Do seasonal changes in metabolic rate facilitate changes in diving behaviour?
1 School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15
2TT, UK
2 Sea Mammal Research Unit, Gatty Marine Laboratory, University of St
Andrews, St Andrews, Fife KY16 8LB, UK
3 British Antarctic Survey, High Cross, Madingley Road, Cambridge CB3 0ET,
UK
* Author for correspondence (e-mail: j.a.green{at}bham.ac.uk)
Accepted 10 May 2005
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Summary |
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Rates of oxygen consumption were estimated from fH. As
winter progressed, the rate of oxygen consumption during dive cycles
(sO2DC) declined
significantly and mirrored the pattern of increase in maximum duration and
depth. The decline in
s
O2DC was
matched by a decline in minimum rate of oxygen consumption
(s
O2min). When
s
O2min was
subtracted from
s
O2DC, the net
cost of diving was unchanged between summer and winter. We suggest that the
increased diving capacity demonstrated during the winter was facilitated by
the decrease in
s
O2min.
Abdominal temperature declined during winter but this was not sufficient to
explain the decline in
sO2min. A simple
model of the interactions between
s
O2min, thermal
conductance and water temperature shows how a change in the distribution of
fat stores and therefore a change in insulation and/or a difference in
foraging location during winter could account for the observed reduction in
s
O2min and hence
s
O2DC.
Key words: macaroni penguin, Eudyptes chrysolophus, diving, seasonal change, oxygen consumption, thermoregulation, cADL
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Introduction |
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Green et al. (in press a)
showed that the foraging and diving behaviour of macaroni penguins
[Eudyptes chrysolophus (Brandt 1837)] varies substantially throughout
their annual cycle. Specifically, during the winter months, the penguins tend
to dive to greater depths and for greater durations than during the summer.
However, in an earlier study of their diving energetics, Green et al.
(2003
) showed that female
macaroni penguins may dive close to the limits of aerobic metabolism during
the summer months. Calculated aerobic dive limit (cADL) is a quantity often
used to assess the energetic cost of dives
(Butler and Jones, 1997
). cADL
is the time at which an animal is estimated to have exhausted its usable
oxygen stores while submerged, and is calculated from the total usable oxygen
stores divided by a measure of the rate of oxygen consumption
(
O2) while
submerged. In macaroni penguins, during the summer, cADL was estimated to be
138 s, and 95.3% of all dives were less than this threshold
(Green et al., 2003
). However,
during the middle of winter, mean dive duration of foraging dives by
female penguins was approximately 143 s
(Green et al., in press a
).
This suggests either that the previous estimate of cADL was incorrect or that,
during the winter months, the penguins were either subject to considerable
ecological constraints that forced them to dive beyond their aerobic limits or
else their physiological capability to dive increased.
In the present study, we compare diving behaviour and energetics during the summer/pre-moult foraging trip and winter/migratory period of macaroni penguins in order to determine what might cause the observed changes in diving behaviour. Specifically, we ask: (1) when do the observed large-scale seasonal changes in diving behaviour occur; (2) is variation in diving behaviour caused by variation in the energetic cost of diving, or vice versa; and (3) what physiological and/or ecological factors might cause variation in the behaviour and energetics of diving?
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Materials and methods |
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Deployment of DLs took place during the austral summers of 2001/02 and
2002/03, and retrieval of DLs took place during the austral summers of 2002/03
and 2003/04. Study birds were identified and captured using the procedures
described by Green et al.
(2004), and DLs were
surgically implanted into the abdominal cavity using previously established
techniques (Stephenson et al.,
1986
; Green et al.,
2003
). Long-term implantation of these DLs has previously been
shown to have no detectable adverse effects on the behaviour, breeding success
and survival of this species (Green et
al., 2004
). In 2001/02, DLs were deployed during the chick rearing
phase in January and February (N=39). In 2002/03, DLs were implanted
during the incubation phase in November (N=19), chick rearing period
in January and February (N=12) and moult phase in March
(N=12). DLs were retrieved in the breeding season following
implantation. In the 2002/03 breeding season, 34 of 39 penguins with DLs
returned after the winter. In the 2003/04 breeding season, 43 of 43 penguins
with DLs returned after the winter. In both years, return rates were not
significantly different to control groups or previous data for this colony
(Green et al., 2004
). In both
seasons, DLs that had failed during the winter migration were removed during
the courtship phase, while DLs which had not failed during the winter were
removed during the following moult phase. DLs were removed using the same
procedures as during implantation and, after recovery, the penguins resumed
their normal activities.
Data loggers
The DLs used in the present study were designed by one of the authors
(A.J.W.) and were the same instruments (Mk 3a, Mk 3b) used to study year-round
diving behaviour of macaroni penguins
(Green et al., in press a). Mk
3a instruments were used for all deployments during the 2001/02 season. Mk 3a
instruments were also used for 13 of the deployments in the 2002/03 season,
with Mk 3b used for the remainder. Both instruments had dimensions of 36
x28 x11 mm and weighed 18 g before and 21 g after encapsulation in
paraffin wax to provide waterproofing and a silicone coating for
biocompatibility. Both instruments could record hydrostatic pressure for
conversion to dive depth, heart rate (fH), body attitude
(upright or prone) and abdominal temperature (Tab). Mk 3a
DLs had a 32 Mb memory capacity and were programmed to record dive depth every
2 s, fH and body attitude every 10 s and
Tab every 30 s for 453 days. Mk 3b DLs had a larger memory
capacity (64 Mb) and were programmed to record dive depth every 1 s,
fH and body attitude every 10 s and
Tab every 15 s for 542 days. Mk 3a DLs had a depth
resolution of approximately 0.3 m, while a technical problem with the Mk 3b
DLs meant that, although they had a depth resolution of approximately 0.09 m,
they failed to record further depth changes deeper than approximately 25 m
(Green et al., in press a
).
All DLs were individually calibrated and had a temperature resolution of
approximately 0.06°C. The time that each logger was started, implanted,
removed and stopped was carefully noted as GMT. After retrieval, data from all
DLs were downloaded onto a computer before being transferred to a UNIX
workstation or PC for further analysis.
Dive analysis
While evaluating dive records, dives with maximum depths of <2.4 m were
ignored during analyses since, between the surface and this depth, wave
action, recorder noise and the interaction between temperature and pressure
degraded depth accuracy making it impossible to accurately characterise dives
this shallow. No distinction was made between foraging and non-foraging
(travelling or searching) dives, and hence all dives with maximum depth of
x2.4 m were used in all analyses. In total, 1 616 403 dives were
analysed and, for each dive, maximum depth, dive duration and subsequent
surface duration were extracted.
Data analysis
Data were prepared and analysed using purpose-written computer programs
within the SAS statistical package (version 8.2; SAS Institute, Cary, NC,
USA). As in previous work (Green et al.,
in press a), careful observation of the breeding behaviour of the
individual penguins and preliminary analysis of the depth and body attitude
data allowed each day of the deployment for each penguin to be assigned to a
phase of the annual cycle and a day since the start of that phase for that
bird (phaseday). These phases were: (1) incubation trip, (2) brood, (3)
crèche, (4) pre-moult trip, (5) fail (foraging behaviour during the
breeding season following the failure of a breeding attempt), (6) winter. In
the current project, only data from the pre-moult trip (N=54 birds)
and winter (N=46 birds) phases were used for analysis and are
referred to as summer and winter, respectively. The data were further filtered
to reduce variability. The duration of the pre-moult trip varied slightly
between individuals, so only the first 16 days of the pre-moult trip were
used, as this was the minimum duration of this phase in all birds. For winter,
the first 13 days of winter were removed as, until this time, some birds still
returned to the colony regularly and had not engaged in their full migration,
despite the completion of moult. The duration of the winter phase was limited
to 190 days, as this was the minimum duration of this phase. For analyses
involving dive depth, only data from the 2001/02 season were used
(N=31 for summer, N=26 for winter).
The body mass (Mb) of both male and female macaroni
penguins fluctuates during the breeding season, by a factor of up to two
(Croxall, 1984).
Mb at the end of winter is substantially greater than at
the beginning (Croxall, 1984
)
but, other than this, Mb is unknown during the winter
period. To understand the relative changes in metabolism, it is beneficial to
calculate the rate of oxygen consumption
(
O2),
independently of the potentially confounding effects of fluctuating
Mb and body size. In recent years, there has been much
attention on the correct way to account for the effects of
Mb in physiological investigations (e.g.
Packard and Boardman, 1999
).
Unusually, in macaroni penguins, the mass exponent of
O2 is one,
whereas there is no relationship between heart rate (fH)
and Mb (Green et al.,
2001
; J. A. Green, C. R. White and P. J. Butler, unpublished
data). We found that using mass-specific
O2
(s
O2) accounts
for all of the variation between individuals in
O2 at a given
fH in this species and allows the construction of
predictive relationships between fH and
s
O2
(Green et al., 2001
).
Therefore, in the current study, the use of mass-independent
s
O2 not only
accounts for variation in body size and mass between individuals but also
allows us to account for the confounding effects of variable body mass within
individuals at different times of year.
s
O2 (in ml
min-1 kg-1) was estimated from fH
using the equations of Green et al.
(2005
), and the standard error
of the estimate (S.E.E.) was calculated following the method of
Green et al. (2001
).
In an effort to evaluate potential changes in minimum or maintenance
metabolic rate (MMR), a running average of
sO2 was computed
for each 12-min period throughout each day. The period with the minimum value
was assigned as the basal rate of oxygen consumption for that day
(s
O2min). Twelve
minutes was selected as the interval to evaluate
s
O2min, as it
was the inflection point in a plot of running average size against minimum
fH (Withers,
2001
). In an effort to correct for the possible effects of
anapyrexia (a regulated decrease in body temperature) on MMR,
s
O2min was
normalised to a temperature of 39°C
(s
O2minC).
s
O2minC was
calculated according to van't Hoff principles, assuming an apparent
Q10 of 3 (Heldmaier and Ruf,
1992
).
Mean abdominal temperature was calculated for each day. To gain a better
understanding of the many physiological processes leading to changes in body
temperature, a running average of Tab was calculated every
12 min for each day for each penguin. The minimum and maximum value for each
day for each animal were then extracted (Tab,min and
Tab,max, respectively). Tab,max was
used to represent the normal, core body temperature as it was independent of
the effects of circulatory changes, regional hypothermia or metabolic
suppression associated with diving
(Ponganis et al., 2003;
Butler, 2004
). These factors
can conspire together to reduce Tab, and the magnitude and
duration of this decrease are dependent on the duration of diving bouts
(Green et al., 2003
).
sO2 while
submerged cannot be measured during dives
(Costa, 1988
), but
s
O2DC, the
s
O2 of a
complete dive cycle (dive plus the subsequent surface period), can be
estimated from mean fH of that dive cycle
(Fedak, 1986
;
Bevan and Butler, 1992
;
Butler, 1993
). Calculated
aerobic dive limit (cADL) is usually calculated by dividing useable oxygen
stores by an estimate of
O2 while
submerged (Butler and Jones,
1997
). Green et al.
(2003
) used
s
O2DC as a
measure and indicator of
O2 while
submerged and showed that cADL is not necessarily a fixed quantity. In
macaroni penguins, cADL increased with increasing dive duration, because
s
O2DC decreased
with increasing dive duration. As a result of this, in the present study, cADL
was calculated, at each observed dive duration, and cADL described in the text
is the threshold at which dive duration exceeded the cADL calculated at that
dive duration. cADL was calculated using oxygen stores of 58 ml
kg-1, as in a previous study
(Green et al., 2003
). 95%
confidence intervals of cADL were calculated by repeating this process but
substituting
s
O2DC with the
upper and lower 95% confidence intervals of
s
O2DC at each
dive duration.
Estimates of
sO2 are quoted
in the text ± S.E.E., and comparisons of these data were
made using Woolf's test for differences, which is most appropriate for the
analysis of data derived from a predictive relationship (R. L. Holder,
personal communication). All other data were analysed using general linear
model (GLM), and means are quoted as ± S.E.M. Results were
considered significant at P<0.05, and the significance of
statistical tests is quoted in the text.
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Results |
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To investigate these differences in more detail, mean and maximum dive duration and depth were derived for each bird for the summer (276 641 dives) and for the middle of the two stable periods during mid- and late-winter (phasedays 6985, 121 681 dives; phasedays 149165, 113 174 dives, respectively). These periods are illustrated in Fig. 1. There was no difference between the sexes in mean and maximum dive duration and depth. Mean dive duration was significantly different between each of these periods (GLM with Tukey post-hoc tests; F2,113=95.1, P<0.0001; Table 1). Mean maximum dive duration was also significantly different between each of these periods (GLM with Tukey post-hoc tests; F2,113=154.7, P<0.0001; Table 1). Mean dive depth was significantly greater during mid-winter than during summer and late-winter (GLM with Tukey post-hoc tests; F2,113=12.5, P<0.0001; Table 1). Mean maximum dive depth was not significantly different between mid- and late-winter, but both were significantly greater than mean maximum dive depth during summer (GLM with Tukey post-hoc tests; F2,113=13.8, P<0.0001; Table 1).
|
Abdominal temperature and metabolic rate
There was some variation between individuals in the pattern of change of
daily abdominal temperature (Tab,D), but
Fig. 3A shows the mean for all
animals. In female penguins, Tab,D decreased by
approximately 1°C during early winter from the summer level then remained
at this level for the rest of the winter. In male penguins,
Tab,D declined by approximately 0.8°C at the beginning
of winter from the mean summer level but later increased to approximately the
same as during summer. Changes in minimum abdominal temperature
(Tab,min) also varied between individuals but a general
pattern was identified (Fig.
3B). In both male and female penguins, Tab,min
was variable during winter but was up to 2°C higher than during summer.
Significant changes in maximum abdominal temperature
(Tab,max) were far more consistent between individuals.
Tab,max declined steadily over the first 100 days of
winter to a level around 1.5°C lower than that during summer.
Tab,max then remained at this level for the rest of the
winter in female penguins but increased slightly, while remaining below summer
levels, in male penguins (Fig.
3C). GLM was used to further investigate the changes in
temperature (Tab,D, Tab,min or
Tab,max) for summer, mid-winter and late-winter as
described above. In each analysis, temperature (Tab,D,
Tab,min or Tab,max) was the dependent
variable, with sex and season as factors
(Table 2). Mean
Tab,D was significantly greater in males than females but
not significantly different between the seasons. Mean
Tab,min was not significantly different between the
seasons or sexes. Mean Tab,max was significantly greater
in males than females and was significantly lower during mid-winter and
late-winter than during the summer.
|
|
Minimum sO2
showed an inverse pattern to that of diving behaviour
(Fig. 4A).
s
O2min was lower
during winter than summer. During winter,
s
O2min decreased
initially until approximately day 50 and then remained relatively constant at
around 50% of the summer value until the end of winter. Normalising
s
O2min for the
effects of body temperature had little effect on this pattern
(Fig. 4B). Mean
s
O2min during
summer was significantly greater than
s
O2min during
mid-winter (days 6985) whether normalised or not (Woolf's test for
differences; Table 3). The
magnitude of the decrease in
s
O2min from
summer to winter only changed from 51% to 49% with normalisation.
|
|
Energetic cost of diving
Changes in maximum dive duration and depth as winter progressed were
mirrored by changes in the energetic cost of diving. For any given dive
duration, mean
sO2DC decreased
as winter progressed, whereas during summer,
s
O2DC was
unchanged (Fig. 5). At the
start of winter,
s
O2DC was
slightly less than that during the summer and decreased over the first part of
the winter migration before reaching a stable level after approximately 50
days. This stable level was then maintained for most of the winter before
increasing slightly at the end. As with mean dive duration, mean
s
O2DC was
derived for each bird for the summer and for mid- and late-winter (phasedays
6985 and phasedays 149165, respectively) at three ranges of dive
duration (4150 s, 91100 s,141150 s). With the exception
of 141150 s dives in females,
s
O2DC was
significantly different among these periods at each range of dive duration in
both sexes (Woolf's test for differences;
Table 4). Post-hoc
Z-tests with Bonferroni corrections showed that, where there was a
significant difference,
s
O2DC was the
same during both winter periods but both of these were significantly lower
than s
O2DC
during summer.
|
|
The net cost of diving above MMR or maintenance metabolism
(sO2net) was
estimated by subtracting mean
s
O2min from mean
s
O2DC for each
day (Fig. 6).
s
O2net was
derived for each bird for the summer and for mid- and late-winter (phasedays
6985 and phasedays 149165, respectively) at three ranges of dive
duration (4150 s, 91100 s, 141150 s). With the exception
of 141150 s dives in females,
s
O2net was not
significantly different among these periods at each range of dive duration in
both sexes (Woolf's test for differences;
Table 4). Post-hoc
Z-tests with Bonferroni corrections showed that in dives of 141150
s duration in females,
s
O2net was the
same during both winter periods but both of these were significantly higher
than s
O2DC
during summer.
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Discussion |
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Changes in diving behaviour
In both sexes, diving behaviour during the pre-moult trip was relatively
consistent, with little change in mean and maximum dive duration and depth.
During the winter migration, however, the picture was rather different and two
distinct stable phases can be identified. At the start of winter, both mean
and maximum dive durations and depth were greater than those during the summer
and proceeded to increase further until around day 50. These higher levels
were maintained until around day 100. During this mid-winter period, mean and
maximum depth and duration were significantly greater than those during the
summer. There then followed a period of change where mean depth, mean duration
and maximum duration decreased to other lower stable levels. During this
late-winter stable period, maximum depth was unchanged but mean depth and mean
and maximum duration were significantly lower. Indeed, mean depth was equal to
that during summer.
The driving force behind these changes in behaviour is unclear but is
likely to depend on the distribution of prey species with respect to depth.
Antarctic krill (Euphausia superba) is the dominant species in the
zooplankton assemblage of the Southern Ocean
(Everson, 2000). Macaroni
penguins feed predominantly on Antarctic krill, at least in the summer
(Croxall et al., 1997
), but in
decreasing amounts in recent years (Barlow
et al., 2002
). Antarctic krill vary annually, seasonally,
diurnally and geographically in their location in the water column
(Godlewska, 1996
) but usually
undertake diurnal vertical migration; spending the night close to the surface
and the day at deeper depths. Despite this, during the day, krill will nearly
always be located within the diving depth range of macaroni penguins. The mean
depth of the krill varies substantially between locations in the Atlantic
sector of the Southern Ocean, Scotia Sea and waters around South Georgia
(Everson, 1984
;
Godlewska, 1996
). The mean
depth in a review of studies varied from 28 to 156 m and the amplitude of
migration from 2.5 to 59 m, depending on the timing and location of the
studies. Indeed, some data suggest that close to South Georgia, pressure from
predatory fish feeding on the shelf bottom causes diurnal vertical migration
to be reversed, with krill found relatively close to the surface (around 50 m)
during the day and dispersed throughout the water column at night
(Everson, 1984
).
There is little information on the foraging location of macaroni penguins,
especially during winter. During the chick rearing season, the penguins
undertake short foraging trips and remain close to South Georgia over the
continental shelf (Barlow and Croxall,
2002). During the longer incubation foraging trip, the penguins
range further afield to far deeper waters in the Polar Frontal Zone
(Barlow and Croxall, 2002
). The
incubation foraging trip is of a similar duration and for a similar purpose
(rapidly to replenish or increase body reserves) to the pre-moult foraging
trip, so it seems reasonable to assume for the time being that the penguins
forage in a similar location. The location of macaroni penguins during the
winter is currently unknown. However, it seems likely that during the winter
they migrate to the open ocean away from the vicinity of South Georgia. A
difference in the depth of krill swarms in the open ocean is therefore a
likely explanation for the difference in mean diving depth between summer and
winter. Figs 1 and
2 suggest that there was a
further change in the mean depth of the krill from mid- to late-winter, due
either to a difference in the location of the penguins or to the behaviour of
the krill. In late-winter, mean depth, mean duration and maximum duration
declined while maximum depth did not change. The decrease in maximum duration
was only slight (6.5%; Table 1)
and there were no changes at this time in the physiological parameters
measured (Figs 3,
4,
5,
6), implying that the diving
capacity of the penguins did not change. As a result, they were able to dive
more comfortably within their limits. This is reflected in an increase in the
proportion of dives within the cADL between mid-winter and late-winter
(significantly so in male penguins), despite no significant change in the cADL
(Fig. 7).
Energetic cost of diving
The increases in mean and maximum dive depth and duration from summer to
winter, and the continued progressive increases through the first part of
winter, were inversely matched precisely by changes in the energetic cost of
diving. As mean and maximum dive duration increased, mean
sO2DC for a
given dive duration decreased (Fig.
5). It appears therefore that increased dive duration and depth
were facilitated by a decrease in the energetic cost of diving. A progressive
improvement in diving ability due to a reduction in energetic costs has not
previously been observed in a mature diving animal. Juvenile diving animals
commonly show an improvement in their ability to dive during development
(Burns, 1999
;
Ponganis et al., 1999
;
Noren et al., 2001
). Other
studies have shown that oxygen stores can vary seasonally in adult animals
(MacArthur, 1990
) but that any
apparent advantage of this is cancelled out by an increase in
O2 while diving
(MacArthur et al., 2000
).
Increased oxygen availability during diving was induced in tufted ducks
(Aythya fuligula) by training them to dive for longer
(Stephenson et al., 1989
).
However, a similar increase induced by training in muskrats (Ondatra
zibethicus) was again cancelled out by an increase in
O2 during diving
(MacArthur et al., 2003
). In
the current study, we do not know how, or even whether, oxygen stores varied.
However, the proportion of dives in excess of the cADL did not vary between
summer and mid-winter (Fig.
7),suggesting that whether or not the estimate of oxygen stores we
used is accurate, it did not vary. The penguins must have been under pressure
to dive deeper and for longer during winter, and apparently this increase was
accommodated solely by the decreased energetic cost of diving. This decrease
must be achievable only in the time scale and under the conditions experienced
in winter, or else the penguins would modify their energetic costs in the same
way during the summer and we would see more dives within the cADL at this
time.
Although seasonal variation in
sO2 while diving
has not been demonstrated previously, some authors have speculated on its
existence (Bennett et al.,
2001
). In the current study, we show that, in macaroni penguins,
variation in s
O2
while diving is due almost entirely to variation in
s
O2min. It is
not possible to measure basal metabolic rate (BMR) in an active animal, but
s
O2min provides
an approximation of the maintenance requirements of the penguins while at sea,
excluding diving behaviour.
s
O2min showed a
pattern of change which matched that of
s
O2DC
(Fig. 4) and there are good
linear relationships between mean daily
s
O2min and
s
O2DC
(r2=0.73 and 0.83 for dives of 100 s duration in females
and males, respectively). It seems clear that the decrease in
s
O2DC and
increase in diving capacity are facilitated by this drop in minimum or basal
metabolic rate.
Seasonal change in basal metabolic rate
Seasonal variation in BMR has been demonstrated in many species. Among
diving animals, captive female grey seals
(Boily, 1996;
Boily and Lavigne, 1997
),
harbour seals (Phoca vitulina) and harp seals (Phoca
groenlandica; Renouf and Gales,
1994
) show a marked underlying seasonal variability in resting
metabolic rate, although the pattern of this variability varies between
species.
The maintenance of a high core body temperature in endotherms carries a
high metabolic cost (Bennett and Ruben,
1979). In water, which has a thermal conductance 25 x
greater than air, these metabolic costs are likely to be even higher, even for
an animal as well adapted to an aquatic lifestyle as a penguin. In several
species of penguins, resting
O2 is
approximately twice as high when they are in relatively cold water than when
they are in air (Stahel and Nicol,
1982
; Culik et al.,
1991
; Bevan et al.,
1995
). Other studies have shown that penguins have no
thermoneutral zone in water, and metabolic rate increases with decreasing
water temperature (Stahel and Nicol,
1982
; Barré and Roussel,
1986
). In little penguins (Eudyptula minor), this trend
occurs until a critical temperature, beyond which metabolic rate increases
sharply (Stahel and Nicol,
1982
).
Resting sO2
during summer of macaroni penguins in water at 6.8°C, recorded using
respirometry, was 27.0 and 24.5 ml O2 min-1
kg-1 for females and males, respectively
(Green et al., 2005
). These
values are similar to
s
O2min during
summer in the present study. However, by mid-winter,
s
O2min was
closer to values obtained from the same penguins while resting in air (10.7
and 9.7 ml O2 min-1 kg-1 for females and
males, respectively; Green et al.,
2005
). In fasted king penguins (Aptenodytes patagonicus),
resting
O2 in
water was approximately 2 x that in air. However, in well-fed penguins,
resting
O2 in
water was substantially lower and was the same as resting
O2 in air
(Fahlman et al., in press
). It
is suggested by these authors that a complex interaction between nutritional
state, vasoconstriction, fat deposition and fat mobilisation causes a decrease
in thermal conductance (the inverse of insulation) of around 25% and therefore
a substantial reduction in metabolic rate.
Thermoregulation
Perhaps macaroni penguins are also able to reduce the cost of
thermoregulation during the winter. Thermoregulatory costs can be reduced by
either decreasing the temperature gradient (by reducing body temperature or
increasing external temperature) or by decreasing the rate of heat transfer or
thermal conductance. Temporarily decreasing core temperature (anapyrexia)
while inactive on a daily or seasonal basis is used by some endotherms to
conserve energy when the temperature is very low and/or food is scarce
(Nedergard and Cannon, 1990).
Even in a period of high activity, barnacle geese (Branta leucopsis)
were found to save considerable amounts of energy for their spring migration
through having a reduced Tab
(Butler and Woakes, 2001
).
However, in the present study, mean Tab,D did not change
from the summer to winter (Table
2) and the modest decline in Tab,max (a proxy
for body temperature) of approximately 1.5°C
(Table 2) was not nearly
sufficient to explain the decrease in
s
O2min
(Fig. 4). Perhaps more likely
is that, by migrating northwards, macaroni penguins are able to forage in
warmer waters during winter than they are during the summer. Factors
controlling the sea surface temperature (SST) are beyond the scope of this
article but, as an example, at the longitude of Bird Island (approx. 38°
W) during July, SST increases by approximately 0.92°C for each degree of
latitude travelled north from 53° S (the latitude of Bird Island) to
38° S and beyond.
Thermal conductance has been studied several times in penguins (summarised
in Luna-Jorquera et al.,
1997), although frequently in air rather than water. Thermal
conductance was lower in air than water in little penguins
(Stahel and Nicol, 1982
). In
water, erection of feathers is not possible as they must form a waterproof
layer. This will trap less air, reduce the effective plumage depth, and hence
the contribution to insulation will decrease. When the penguins dive, even
more air will be removed from the plumage and the remaining air will be
compressed, both of which will further increase conductance
(De Vries and Van Eerden,
1995
). It is estimated that penguin plumage comprises 7387%
of total insulation in air (Le Maho et
al., 1976
; Stahel and Nicol,
1982
; Barré,
1984
), but this declines to 8 and 10% while fully immersed in
water for macaroni and king penguins, respectively
(Barré and Roussel,
1986
), with internal insulation accounting for the remainder.
Internal insulation will therefore play a major role in thermoregulation while
the macaroni penguins are engaged in long foraging trips at sea. During the
winter, it may be supposed that the body condition of the penguins is better
than that during the pre-moult period, as the penguins are less constrained in
diet, foraging area and behaviour. This may enable them to have a more
efficient and evenly distributed insulative fat layer than during the summer.
In other animal models, the abdominal fat is the first resource to become
exhausted during fasting and the first restored during re-feeding, while
subcutaneous tissues are the last to be restored
(Blem, 1990
). Fasting,
re-feeding and the large variation observed in body mass during the breeding
season in macaroni penguins (Croxall,
1984
) may be the result of changes in abdominal fat stores, while
during the winter the more insulative subcutaneous tissues are restored.
Furthermore, although the insulative contribution of the feather layer
decreases, its insulative effect is bound to be greater during the winter when
the feathers are new, rather than immediately before the moult when they will
be worn and undoubtedly less effective.
|
Modelling thermal conductance in this way assumes that animals are passive
bodies, and studies have shown that such an assumption can oversimplify the
complexity of changes in conductance in animals
(Hind and Gurney, 1997).
Furthermore, heat generated during locomotion may be used in thermoregulation,
while movement itself will alter conductance
(De Vries and Van Eerden,
1995
; Hind and Gurney,
1997
). However, penguins do not dive to forage at night
(Wilson et al., 1993
;
Green et al., in press a
) and
therefore at this time probably remain inactive at the water surface. Indeed,
in the present study,
s
O2min was
nearly always recorded during the hours of darkness. Therefore, while changes
in conductance are unlikely to provide the full explanation for the decrease
in MMR during winter, Fig. 8
suggests that this will be an important component. This simple model shows us
that small increases in insulation, particularly internal insulation, and/or
water temperature can have a large effect on the reduction of metabolic rate.
The progressive decrease in
s
O2min at the
start of winter and the increase towards the end of winter could be explained
by the penguins moving from cooler to warmer waters and vice versa or
a progressive improvement in body condition and insulation. In great
cormorants (Phalacrocorax carbo carbo), water temperature, body
temperature and body fat thickness were found to be major contributors to
diving energetics (Grémillet et
al., 1998
). Further work on the winter location, body condition
and mass of penguins will assist us in assessing the relative contribution of
the effect of a change in thermal conductance and/or
T in
macaroni penguins.
List of symbols
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Acknowledgments |
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References |
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