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First published online July 20, 2007
Journal of Experimental Biology 210, 2723-2729 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.005009
Ventilation patterns in red kangaroos (Macropus rufus Desmarest): juveniles work harder than adults at thermal extremes, but extract more oxygen per breath at thermoneutrality
1 School of Biological Science, University of New South Wales, Sydney, NSW,
2052, Australia
2 Physiology: School of Biomedical, Biomolecular and Chemical Science,
University of Western Australia, Perth, Western Australia
* Author for correspondence (e-mail: a.munn{at}unswalumni.com)
Accepted 16 May 2007
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Summary |
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Key words: allometry, kangaroo, marsupials, juveniles, thermoregulation, ventilation
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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). The survival of juvenile red kangaroos in this environment
is problematic and significant population recruitment occurs mainly after
periods of high or extended rainfall. Such events provide juvenile kangaroos
with access to the high-quality forage needed for their long-term growth and
survival (Munn et al., 2006;
Munn and Dawson, 2006).
However, in addition to their requirement for high-quality forage, which
occurs over a relatively long physiological time-scale (i.e. weeks to months),
juvenile red kangaroos must be able to cope with the more immediate challenges
of their environment. These challenges include high radiant heat loads, daily
thermal extremes and scarce free water
(Dawson, 1995).
The red kangaroos' reproductive strategy affords their offspring some
protection from environmental extremes in the form of maternal care while the
young develop inside the pouch, but only during the early stages of
development. By 190 days old (d) and weighing around 2 kg, the young is fully
furred and will venture out of the pouch for short periods. At this
`in–out' stage, the young kangaroo is still unable to maintain deep body
temperature (Tb) for long periods, regularly returning to
the pouch for warmth and safety (Frith and
Sharman, 1964; Dawson,
1995). By 230–250 d, thermoregulation is well developed
(Munn and Dawson, 2001) and
the young kangaroo permanently leaves the pouch, becoming a young-at-foot
(YAF; mass 4–5 kg). YAF red kangaroos forage in association with their
mothers but also continue to take milk by putting their head into the pouch to
access the same teat used during pouch-life. It is not for another 100 days or
so that the YAF is fully weaned, at around 360 d and weighing 10–11 kg
(Frith and Sharman, 1964;
Dawson, 1995). Once young
kangaroos have permanently left the mother's pouch they face the same
environmental challenges as adults, but their smaller body size and
high-energy requirements for growth (Munn
and Dawson, 2001; Munn and
Dawson, 2003) potentially impact on their ability to meet such
thermal challenges.
Munn and Dawson showed that the energy and water requirements of YAF red
kangaroos differ from those of adults
(Munn and Dawson, 2001;
Munn and Dawson, 2003). For
example, at thermoneutral ambient temperatures (Ta) around
25°C, YAF red kangaroos had absolute rates of oxygen consumption (ml
min–1) that were 58% that of mature, non-lactating females,
despite being only 30% of maternal body mass. To maintain heat balance at cold
Tas, at –5°C, the absolute oxygen consumption
(ml min–1) of YAFs increased to 68% that of mature females
(Munn and Dawson, 2001). In
addition, YAF also had high water requirements at high Ta
(
45°C), where juvenile kangaroos evaporated 2.5-times more water per
unit body mass than mature females. These high evaporative water losses were
achieved largely through elevated rates of respiratory evaporative cooling
(i.e. panting) (Munn and Dawson,
2001). There is clearly a requirement for a larger relative
capacity of the ventilatory system of the juvenile kangaroo compared to the
adult. Therefore, we here explore the ventilatory physiology of juvenile red
kangaroos by asking whether their ventilatory characteristics are similar to
those of adults.
To evaluate the capabilities of the juvenile kangaroo ventilatory system,
relative to adults, we used an allometric approach
(Schmidt-Nielsen, 1984). That
is, we compared the juvenile and adult red kangaroos' ventilation/respiratory
patterns (including oxygen consumption) using the relevant body-mass exponents
predicted from quarter-power scaling (West
et al., 2000). The body mass (m) exponents that we used
for oxygen consumption (ml min–1; m0.75),
respiration rate (breaths min–1;
m–0.25), tidal volume (ml;
m1.0), ventilation rate (ml min–1;
m0.75) and oxygen extraction (%; m0.0)
are supported empirically from studies on both eutherians
(Stahl, 1967) and marsupials
(Dawson and Needham, 1981;
Frappell and Baudinette, 1995;
Withers et al., 2006). Because
there is some controversy about exponent values for various parameters
(Dodds et al., 2001;
Kozlowski and Konarzewski,
2004; West and Brown,
2005; White and Seymor,
2005), we also present results using an alternative exponent of
0.67 for oxygen consumption and ventilation. We therefore compared
allometrically adjusted data for the ventilation/respiration characteristics
of juvenile and adult kangaroos at thermoneutral (25°C) and extreme
Tas of –5°C and 45°C.
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Materials and methods |
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;
Sharman et al., 1964;
Munn and Dawson, 2003). Food
was withheld for 24 h prior to experimentation. During the major part of this
study the juvenile red kangaroos were at an average age of 313±5 d,
with a mass of 8.6±0.3 kg (mean ± s.e.m.).
Experimental procedure
For metabolic and ventilatory measurements, kangaroos were weighed to the
nearest 0.1 kg (Salter Scales, Sydney, Australia) and placed in an
open-circuit metabolism chamber (69.5x45x58 cm) within a
temperature-controlled room. Ta was regulated to
±0.5°C of a set point and each animal was tested at
Tas of –5°, 25° and 45°C.
Ta was measured (±0.1°C) using a thermocouple
placed in the excurrent port of the chamber. The metabolism chamber had a mesh
floor above a bath of vegetable oil to trap excreta. The walls of the
metabolism chamber were painted flat black to reduce radiation reflection
(Porter, 1969;
Maloney and Dawson, 1994).
Experiments were performed between 08.00 and 16.00 h, corresponding to the
resting phase of adult red kangaroo circadian rhythm
(Watson and Dawson, 1993).
Animals were monitored throughout each experiment via a low-light CCD
camera (Oatley Electronics, Sydney, Australia) mounted inside the chamber.
After an animal was sealed into the chamber, at least 3 h was allowed for
equilibration at any given temperature; data collection then commenced when
the animal's body temperature had stabilised. Flow rate (FR) of dry air into
the metabolism chamber was measured upstream using a Hastings Mass flowmeter
(model HFM-201; John Morris Scientific, Sydney, Australia). Flow rate was
adjusted to prevent water vapour pressure inside the chamber from exceeding 15
mmHg (1 mmHg=133.3 Pa). A sub-sample of air (125 ml min–1)
was drawn from the excurrent port using a flow controller (Ametek Applied
Electrochemistry R2 flow controller; Pittsburgh, PA, USA) and passed through a
capacitance type relative humidity (%RH) sensor (±0.1%)
(CHK-Engineering, Sydney, Australia), which was calibrated regularly using
saturated solutions of lithium chloride, sodium chloride and magnesium
chloride (Winston and Bates,
1960). After leaving the humidity sensor, the excurrent air was
dried with drierite, scrubbed of CO2 with ascarite and re-dried
before passing through an oxygen analyser (Ametek Applied Electrochemistry
S3A-III).
Sensor outputs (FR, %RH, %O2) were logged on a personal computer
at 5 s intervals using Warthog Labhelper software (Warthog Systems, University
of California, Riverside, CA, USA) running a 12-bit analog/digital (A/D)
converter (National Instruments Lab-NB card, North Ryde, NSW, Australia). This
system averaged approximately 120 readings for each recorded value and gave a
maximum resolution of 0.006% for %O2. The whole system was
calibrated regularly using the iron-burn method
(Young et al., 1984). Oxygen
consumption (
O2)
(ml min–1) was calculated as described in detail elsewhere
(Munn and Dawson, 2001). At
least 20 min of continuous minimal
O2 during an
exposure was used to determine the mean metabolic rate at each
Ta.
The metabolism chamber acted as a whole-body plethysmograph, which allowed
measurement of respiratory frequency (fR; breaths
min–1) and tidal volume (VT; ml)
(Malan, 1973;
Maloney and Dawson, 1994).
Described in detail by Maloney and Dawson
(Maloney and Dawson, 1994),
plethysmography measures changes in the chamber air pressure caused by the
humidification and warming/cooling of chamber air during inspiration. Chamber
pressure was measured with a pressure transducer (PT-100; Sable Systems
International, Las Vegas, NV, USA) and logged on a personal computer
via an analog/digital converter. Data were logged at 0.05 s intervals
at –5 and 25°C and at 0.03 s intervals at 45°C. The system was
calibrated by injecting 115 ml of air into the chamber at the end of each
experiment. Calibrations were repeated until the injection deflections were
stable and matched the deflection kinetics exhibited by the respiring animal
(Maloney and Dawson,
1994).
Data analysis
Tidal volume was estimated using equation 6 from Malan
(Malan, 1973), assuming lung
temperature was equal to Tb:
 | (1) |
PT=change in chamber pressure with animal
inspiration (volts); PK=change in chamber pressure
with calibration injection (volts); P=chamber pressure (mmHg);
Pa,H2O=chamber water vapour pressure (mmHg);
PTb=lung vapour pressure at
Tb; and Ta and Tb
are in degrees Kelvin. Vapour pressures were calculated from steam tables
(Weast and Astle, 1982) using
chamber relative humidity and assuming air in the lungs was saturated at
Tb. Chamber pressure was estimated from barometric
pressure corrected for chamber pressure relative to ambient air measured with
a manometer connected to the chamber.
For each animal, VT was established as the mean of five
sets of respiratory traces taken throughout the 20-min period for minimal
O2 at each
Ta. VT and respiratory minute volume
(ventilation rate,
I=VTxfR)
was measured at body temperature and pressure, saturated, but converted to
standard temperature and pressure, dry, for analysis.
Oxygen extraction (EO2), or the percentage
of inspired oxygen ultimately used by the animal, was calculated as:
 | (2) |
Data for juveniles were compared directly to that for adult red kangaroos
obtained previously (Dawson et al.,
2000a) (N=7). Mean mass of the adults was 23.5±1.1
kg.
Statistical analysis
The effect of temperature on ventilation in the YAF red kangaroos was
assessed by comparing responses at Tas of –5°C,
25°C and 45°C using one-way repeated-measures ANOVA. Assumptions for
ANOVA were tested by Levene's test for variances and Kolmogorov–Smirnov
test for normality. To account for heterogeneity of variances in YAF,
fR, I
and EO2, these data sets were log10
transformed (Zar, 1999).
Allometrically adjusted data for the YAF and adult red kangaroos were compared
at –5°, 25° and 45°C using a two-way repeated measures
ANOVA. Assumptions for ANOVA were tested by Levene's test for variances and
Kolmogorov–Smirnov test for normality. To account for heterogeneity of
variances in the YAF versus adult fR,
I (for data using body-mass
exponents of 0.67 or 0.75) and EO2, these data
sets were log10 transformed
(Zar, 1999). When ANOVA
yielded significant differences, a Student–Newman–Keuls (SNK) test
was performed to compare individual means. All statistical analyses were
performed using Statistica 4.1 for Macintosh (Statsoft, Tulsa) and results are
presented as means ± s.e.m.
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Results |
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O2 was 2.6 times
higher than it was under thermoneutral conditions at Ta
25°C (P<0.05, N=7;
Table 1). The YAF accommodated
their higher O2
at Ta –5°C by taking significantly deeper
breaths (i.e. higher VT) and more of them (i.e. higher
fR), leading to a 2.1 times higher
I than at
Ta 25°C (P<0.05, N=7;
Table 1). The high
O2 was also
accommodated by a slight, though non-significant, rise in
EO2 of around 4.3% units (P=0.2;
Table 1).
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At 45°C, the YAF kangaroos were unable to maintain their
Tb at the levels exhibited under thermoneutrality.
Although stable, the YAF Tb at Ta
45°C was significantly higher than that at Ta
25°C, being 38.3±0.2°C (P<0.05, N=7;
Table 1). At
Ta 45°C, the YAF panted heavily, with respiratory
rates 30 times higher than at Ta 25°C
(Table 1). This was accompanied
by significant reductions in VT. There was also a
significant reduction in EO2 to around 1.5% at
Ta 45°C, compared with 21% at Ta
25°C (P<0.05; Table
1). Notably, I
in the YAF at Ta 45°C was 20 times that seen at
thermoneutral Tas of 25°C (P<0.05;
Table 1).
YAF versus adult red kangaroos
Using the exponents predicted from quarter-power scaling
(West et al., 2000), we
compared the YAF's ventilatory characteristics directly with those obtained
from adult red kangaroos (Dawson et al.,
2000a). The YAF red kangaroos showed respiratory responses to
Tas of –5°, 25° and 45°C that were
similar to those of mature females (Fig.
1) but at all Tas the YAF
O2 (ml
min–1 kg–0.75) was around 1.6 times that of
the mature females (P<0.05;
Fig. 1A). At a thermoneutral
Ta of 25°C, we found no significant difference between
the YAF and adult red kangaroos' allometrically adjusted
fR (breaths min–1 kg0.25;
Fig. 1B),
VT (ml kg–1;
Fig. 1C) or
I (ml
min–1 kg–0.75;
Fig. 1D), although differences
were apparent at thermal extremes. The higher oxygen use by juveniles at
25°C compared to adults was accommodated by higher
EO2 (%), being 21.4±1.8% compared to
16.6±1.9% in the adults (P<0.05;
Fig. 1E).
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O2
(Fig. 1A) and
I
(Fig. 1D) by around 1.5 and 2.2
times, respectively, from thermoneutral levels. The YAF
I at Ta
–5°C was significantly higher than that of the mature females by a
factor of 1.5 (Fig. 1D). This
was associated with the YAF's VT being 35% greater at
Ta –5°C than it was at Ta
25°C (P<0.01), and it was also 40% higher than that of the
mature females (P<0.05; Fig.
1C). Furthermore, the mature females did not significantly
increase VT at Ta –5°C
compared with that at Ta 25°C
(Fig. 1; P>0.05).
Notably, the YAF and adult red kangaroos showed distinctly higher
fRs at Ta –5°C compared with
those seen at Ta 25°C, by between 7.4 and 4.5 breaths
min–1 kg0.25, respectively, and these differences
showed a strong tendency for significance (P=0.06) in each case (see
Fig. 1B).
At high Tas of around 45°C, well above the
Tb of juvenile and adult red kangaroos, the
I of YAF was over 20 times
higher than at thermoneutral conditions and was over 1.9 times that of the
mature females on an allometrically adjusted basis
(Fig. 1D). There was no
significant difference between the VT of the YAF and the
mature female kangaroos at 45°C (Fig.
1C). Therefore, the higher rate of
I exhibited by the YAF at
Ta 45°C compared with mature females
(Fig. 1D) was due solely to the
YAF's higher fR (Fig.
1B), which exceeded 320 breaths min–1 on average
(Table 1), compared with 150
breaths min–1 for the mature females.
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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) found that the resting metabolic rate (ml O2
min–1 kg–0.75) of YAF red kangaroos was
around 1.5 times that of fully mature, non-reproductive females, indicating
that juvenile red kangaroos have intrinsically higher rates of energy
turnover. We have re-iterated that finding here, placing our study of their
ventilation patterns within the appropriate context. Juvenile mammals
generally have higher basal metabolic rates than adults, due mainly to the
extra energy turnover associated with growth
(Robbins, 1993;
Munn and Dawson, 2003). Here,
we have shown that the YAF's higher
O2 was not
accommodated simply through higher fR or even a higher
overall I but was
accommodated by a higher level of oxygen being extracted from each breath
(i.e. a higher EO2;
Fig. 1E). It is generally
assumed that EO2 is a fairly constant fraction
of I across adult animals
from different mammal groups, but we have shown that
EO2 can vary with animal age. This is
reminiscent of the conclusion of Chappell et al.
(Chappell et al., 2003) that
EO2 decreased with age in deer mice. Chappell's
results (Chappell et al., 2003)
were most likely due to senescence, but the higher
EO2s reported here for the very young animal
deserves further investigation. Differences in
EO2 can arise from either changes in
ventilation/perfusion matching or differences in the oxygen content of mixed
venous blood because arterial blood is nearly 100% saturated under
non-pathological conditions (Bartels,
1971; Withers,
1992). Thus, an increased EO2
reflects either improved ventilation/perfusion matching or increased
O2 unloading from haemoglobin in tissues. Whichever the reason, it
points to differences in the handling of oxygen with age in these large
macropods.
Our red kangaroos showed typical mammalian responses to the higher
O2 demands imposed by cold Tas
(Fig. 1A). Both the YAF and
mature females increased
O2 by around
2-fold at Ta –5°C compared with that at
Ta 25°C. In both age groups, the higher
O2 at
Ta –5°C was met largely by increases in
I. In the adult animals, a
significant increase in EO2 also contributed
(Fig. 1E), which is a typical
mammalian response to cold exposure
(Mortola and Frappell, 2000).
That the YAF's EO2 did not increase at
Ta –5°C relative to that seen at
Ta 25°C, as was the case for the adults, suggests that
they may be operating near their maximum level of extraction even under
standard conditions. Therefore, unlike adult kangaroos, the YAF would appear
to have little reserve capacity in their EO2
potential to ameliorate the extreme cold
(Fig. 1E), and their higher
O2 at
Ta –5°C was met solely through increased
I
(Table 1). Notably, we were
unable to push our juveniles (or adults) to the limits of their abilities, as
indicated by the maintenance of constant Tbs at all
Tas; further research is required to determine their
maximum levels of EO2 at even lower
Tas or in response to exercise. Nonetheless, the higher
I of the YAF at a
Ta of –5°C, compared with that at
Ta 25°C, was accomplished by an increase in
VT, while VT of the adults remained
unchanged between thermoneutral and cold Tas. Therefore,
the juvenile kangaroos' ventilation system needed to work harder than that of
adults at Ta –5°C in order to maintain
Tb. Arid-zone kangaroos routinely face such cold
conditions, particularly in winter when Ta regularly falls
below freezing at night
(http://www.bom.gov.au/climate/averages/
– date viewed 01/12/2006).
In addition to managing homeostasis during cold conditions, free-ranging
red kangaroos often encounter particularly hot conditions. During summer
months, for example, the average incident radiation across much of the red
kangaroo's range exceeds 1000 W m–2
(Dawson, 1995), and they
experience average daily Tas of 30 to >45°C
(http://www.bom.gov.au/climate/averages/
– date viewed 01/12/2006). Munn and Dawson
(Munn and Dawson, 2001) and
Dawson et al. (Dawson et al.,
2000a; Dawson et al.,
2000b) found that both YAF and mature female red kangaroos,
respectively, showed typical mammalian responses to high
Tas of 45°C. These principally included increases
in evaporative cooling through both cutaneous (i.e. licking) and respiratory
(i.e. panting) routes. Notably, panting was the major source of evaporative
cooling under hot conditions for the adult red kangaroos, accounting for
60% of total evaporative heat loss
(Dawson et al., 2000b). Mature
kangaroos do not sweat in response to thermal heat loads (although they do in
response to exercise) (Dawson et al.,
1974), and so the remaining portion of their evaporative heat loss
at Ta 45°C can be attributed to insensible cutaneous
evaporation and licking of the body surface, especially the forearms
(Needham et al., 1974;
Dawson et al., 2000b).
Conversely, the YAF red kangaroos relied equally on cutaneous and respiratory
evaporative cooling to maintain Tb at
Ta 45°C (Munn and
Dawson, 2001). We do not know if the YAF were sweating. Sweating
in adult kangaroos occurs only during exercise, when Tb
increases markedly. But if there is a threshold Tb above
which sweating is initiated in resting kangaroos, then perhaps the YAF reached
that Tb while the adults did not. Juvenile
Tb reached 38.3°C while adults reached only 36.8°C
at Tas around 45°C (see
Munn and Dawson, 2001). By
weaning age, when they had increased to a body mass of around 11–12 kg,
the juveniles became more reliant on respiratory evaporative cooling at high
Tas (Munn and Dawson,
2001), suggesting that the smaller YAF kangaroos' ventilatory
system alone was not sufficient to support the higher rates evaporation
required to maintain Tb, thereby necessitating the higher
levels of cutaneous evaporation observed. The data presented here support this
conclusion, and at a Ta of 45°C, well in excess of
Tb, there were indications that the YAFs' ventilatory
system was working harder than that of adults. In particular, at
Ta 45°C, the YAF red kangaroos showed one of the
highest fRs that we are aware of for any mammal, once body
mass was taken into account. On an allometric basis, the fastest previously
recorded fRs were 189 breaths min–1
kg0.25 for an exercising 2 g Etruscan shrew (Suncus
etruscus) (Jürgens et al.,
1996) and 253 breaths min–1 kg0.25 for
the masked shrew (Sorex cinereus)
(Morrison et al., 1959) (but
see Jürgens et al.,
1996). These values are less than half our measured
fR of 560 breaths min–1 kg0.25
(i.e. 323 breaths min–1;
Table 1) for the heat-stressed
YAF red kangaroos at an average body mass of 9 kg.
A note on allometry
In this study we have focussed on scaling exponents empirically derived for
adult mammals (Stahl, 1967;
Dawson and Needham, 1981;
Frappell and Baudinette, 1995;
Withers et al., 2006) and that
are consistent with quarter-power scaling
(West et al., 2000). However,
we recognise that there is considerable controversy about the appropriate
scaling exponent for metabolic rate in mammals (e.g.
Dodds et al., 2001;
Kozlowski and Konarzewski,
2004; West and Brown,
2005; White and Seymor,
2005). For example, a body-mass exponent of 0.67 has been
suggested as more appropriate for both intra- and inter-specific comparisons
(Heusner, 1991; White and Seymour,
2003). Choosing an appropriate exponent is further complicated
when juvenile animals are considered
(Wieser, 1984), but our
objective was to examine whether juveniles were small adults in terms of
ventilatory physiology (Munn and Dawson,
2001). We therefore chose an exponent of 0.75 for comparisons of
O2 and
I, which is consistent with
adult data (Stahl, 1967;
Dawson and Needham, 1981;
Frappell and Baudinette, 1995;
Withers et al., 2006). Our
results, however, were consistent both in pattern and implication when we
compared O2s and
Is of the YAF and adult
kangaroos using a body-mass exponent of 0.67 rather than 0.75
(Table 2). Specifically, using
a scaling exponent for body mass of 0.67, we found that the YAFs' resting
O2 (at
Ta 25°C) was still 1.4 times that of adult animals
(P<0.01; Table 2).
We are unaware of alternative scaling exponents for VT,
fR or EO2, but regardless
of which body-mass exponent is used for
O2 and
I, the theoretical and
measured body-mass exponent for EO2 should
remain constant at zero. In other words, regardless of the choice of exponent,
our conclusion that the juvenile kangaroos meet higher resting oxygen
consumptions by extracting more oxygen per breath is supported. Moreover, even
with the more conservative body-mass exponent of 0.67, the YAF kangaroos had
significantly higher
O2s and
Is compared with those of
adults at Ta –5°C and 45°C
(Table 2).
|
Conclusions
There are two primary conclusions that can be drawn from this study.
Firstly, in terms of their fR, VT and
I, the ventilatory system
of juvenile red kangaroos at thermoneutral Tas was not
significantly different from that expected for an adult marsupial of similar
body mass. However, the YAF did have a higher
EO2 (%) at Ta 25°C,
compared with adults, which explains how they meet their comparatively higher
O2 demands at this Ta. How this may be involved
with active growth, which is usually cited as the main reason for juveniles
having higher
O2s, relative to
adults (Robbins, 1993), is
unknown. The second conclusion from this study is that, in the face of thermal
extremes, the juvenile kangaroo ventilatory system must work considerably
harder than that of adult animals to maintain heat balance. Overall, juvenile
kangaroos appear more sensitive to extreme conditions, not only with respect
to long-term stresses, such as food limitation
(Munn and Dawson, 2006), but
also to short-term extremes, such as severe cold or heat (present study)
(Munn and Dawson, 2001).
Short-term stress has been implicated in the mortalities of other large
herbivores, such as caribou (Rangifer tarandus), where severe winter
storms, rather than starvation, appeared to be the immediate cause of
mortality in animals that were also exposed to long-term malnutrition
(Dau, 2005). It is therefore
important that these facets of juvenile mammal physiology be taken into
account when considering the possible impacts of a changing climate.
Currently, the bulk of models that evaluate species' extinction risks in
relation to climate change often neglect the potential impacts on juvenile
survival (e.g. Thomas et al.,
2004; Humphries et al.,
2004). Variation in juvenile survival, however, is particularly
important for large mammalian herbivores from a range of climate and habitat
types (Gaillard et al.,
1998).
|
Acknowledgments |
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|
Footnotes |
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Present address: School of Biological Sciences, The University of Sydney,
Sydney, NSW, 2006, Australia 
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References |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Chappell, M. A., Rezende, E. L. and Hammond, K. A.
(2003). Age and aerobic performance in deer mice. J.
Exp. Biol. 206,1221
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Dau, J. (2005). Two caribou mortality events in Northwest Alaska: possible causes and management implications. Rangifer 16,37 -50.
Dawson, T. J. (1995). Kangaroos: Biology of the Largest Marsupials. Sydney: University of New South Wales Press.
Dawson, T. J. and Needham, A. D. (1981). Cardiovascular characteristics of two resting marsupials: an insight into cardio-respiratory allometry in marsupials. J. Comp. Physiol. 145,95 -100.[CrossRef]
Dawson, T. J., Roberstshaw, D. and Taylor, C. R.
(1974). Sweating in the kangaroo: a cooling mechanism during
exercise, but not in the heat. Am. J. Physiol.
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