Limits to sustained energy intake VIII. Resting metabolic rate and organ morphology of laboratory mice lactating at thermoneutrality
1 Aberdeen Centre for Energy Regulation and Obesity (ACERO), School of
Biological Sciences, University of Aberdeen, Aberdeen AB24 2TZ, UK
2 ACERO, Division of Appetite and Energy Balance, Rowett Research Institute,
Bucksburn, Aberdeen, AB21 9SB, UK
* Author for correspondence (e-mail: e.krol{at}abdn.ac.uk)
Accepted 14 August 2003
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Summary |
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Key words: resting metabolic rate, organ morphology, peripheral limit, heat dissipation limit, laboratory mouse, Mus musculus
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Introduction |
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However, other observations are harder to reconcile with this framework.
For example, mice at peak lactation that are simultaneously pregnant
(Johnson et al., 2001c) or
forced to exercise (Perrigo,
1987
) do not eat more food than mice that are only lactating,
despite the fact that these manipulations do not require elevations in milk
energy output. In addition, in MF1 mice, milk production is not constant as a
function of ambient temperature (Johnson
and Speakman, 2001
;
Król and Speakman,
2003b
) but rather closely mirrors changes in food intake. This
pattern appears to be linked to the ability of mice to dissipate body heat
generated as a by-product of processing food and producing milk (Król
and Speakman
2003a
,b
).
At lower temperatures, there is a greater driving gradient for heat loss,
which permits the mice to increase their heat production, thereby allowing
greater milk production and hence greater food intake (Król and
Speakman,
2003a
,b
).
It has been widely suggested that the maximal capacity for daily energy
expenditure (DEE) is regulated by the level of resting metabolic rate
(RMR) (Drent and Daan,
1980; Peterson et al.,
1990
; Weiner,
1992
). This might occur because RMR reflects the energy
demands of sustaining the visceral organs that are responsible for most of the
energy flux observed as DEE and hence food intake. The heat
dissipation limit hypothesis (Król and Speakman,
2003a
,b
)
suggests that the route of causality in these associations may be reversed.
DEE may be limited by heat dissipation capacity, which defines the
sizes of organs that will be necessary to supply this energy, and these organs
in turn establish the rates of RMR. Hence, the heat dissipation model
predicts that the components of morphology responsible for the energy flux
through the body will be smaller at higher ambient temperatures and this will
result in a smaller increase of RMR in lactation above the level
observed prior to breeding. To test these ideas, we measured RMR
(prior to breeding and at peak lactation) and organ morphology (at peak
lactation) in MF1 laboratory mice exposed to 30°C (thermoneutrality) and
compared these traits with the same parameters measured in mice at 21°C
and 8°C (Johnson et al.,
2001b
; Johnson and Speakman,
2001
).
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Materials and methods |
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Resting metabolic rate measurements
We assessed RMR from the rate of oxygen consumption at 30°C
(constant-temperature incubator; model INL-401N-010; Gallenkamp, Loughborough,
UK), measured during the light phase (between 10:00 h and 17:00 h) by an
open-flow respirometry system connected to a paramagnetic oxygen analyser
(Model 1100A; Servomex Ltd, Crowborough, UK). Individual mice were placed in a
cylindrical Perspex respirometry chamber with rubber stoppers (volume 885 ml)
for 3 h. The flow of air (dried with silica gel; BDH Laboratory Supplies,
Poole, UK) was maintained by a diaphragm pump (Charles Austen Pumps Ltd,
Byfleet, UK) and measured by a wet type laboratory gas flow meter (Model DM3A;
G. H. Zeal Ltd, Alexander Wright Division, London, UK) upstream of the
chamber. Flow rate was 426702 ml min1. Gases leaving
the chamber were dried (silica gel) and passed through the oxygen analyser at
approximately 150 ml min1. Carbon dioxide was not absorbed,
to maximise accuracy in the derived estimates of energy expenditure when the
respiratory quotient (RQ) is not known
(Koteja, 1996a;
Speakman, 2000
). Analyzer
outputs were sampled at 30 Hz, averaged and recorded every 30 s by a PC
equipped with an analogue-to-digital converter (PC-ADH24; Bede Technology Ltd,
Jarrow, UK) and customised BASIC software. The ambient oxygen content of
incurrent air was measured before and after each animal was placed in the
chamber. These data were used to compensate for any drift in the ambient
output of the analyser during each experiment. The rate of oxygen consumption
was calculated by multiplying the incurrent flow rate (corrected to STPD) by
the decrease in fractional oxygen content between ambient and excurrent flows
(Speakman, 2000
). RMR
was estimated from the lowest rate of oxygen consumption over 5 min. The
RMR data (ml O2 min1) were converted to
energy equivalents using an oxycalorific value of 21.117 J
ml1 O2, derived from the Weir
(1949
) equation for an RQ of 1
(Speakman, 2000
). Mean body
mass was calculated from mass before and after each run.
The RMR of 43 adult females was measured both when the mice were virgins and 3650 days later when 28 of the mice were at peak lactation (day 15 and 16 of lactation). The remaining 15 females were non-reproductive controls. All measurements at each time point were repeated for each animal on two consecutive days, to assess the repeatability of respirometry measurements, and then averaged for further analysis. Thus, for each reproducing female we measured RMR prior to breeding (RMRPB) and at peak lactation (RMRL). Non-reproductive females were characterised by RMRNR-1 (measured at the same time as RMRPB) and RMRNR-2 (measured at the same time as RMRL).
Organ morphology
On day 18 of lactation, nine females (litter size 812) were weighed,
killed by cervical dislocation and immediately dissected. We removed brown
adipose tissue, abdominal and mesenteric fat depots, brain, thyroid, heart,
lungs, liver, spleen, pancreas, kidney, front mammary glands, rear mammary
glands and uterus. The gut was cut at the pyloric and cardiac sphincters, the
ileocaecal junction and the anus. The excised stomach and small and large
intestines were cut open longitudinally to remove any residual gut contents
and mucous. The remaining body parts were divided into tail, pelage and
carcass, including skeletal muscle and bone. We recorded wet mass of organs
(±0.0001 g; Ohaus Analytical Plus), dried them in a convection oven at
60°C for 14 days (Król and
Speakman, 1999) and re-weighed them to determine dry mass.
Statistics
Data are reported as means ± S.D. (N = sample
size). For mice exposed to 30°C, the significance of changes in body mass
and RMR over time was assessed by paired t-tests. The
relationship between RMR and body mass was examined by least-squares
linear regression analysis. The regression lines for lactating and
non-reproductive mice were compared using analysis of covariance (ANCOVA). We
calculated residuals for RMR, litter size, pup body mass, litter
mass, litter mass increase and food intake from the least-squares regression
lines on female body mass. Relationships between body masses of the same
individuals measured on separate occasions, RMR measured prior to
breeding and at peak lactation and RMR and life-history traits were
described using Pearson product-moment correlation coefficients. We compared
changes in maternal body mass, RMR and organ morphology following
exposure to different temperatures (30°C, 21°C and 8°C) using
analysis of variance (ANOVA). The Tukey post-hoc test was used when
differentiation between the temperatures was required. The differences in
RMR among the three temperatures were also examined by ANCOVA, with
maternal body mass as a covariate. All statistical analyses were conducted
using Minitab for Windows (version 13.31; Minitab Inc., State College, PA,
USA; Ryan et al., 1985).
Statistical significance was determined at P<0.05. All tests were
two-tailed.
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Results |
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Reproductive females increased their body mass from 28.6±1.6 g prior to breeding to 35.3±2.0 g at peak lactation (paired t=17.1, P<0.001, N=28). The correlation between pre-breeding and peak lactation body masses marginally failed to reach significance (r=0.34, P=0.07, N=28). The increase in body mass was accompanied by an increase in RMR from 17.9±1.6 kJ day1 to 26.0±3.5 kJ day1 (paired t=13.0, P<0.001, N=28). RMRPB was not correlated with RMRL (r=0.32, P=0.10, N=28). The mass-adjusted values (residuals) of RMRPB and RMRL were not correlated either (r=0.06, P=0.77, N=28). However, females with a greater increase in body mass between pre-breeding and peak lactation also had greater increases in RMR (r=0.59, P=0.001). Over the same period of time (3650 days), the non-reproductive females also increased their body mass (from 30.2±2.4 g to 31.7±3.3 g;paired t=4.1, P=0.001, N=15), but the increase was much less than in reproductive females. The NR-1 and NR-2 body masses were highly correlated (r=0.92, P<0.001, N=15). Despite the increase in body mass, there was no significant difference between RMRNR-1 (18.3±2.2 kJ day1) and RMRNR-2 (18.9±2.1 kJ day1) (paired t=1.1, P=0.30, N=15). There was no correlation between RMRNR-1 and RMRNR-2 (r=0.46, P=0.09, N=15). Residual values of RMRNR-1 and RMRNR-2 were also not significantly correlated (r=0.23, P=0.41, N=15).
RMR increased with body mass in all groups (NR-1, NR-2, PB and L). As anticipated, there was no significant difference in RMR between mice that were destined to breed (PB) and those we selected not to (NR-1) (ANCOVA: interaction body mass x group, P=0.67; body mass effect, F1,40=11.8, P=0.001; group effect, F1,40=0.4, P=0.55). Pooling the data across both these groups (N=43), the relationship between RMR (kJ day1) and body mass (BM; g) was RMRNR=5.56+0.43BM, with body mass explaining 22.8% of the individual variation in RMRNR (F1,41=12.1, P=0.001). The relationship between RMR and body mass was stronger at peak lactation (RMRL=18.16+1.25BM), with body mass explaining 52.0% of the variation in RMRL (F1,41=28.1, P<0.001; Fig. 1). The RMR of lactating females was compared with that of NR-1 and NR-2 groups separately. The slope of the regression line for lactating females was higher than for non-reproductive females from the NR-1 group (ANCOVA: interaction body mass x reproductive status, F1,39=4.8, P=0.034) and the NR-2 group (ANCOVA: interaction body mass x reproductive status, F1,39=9.2, P=0.004). This shows that the increase in RMR from a mean of 17.9 kJ day1 (prior to breeding) to a mean of 26.0 kJ day1 (peak lactation) was greater than expected from the increase in body mass (on average, 28.6 g prior to breeding and 35.3 g during lactation).
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For reproductive females, neither RMR measured prior to breeding nor RMR at peak lactation were significantly correlated with any life-history traits (litter size, pup body mass, litter mass and litter mass increase), asymptotic food intake, residual life-history traits or residual asymptotic food intake (Table 1). Using residual RMRPB and residual RMRL yielded no significant correlations either. For non-reproductive females, neither RMRNR-1 nor RMRNR-2 was significantly correlated with food intake or with mass-adjusted food intake (Table 1). There was also no significant correlation when we used residual RMRNR-1 and residual RMRNR-2.
|
The effect of temperature on maternal RMR
We compared RMR and organ morphology of mice that were raising
their first litters in hot (30°C; present study), warm (21°C;
Johnson et al., 2001b) and
cold (8°C; Johnson and Speakman,
2001
) temperatures. The hot and the warm mice were exposed to
30°C and 21°C, respectively, through a two-week acclimation period
(prior to breeding) as well as the whole course of pregnancy and lactation.
The cold mice were maintained at 21°C until the pups had grown fur and
were then exposed to 8°C from day 10 of lactation onwards.
All measurements of RMR were conducted at 30°C, using the same respirometry system and the same protocol. Pre-breeding measurements (RMRPB) were taken at the end of the acclimation period to 30°C (hot mice) or 21°C (warm and cold mice). Peak lactation measurements (RMRL) were taken on days 1516 (hot mice) or 18 (warm and cold mice). Sample sizes for the hot, warm and cold groups were 28, 71 and 15, respectively.
Prior to breeding, the RMR of hot, warm and cold mice averaged 17.9±1.6 kJ day1, 21.5±6.1 kJ day1 and 22.2±2.6 kJ day1, respectively (Table 2; Fig. 2). There was a significant difference between the groups (ANOVA, F2,111=6.0, P=0.003), with hot mice having a lower RMRPB than both warm and cold mice (Tukey pairwise comparisons, P<0.05). As expected, the RMRPB of warm and cold mice did not differ (Tukey pairwise comparison, P>0.05), since at this stage both groups were kept at the same temperature (21°C). Hot mice still had a lower RMRPB than warm or cold mice after adjusting for the differences in female body mass (ANCOVA: interaction body mass x temperature, P=0.83; body mass effect, F1,110=9.8, P=0.002; temperature effect, F2,110=8.6, P<0.001). At peak lactation, RMR also differed between the groups (ANOVA, F2,111=35.0, P<0.001), with mice at 30°C having a lower RMRL (26.0±3.5 kJ day1) than mice at 21°C (47.0±13.8 kJ day1; Tukey pairwise comparison, P<0.05) and mice at 8°C (51.8±14.3 kJ day1; Tukey pairwise comparison, P<0.05). After adjusting for the differences in maternal body mass, the effect of temperature on RMRL was not significant (ANCOVA: interaction body mass x temperature, P=0.82; body mass effect, F1,110=38.3, P<0.001; temperature effect, F2,110=2.5, P=0.07). The ratios of mean asymptotic food intake (Table 2) to mean RMRL in the hot, warm and cold mice were 7.5, 7.9 and 9.4, respectively.
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The increase in RMR at peak lactation above the level measured prior to breeding (RMRLRMRPB) averaged 8.1±3.3 kJ day1, 25.5±13.1 kJ day1 and 29.6±13.6 kJ day1 in hot, warm and cold mice, respectively (Table 2). Thedifference between the groups was significant (ANOVA, F2,111=26.6, P<0.001), with hot mice having a lower increase in RMR than both warm and cold mice (Tukey pairwise comparisons, P<0.05). However, when we adjusted for the differences in the increase in body mass (BMLBMPB), the effect of temperature on the increase in RMR was not significant (ANCOVA: interaction body mass increase x temperature, P=0.40; body mass increase effect, F1,110=40.3, P<0.001; temperature effect, F2,110=0.8, P=0.47). Thus, the relatively small increase in RMR observed in mice at 30°C was associated with their relatively small changes in body mass (Fig. 3). The increase in body mass at peak lactation above the non-reproductive level averaged 6.7±2.1 g, 17.1±2.8 g and 18.3±4.2 g in hot, warm and cold mice, respectively. These values were significantly different (ANOVA, F2,111=146.9, P<0.001), with hot mice having a smaller increase in body mass than both warm and cold mice (Tukey pairwise comparisons, P<0.05).
|
The effect of temperature on maternal organ morphology
To evaluate the effect of the hot, warm and cold temperature treatments on
maternal morphology, we compared the dry masses of 15 organs: brown adipose
tissue, heart, lungs, stomach, small intestine, large intestine, liver,
pancreas, spleen, white adipose tissue (abdominal and mesenteric fat), mammary
glands, uterus, tail, pelage and carcass. Since the kidneys were used for
other analyses (M. S. Johnson and J. R. Speakman, manuscript in preparation),
the comparison was made only between wet masses for this organ. All mice were
dissected on day 18 of lactation, using the same protocol. The comparisons
excluded females that had been previously milked
(Król and Speakman,
2003b). For the warm and cold groups, dissections were performed
on animals that had undergone measurements of RMR. No RMR
measurements were taken for the mice dissected from the hot group. The sample
sizes for the hot, warm and cold groups were 9, 16 and 15, respectively. The
morphology data for the hot group are presented in
Table 3.
|
On the day of dissection, the body masses of the hot, warm and cold mice
averaged 36.6±3.0 g, 40.8±2.5 g and 51.0±5.5 g,
respectively. The differences between the groups were significant (ANOVA,
F2,37=43.5, P<0.001; all Tukey pairwise
comparisons, P<0.05). Since organ size frequently correlates with
body mass (e.g. Selman et al.,
2001), comparison of organ morphology usually requires corrections
for the differences in body mass. In our study, however, the differences in
body mass at peak lactation between the hot, warm and cold mice were a
consequence of the exposure to different temperatures
(Table 2). Therefore,
correcting for differences in body mass would inevitably remove differences
caused by the temperature treatment. To avoid this, we compared mean absolute
masses of organs by ANOVA (Table
4).
|
The temperature to which the animals were exposed during lactation had a significant effect on masses of most of the organs (apart from the uterus), with mice at 8°C having heavier organs than mice at 21°C and 30°C (Table 4). The masses of heart, liver and kidneys in hot mice were significantly lower than those of the warm mice. The dry masses of brown adipose tissue, lungs, stomach, small intestine, large intestine, pancreas, spleen, white adipose tissue, mammary glands, tail, pelage and carcass did not differ significantly between the hot and warm mice.
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Discussion |
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We demonstrated that mice exposed to 30°C had significantly higher
RMR at peak lactation than prior to breeding but that the values of
RMRPB and RMRL (both absolute and
mass-adjusted) were not correlated. An increase in RMR between
pre-breeding and peak lactation conditions has been previously shown in MF1
laboratory mice at 21°C (Speakman and
McQueenie, 1996; Johnson et
al., 2001b
) and 8°C
(Johnson and Speakman, 2001
)
as well as in other small rodents (e.g.
Garton et al., 1994
;
Künkele and Trillmich,
1997
; Antinuchi and Busch,
2001
). We found no evidence that individual variation in either
RMRPB or RMRL was correlated with
variation in litter size, litter mass, pup body mass or litter mass increase,
for both absolute and residual values
(Table 1). Previous studies
have also shown no link between maternal RMR and life-history traits
at temperatures of 2022°C in MF1 mice
(Johnson et al., 2001b
),
HSD/ICR mice (Hayes et al.,
1992
), deer mice (Peromyscus maniculatus;
Earle and Lavigne, 1990
) and
hispid cotton rats (Derting and McClure,
1989
). It would therefore appear that while the general pattern of
increase in RMR during reproduction is compatible with the idea that
these changes reflect changes in the capacity of the system to digest and
process extra energy to support lactation, at an individual level this
association breaks down. The reasons why no relationship between maternal
RMR and reproductive performance was observed are unclear, since the
repeatability of our RMR measurements was high (coefficient of
variation=7.7%) when compared with the overall variation in RMR
between individuals (20.032.6 kJ day1). Hence, the
absence of a link between RMR and life-history traits was probably
not because of errors inherent in the RMR estimate. Moreover, the
estimates of RMR in the current study were predominantly the average
of measures of RMR made on two consecutive days, further reducing
variation attributable to analytical factors.
As predicted by both the heat dissipation and peripheral limit hypotheses,
the increase in RMR at peak lactation above the level measured prior
to breeding was significantly lower in mice exposed to 30°C than in mice
at 21°C and 8°C (Table
2; Fig. 2). As
temperature declined, increases in RMR were closely paralleled by
changes in maternal body mass, and there was no independent temperature effect
on RMR (Fig. 3).
Examination of the morphological changes of mice at different temperatures
revealed a progressive increase in mass as a function of the cold in several
organs including heart, lungs, stomach, small intestine, large intestine,
liver, pancreas, spleen, kidneys and the mammary glands. However, only the
masses of the heart, liver and kidneys differed significantly between all
three temperature groups (Table
4). These data indicate that the increased body mass and
RMR were a consequence of the increases in the masses of the
metabolically active organs primarily involved in the energy flux
through the body. Further tests of heat dissipation and peripheral limit
hypotheses should involve measurements of organ safety margins (excesses of
capacities over prevailing loads; e.g.
Toloza et al., 1991;
Diamond, 1998
;
Hammond, 1998
). Since
sustaining organ safety margins produces extra heat associated with tissue
maintenance and enzyme biosynthesis, we expect these margins to be
substantially reduced in mice at 30°C.
Milk energy output (MEO) in mice exposed to 21°C and 8°C
was 90.1% and 228.4%, respectively, higher than the level measured in mice at
30°C (87.7 kJ day1;
Król and Speakman,
2003b). The increase in MEO was paralleled by the
increase in the mass of mammary glands (16.6% in mice at 21°C and 156.3%
in mice at 8°C), although the difference between the warm and hot groups
was not significant (Table 4).
Thus, the increase in milk production by 228.4% at 8°C was associated with
a substantial increase in the mass of the mammary glands, whereas the 90.1%
increase in MEO at 21°C was accommodated by mammary glands of a
size similar to those at 30°C. These results suggest that mass might be a
poor indicator of capacity of mammary glands to produce milk, especially when
no adjustments are made for individual variation in organ composition such as
lipid or connective tissue content. The use of techniques that measure the
number of mammary secretory cells (e.g. the bromodeoxyuridine-labelling index;
Capuco et al., 2002
), the
activity of the secretory cells (e.g. the explant method;
Wilde et al., 1999
) and the
rate of their apoptosis (e.g. DNA laddering intensity;
Wilde et al., 1997
) could be
more informative.
Although cold exposure enabled mice to increase milk production by
releasing them from the heat dissipation constraint, there were some changes
in the maternal organ morphology that suggest that cold was still a
thermoregulatory burden. These include increases in the masses of brown
adipose tissue, white adipose tissue, pelage and tail
(Table 4). Changes in these
organs are often observed in non-reproductive small rodents exposed to cold,
since brown adipose tissue hypertrophy is associated with elevated
non-shivering thermogenesis (e.g. Klaus et
al., 1988), bigger white adipose tissue depots and heavier pelts
provide better insulation (e.g. Heldmaier
and Steinlechner, 1981
), and increased vascularisation of
peripheral tissue (e.g. tail and ears) prevents frostbite (e.g.
Héroux, 1959
). The fact
that mice lactating at 8°C benefited from cold exposure in terms of
reproductive performance but at the same time underwent morphological changes
that increase heat production and improve heat retention has three possible
explanations. First, heat generated via food processing and milk
production might not be used to offset the costs of thermoregulation, either
fully or partially. Such a lack of any level of compensation of
thermoregulatory costs by the biochemical heat increment of feeding has been
demonstrated in star-nosed moles (Condylura cristata;
Campbell et al., 2000
).
The second possibility is that heat produced from elevated food intake and
milk production can substitute for active thermogenesis, but only partially.
In this case, mice at 8°C would still need more brown adipose tissue,
better insulation and increased vascularisation of peripheral tissue. This
view is supported by a study of thermoregulation in Sprague-Dawley female rats
(Eliason and Fewell, 1997).
According to the data presented by Eliason and Fewell in
fig. 3, RMR of
non-reproductive rats averaged 72 ml O2 kg1
min1 at 14°C and 22 ml O2
kg1 min1 at 28°C (thermoneutrality),
giving thermoregulatory costs of 50 ml O2 kg1
min1. However, when lactating rats (day 20 post partum) were
measured at 14°C, their RMR averaged 60 ml O2
kg1 min1, i.e. 12 ml O2
kg1 min1 below the level of
non-reproductive individuals. These data suggest that the 24% reduction in
thermoregulatory costs of lactating rats (12 of 50 ml O2
kg1 min1) could be attributed to the heat
generated by lactogenesis. Since the measurements of RMR in the
lactating rats were not paralleled by measurements of milk production, the
proportion of heat used to compensate the cost of thermoregulation (12 ml
O2 kg1 min1) to the total
amount of heat produced by lactogenesis is unknown.
The third possibility is that heat generated via food processing
and milk production could fully substitute for active thermogenesis. This
would imply no need for bigger brown adipose tissue, white adipose tissue,
pelage and tail, providing that the masses of these organs correlate with
their function. It might be the case, however, that the mice lactating at
8°C increased the mass of brown adipose tissue, white adipose tissue,
pelage and tail in anticipation of post-weaning thermoregulatory demands, so
that the greater organ masses did not reflect increased function during
lactation. Indeed, it has been demonstrated in Aston laboratory mice lactating
at 23°C that the thermogenic capacity of brown adipose tissue (measured as
the uncoupling protein content of the tissue) is as low as 8% of that of
virgin mice, despite the morphological hypertrophy of the organ
(Trayhurn and Jennings, 1987).
Similar results have been obtained from measurements of the capacity for
non-shivering thermogenesis following noradrenaline injections
(Trayhurn, 1983
). However, the
changes in thermogenic capacity of brown adipose tissue during lactation at
different temperatures remain unknown and would be a useful topic for future
studies.
In summary, comparison of organ morphology in MF1 mice lactating at 30°C, 21°C and 8°C revealed that the masses of visceral organs responsible for energy flux increased as temperature declined. The differences in the organ masses between the cold and warm mice were all significant, whereas for warm and hot groups, only the masses of heart, liver and kidneys were significantly different. The increases in organ masses were paralleled by the increases in RMR above the levels measured prior to breeding, with warm and cold mice having significantly larger increases in RMR than hot mice. The observed changes in visceral organs and RMR are consistent with both the heat dissipation and peripheral limit hypotheses. However, mice exposed to 8°C had substantially bigger mammary glands than mice at 21°C and 30°C, which argues against the peripheral limitation hypothesis and supports the heat dissipation limit hypothesis. Cold exposure also resulted in greater masses of brown adipose tissue, white adipose tissue depots, pelage and tail, but the functional significance of these changes has yet to be established.
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Acknowledgments |
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Footnotes |
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