to 15 s.
After long dives, the mean total oxygen uptake during the first 15 s of the surface interval (17.9 ml) was significantly higher than that after short dives (15.3 ml, P<0.001; Fig. 6). Statistical comparison of the mean uptake curves for the two dive duration bins was achieved by testing for a significant difference between the cumulative oxygen values of the curves at 5 s, 10 s and 15 s. The values at 5 s, 10 s and 15 s were significantly higher in the oxygen uptake curve associated with longer duration dives than in the shorter ones (Table 2).
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Biphasic analysis
The break points with the lowest residual variance used to calculate the
biphasic regression lines were 5.00 s for short dives and 3.00 s for long
dives (Fig. 7). Using these
values in Equations 1, 2 and 5 gave the point of inflection for biphasic
oxygen uptake, C, as 3.3 s for short dives and 3.3 s for long dives.
Least-squares regression analysis was performed using both linear and biphasic
equations on log transformed smoothed mean VO2
data for both long (Fig. 7) and
short dives.
|
All linear and biphasic regression lines used were highly significant (Table 3). F-tests were then used on the residual mean sum of squares for the linear and the biphasic regression lines to see whether the biphasic constructs were a significantly better description of the data. Biphasic regression was not significantly better for short dives (C=3.34, F56,53=1.45, not significant). For long dives, the biphasic regression was a significantly better fit for the data than linear regression (C=3.28, F56.53=1.96, P<0.01). Thus, oxygen uptake is only biphasic for long duration dives, with the point of inflection at 3.3 s (Fig. 8). Due to the effect of the residual time constant on the cumulative oxygen uptake curves, the points of inflection may be slightly inaccurate. Nevertheless, the true point of inflection for both these curves is very close to 3.3 s.
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Discussion |
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The rate of oxygen uptake
O2 changes over
time at the surface after both long and short dives. In both cases,
O2 is higher at
the start of the surface period and decreases against time. This relationship
is not linear, as shown by the oxygen uptake curves for long and short dives
in Fig. 5. Rather, both curves
can be seen to consist of far higher
O2 for
approximately the first 3 s of surface time.
The shape of the oxygen uptake curve changes with the duration of the dive
(Figs 5,
6) and oxygen was taken up
significantly faster during surface periods associated with longer dive
durations. This suggests that, as dive duration increases, and presumably
total oxygen consumed during the dive (VO2d)
increases, initial surface
O2 increases.
While
O2 from 3
s to 15 s was not significantly different between the two conditions, it was
significantly higher after longer dives during the first 3 s. Whether this is
due partly to an increase in effort by the birds to take up oxygen more
quickly, or is purely a passive phenomenon dependent upon the difference in
partial pressure of oxygen inside and outside the cardio-respiratory system,
is not clear. Higher
O2 for the first
3 s after longer dives, coupled with a
O2 beyond 3 s
that does not vary with dive duration, creates a sharper `kink' in the oxygen
uptake curve after longer dives.
Implications for optimal foraging models
The kink in the oxygen uptake curve produced by the ducks for long dive
durations was sufficiently pronounced to make the measured curve statistically
biphasic, while the uptake curve for short dive durations was not. This
indicates that the break in the curve becomes more prominent during surface
periods when the dive duration was longer and
VO2 was higher. So, for tufted ducks, dives of
a relatively short duration are followed by surface periods where rates of
oxygen uptake produce a curve similar to that predicted by Kramer
(1988). Longer dive durations
produce oxygen uptake curves with a clearer biphasic element and so become
more like the curve predicted by Walton et al.
(1998
).
According to the predictions of Walton et al.
(1998), a range of dives up to
a certain duration will be associated with very similar surface durations
because the tangent from travel time tT will be `locked'
to the kink of the curve. However, the mean surface duration for long duration
dives is more than fourfold greater than the surface duration at which the
kink often occurs (15.4 s versus approx. 3.3 s). For tufted ducks,
therefore, the volume of oxygen consumed during the dive may be high enough
that the tangent routinely touches the curve beyond the kink
(Houston, 2000
). Shorter
dives, where less oxygen is consumed, produce smoother oxygen uptake curves
and so there is not such a pronounced kink to intercept the tangent. Extended
dives by tufted ducks, although utilising very high volumes of oxygen, might
possibly produce oxygen uptake curves with such an acute kink that the tangent
still touches it. However, although occasional dives of over 40 s have been
reported in tufted ducks (Stephenson et
al., 1986
), Table 4
indicates that the vast majority of dives by this species are unlikely to be
long enough to cause such a large change to the post-dive oxygen reloading
dynamics. Furthermore, field studies suggest that dives are normally fairly
short, for example Magnusdottir and Einarsson
(1990
) recorded a mean dive
time for tufted ducks diving on Lake M
vatn of 18.3 s.
Respiratory frequency during periods of oxygen uptake
Walton et al. (1998) may
have made an incorrect assumption that oxygen must be taken up into the caudal
air sacs before it is then made available for gaseous exchange. In fact, on
inspiration, a significant proportion of air directly enters the paleopulmonic
parabronchi via the main bronchus
(Bretz and Schmidt-Nielsen,
1971
; Butler et al.,
1988
; Powell,
2000
). Indeed, Powell
(2000
) suggests that when the
tidal volume is large, some inspired gases reach as far as the cranial air
sacs, via the paleopulmonic parabronchi, during the same breath. In
this case, birds would not exhibit a biphasic oxygen uptake curve for the
reasons stated by Walton et al.
(1998
), since fresh air would
reach the lungs on the first inspiration. Nevertheless, tufted ducks do
demonstrate biphasic oxygen uptake after relatively long dives and so there
must be an alternative explanation for this kinked curve.
O2 not only
decreases against surface duration but shows a cyclical aspect that is not
attenuated when the data are smoothed after long duration dives
(Fig. 9). This cyclical aspect
is not as clear after short duration dives. After long duration dives, the
peaks in VO2 data reflect a drop in
respirometer oxygen concentration and presumably correspond to exhalation by
the bird. Similarly, the drop in
O2 would
therefore correspond to inspiration. If this is so, then the first post-dive
exhalation occurs about 0.5 s after surfacing.
|
Butler and Woakes (1979)
studied the respiratory patterns of diving pochards (Aythya ferina)
before and after feeding dives using implanted tracheal thermistors. They
reported that the respiratory frequency decreased from 54.5 breaths
min-1., 1 s after surfacing to 42.7 breaths min-1 after
5 s and longer. If the respirometry system used in the present study was able
to detect individual breaths, the rates of post-dive ventilation for the
pochard are comparable to those from the present study. There is clearly a
change in respiratory frequency after the third exhalation, according to
Fig. 9. The first three
expiration markers cover approx. 2.5 respiratory cycles in 2.25 s, implying a
respiratory frequency of 66.7 breaths min-1. The next five markers
cover approx. 4.75 cycles in 8.75 s, a respiratory frequency of 32.5 breaths
min-1. The biphasic inflection point, at 3.3 s, occurs in between
the third and fourth expirations. Thus, the biphasic nature of oxygen uptake
following longer dives may be explained by a fairly sudden slowing of
ventilation rate after the first three exhalations. This agrees with reports
of other diving vertebrate species reloading their oxygen stores and removing
carbon dioxide after dives (Butler and
Jones, 1997
). However, not all air-breathing divers exhibit the
same respiratory patterns as avian species. Weddell seals show a steady
decline in minute volume (volume of air inhaled per minute) during the first 5
min post-dive, and beyond this point the decline decays to a constant
(Kooyman et al., 1971
).
A hypothesis borne from the assumptions on avian anatomy by Walton et al.
(1998) is that the break point
of the oxygen uptake curve would occur just after the second post-surface
expiration, since this would be the first opportunity for the inspired gases
to diffuse into the blood and tissues through the paleopulmonic parabronchi.
The biphasic point of inflection is at 3.3 s for long duration dives, whereas
the second exhalation occurs at 1.5 s (Fig.
9). This is further evidence that the biphasic uptake that occurs
during longer dives in the tufted duck is probably associated with a change in
respiratory frequency, rather than as a consequence of the anatomy of its
respiratory system.
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Acknowledgments |
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References |
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