J Camp Physiol B 11996) 166: 000-000
(. Spriuger- Verlag 19')6
ORIGINAL PAPER
R. M. McDevitt· J. R. Speakman
Summer acclimatization in the short-tailed field vole, Microtus agrestis
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Abstract We investigated the changes that occurred in to compensate for a reduction in regulatory non­
basal and noradrenaline-induced metabolic rate, body shivering thermogenesis. Here we found that a combi­
temperature and body mass in short-tailed field voles, nation of increased ambient temperature and photo­
period did significantly reduce thermogenic capacity
Microtus aqrestis, during exposure to naturally increas­
in winter-acclimatized voles, This provided evidence
ing photoperiod and ambient temperature. These param­
eters were first measured in winter-acclimatized voles that the two aspects of non-shivering thermogenesis,
obligatory and regulatory, are stimulated by different
(n = 8) and then in the same xoles which had been
allowed to seasonally acclimatize to photoperiod and exogenous cues, Summer acclimatization in the short­
ambient temperature (6 months later). Noradrenaline tailed field vole is manifest as a significant decrease
induced metabolic rate, basal metabolic rate and non­
in both basal and noradrenaline-induced metabolic
shi vering thermogenesis were significantly higher in rate, combined with a significant increase in body
winter-acclimatized compared to summer-acclimatized mass,
voles. There was a significant positive relationship be­
tween basal metabolic rate and noradrenaline-induced Key words Seasonal acclimatization' Basal metabolic
metabolic rate. Body mass was significantly higher in rate' Non-shivering thermogenesis' Photoperiod'
summer-acclimatized compared to winter-acclimatized Field vole, Microtus aqrestis
voles. There was a significant positive relationship be­
tween body mass and noradrenaline-induced metabolic Abbreviations AN CO V A analysis of covariance'
rate in both winter-acclimatized and summer-acclima­
BA T brown adipose tissue' BM body mass'
tized voles; however, there was no relationship between BMR basal metabolic rate' NST Don-shivering
basal metabolic rate and body mass in either seasonal thermogenesis' N A noradrenaline' N A VOz the
group of voles. Body temperature after measurements maximum VOz recorded following mass specific
of basal metabolic rate was not significantly different in injection of noradrenaline' SAVO z the maximum
the seasonal cohorts of voles. However, body temper­
VOz recorded following mass specific injection of saline'
ature was significantly higher in winter-acclimatized T. ambient temperature' T b rectal body temperature'
compared to summer-acclimatized voles after injection TIc lower critical temperature' UCP uncoupling
of noradrenaline. Previously we have found that a long protein' VOz oxygen consumption
photoperiod was not a sufficient stimulus to reduce
thermogenic capacity in winter-acclimatized voles dur­
ing cold exposure, since basal metabolic rate increased
R.M. McDevitt (181)" J.R. Speakman
Department of Zoology, University of Aberdeen, Aberdeen,
AB9 2TN, Scotland. UK
, Present address:
The Dunn Clinical Nutrition Centre, Hills Road, Cambridge,
CB2 2DH, England, UK
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During the process of seasonal acclimatization in free
living small endotherms, several environmental factors,
namely T. or photoperiod, or a combination of the
two, provide the required stimuli or cues to begin the
appropriate physiological alterations (Heldrnaier et at
1982; Haim 1982; Klaus et aI. 1988; Heldmaier 1989).
As photoperiod is a more predictable environmental
parameter relative to T a , it may be a more effective cue
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R.M. McDcvrtt and J.R Speak man: Summer
for seasonal acclimatization (Heldmaier and Steinlechner
1981) and indeed, in many species photoperiod has
been identified as the major acclimatization stimulus
(Hairn et a]. 1988: Banin et al. 1994). During winter
acclimatization, i.e. decreasing T, and photoperiod,
several physiological alterations occur which ensure
minimisation of energy expenditure and improved cold
tolerance (Blank and Ruf 1992). These include a reduc­
tion in BM (Mezhzhenn 1964; Merritt 1986; McDevitt
and Andrews 1995), a reduction in BMR (Wunder et al.
1977; Heldmaier 1989; McDevitt and Andrews 1995) to
reduce energy costs, and a reduction in thermal con­
ductance (Heldmaier and Steinlechner 1981; Reynolds
and Lavigne 1988; Heldmaier 1989). In addition, there
is an increase in the ability to produce heat, so that
when faced with a cold challenge the animal is primed
to respond thermogenically (Held maier and Buchber­
ger 1985; Heldmaier et al. 1986; Himrns-Hagen 1986).
Small mammals which remain active in winter rely
primarily on their BAT for generating this heat by NST
(Jansky 1973; Rafael et al. 1985a; Rafael et al. 1985b;
He1dmaier and Buchberger 1985; Heldmaier et al.
1985). The thermogenic capacity of BAT increases sig­
nificantly in many species such as hamsters iPhodo pus
sunqoruss, voles iCtethrionom ys qlareolus and M icrotus
agrestis) and mice iApodemus sylvaticus and A.
fiavicolus) during natural winter acclimatization
(Rosenmann et al. 1975; Klaus et al. 1988; McDevitt
and Speakman 1994a). Changes of a similar magnitude
are observed when animals are acclimated by artificial
means by exposure to the cold and short photoperiod
(Klingenspor et al. 1989; Bourhim et al. 1990; Wiesinger
et al. 1990).
When acclimatization to summer conditions occurs,
where the environmental cues are increasing T, and
photoperiod, there is a reversal of the many physiolog­
ical changes that occurred during winter acclimatiza­
tion. In most small non-hibernating mammal species
there is an increase in BM (Wunder et al. 1977; Klaus
et al. 1988; Heldmaier 1989; McDevitt and Andrews
1995), an increase in thermal conductance (Wunder
et al. 1977; Haim et al. 1991) and an increase in BMR
(Wunder et al. 1977; Haim et al. 1991). Seasonal com­
parisons within species have also demonstrated that
there is a significant decrease in the thermogenic capac­
ity of BAT, and thus NST, in summer-acclimatized
compared to winter-acclimatized individuals (Wunder
et al. 1977; Rosenmann et al. 1975; Heldrnaier et al.
1986; Feist and Feist 1986; McDevitt and Speakman
1994a). The same changes are also observed in many
species when exposed artificially to long photoperiod
and warm T a (Maier and Feist 1991; Banim et al. 1994)
or upon exposure to long photoperiod alone (Hairn
and Levi 1990). However, there are exceptions to the
usual trend of changes in BM; for example, there is no
change in BM during seasonal acclimatization in the
pouched mouse, Saccus tom liS campestris (Ellison et al.
1992; Ellison et al. 1993) and C. qlareolus showed
aCCl1l11ali/ation In
the helJ vole
a slight increase in winter BM (Riga udiere 1969). In
addition, BM R did not change significantly durin"
seasonal acclimatization in two species of volcAC
qiareoius (Klaus et al, 1988) or C. rutilus (Feist and
Feist 1986) or in two species of wood mice. .4. sylw[ICLIS
and A.(lauicoilis (Klaus et al. 1988).
All microtine rodents regulate body temperature
continuously at euthermic levels, i.e. they do not ern­
ploy reversible hypothermia, either in the short term as
daily torpor, or in the long term as hibernation (Brad­
ley 1976; Wunder et al. 1977; Wunder 1985). In the case
of the short-tailed field vole, Microtus aqrestis, no evi­
dence of torpor was recorded despite exposure to tem­
peratures ranging from +25 "C to as low as -5°C for
up to 72 h. (McDevitt and Speakman 1994b). Microtus
agrestis, therefore, relies on adj ustments of beha vioural
and thermoregulatory mechanisms, such as shivering
and NST to seasonally acclimatize. We have found
a Significant seasonal decrease in the concentration of
VCP in BAT in summer-acclimatized M, aqrestis com­
pared to winter-acclimatized voles, indicating a prob­
able reduction in thermogenic capacity (McDevitt
and Speakman 1994a). When winter-acclimatized
M. agrestis were further cold acclimated (5"C for
100 days) and exposed to a long photoperiod of
14L: 10D, none of the biochemical parameters of BAT
thermogenic activity decreased significantly, i.e. there
was no evidence of any "de-acclimatization" in re­
sponse to long photoperiod (McDevitt and Speakman
1994a). However, both BMR and BM did increase
significantly in the long photoperiod with duration of
cold exposure. This could indicate that photoperiod
was cueing a change in BMR and BM in the direction
generally observed during summer acclimatization
(Klaus et al. 1988; Heldmaier 1989) despite the pro­
longed cold exposure. However, we do not know the
natural pattern of seasonal changes in BM and BMR in
M. aqrestis. The alternative explanation for these re­
sults is that the prolonged cold exposure caused an
increase in BMR [obligatory NST; Jansky (1973)J to
compensate for the reduction in regulatory NST that
occurred in response to long photoperiod (McDevitt
and Speakman 1994a).
In the present study we investigated the changes
in BMR, NST, T b, and BM that occurred in M. aqrest is
during the process of summer acclimatization, i.e.
during exposure to naturally increasing photoperiod
and T a . As the voles were exposed to continuously
changing environmental stimuli rather than one con­
stant controlled variable under laboratory condi­
tions, they were undergoing acclimatization rather
than acclimation. We aimed to test the hypothesis
that the combined effects of increasing photo­
period and T a would increase BM and BMR but re­
duce NST in summer-acclimatized M. aqrestis when
compared to winter-acclimatized voles if this was the
natural pattern of changes that occurred in summer
acclimatization.
R.M. Mc Devrt t and l.R. Speakman: Summer acclimatization
In
the field vole
Materials and methods
Animals
Short-tailed field voles were caught 30 krn north of Aberdeen, Scot­
land (57 N) in a young (approximately 8 years old) evergreen
plantation (Pinus sylvCl(icus). Voles were caught using Longworth
live traps using carrots as bait and hay for bedding. Winter-accli­
matized voles were captured in November 1993 (n = 8) and meta­
bolic measurements commenced within a week of capture. Between
measurements, which took 3 weeks in total to conduct, the voles
were housed in an unheated outdoor building to ensure that they
remained winter acclimatized. This building was an unheated "lean­
to" on the roof of the Zoology building in Aberdeen, which was
constructed with a clear polythene roof and sides, attached to
a wooden frame. After all the metabolic measurements had been
conducted on the winter-acclimatized voles, they were maintained in
the outdoor housing for 6 months. In this manner, the voles were
exposed to natural seasonally changing cues of both photoperiod
and T a- All of the metabolic measurements were repeated on the
same individuals in May 1994. The voles were maintained singly In
large cages (60 x 20 x 30 cm) with sawdust as substrate and shredded
tissue as bedding. The animals were fed a diet of rodent chow
ad libitum (SRC, special diets), supplemented weekly with fresh
vegetables. Water was also provided ad libitum.
Measurement of metabolic rates
Metabolic rate was measured in the voles using an open-circuit
indirect calorimeter system [see McDevitt and Speakman (! 994b)
for specific details]. Briefly, the voles were placed in a metabolic
chamber within a constant temperature cabinet (Gallenkarnp,
±O.I 'C). Excurrent air, which was dried (Silica Gel, BDH) before
and after passing through a flow meter (Alexander Wright, 0.25 I)
was drawn from the metabolic chamber at a rate of
500 mi· min - I and through an oxygen analyser (Applied Electro­
chemistry 53A) for the measurement of V0 2 (rnl min - I). The only
difference in detail was that V0 2 measurements were carried out
when the voles were in a 2 I Perspex cylindrical metabolic chamber
sealed by large rubber bungs at either end. Each bung had an
incurrent or excurrent port drilled in it which allowed air to flow
through the chamber. The metabolic chamber had a removable
perforated Perspex platform which extended the whole length of the
chamber and which kept the voles separated from their voided urine
and faeces. The design of these chambers facilitated speed of hand­
ling of the voles to ensure minimum delay between injections and
measurement of metabolic response. NA-induced
2 (NA
1)
was the maximum Val measured in response to a mass specific
subcutaneous injection of NA at a T. below the Tic (Heldmaier
1978). The NA solution was made up of I mg noradrenaline bitar­
trate salt (Sigma, UK) per 2 ml of9% saline and was administered as
1.5 rng : kg- I of BM. This high dose of NA should have been
sufficient to induce a significant thermogenic response in a small
mammal which weighs circa 25 g (Heldrnaier 1971) and is in keeping
with doses stated previously in the literature (Haim et al., 1993;
Hislop and Buffenstein, 1994; Haim et al. 1995). The volume of NA
administered was 0.015-0.025 rnl, which vaned with season since
BM was found to increase in summer-acclimatized compared with
winter-acclimatized voles (Wunder 1985; Heldmaier 1989). Non­
shivering thermogenesis was the difference between NAVal, i.e.
regulatory thermogenesis and BMR, i.e. obligatory thermogenesis
(Jansky 1973; Ellison et al, 1992).
The voles were denied food for I h before the experiments and for
the duration of each experiment. Each vole was weighed (Sartorius,
0.1 g) prior to measurements of vo, Val was measured at the Tic
which was either 25 'C (winter acclimatized) or 26'C (summer
va
ro
3
acclimatized] for 2 h (Mc Oevitt and Speakman 1994<:1. ~~O, was
recorded every 30 s and the lowest reading over a consecutive
10-min period was taken as the BMR (Hayes et al. I992b). The vole
was then removed from the chamber and injected subcutaneously
with NA, replaced immediately within the chamber and the response
of ~i02 recorded for a further hour. The maximum vo. recorded
over a 10-min period within this hour was taken to be NA ro z
Since we were only making within-study comparisons, an instant
correction procedure was not carried out (Bartholomew et al. 1981).
The same procedure was duplicated in each vole except that
a matched-volume saline (9%) dose was injected instead of NA after
a 2-h BMR recording (SAV0 2 ). This was to act as a control to
ensure that a thermogenic response was being measured and not
simply a stress response to handling and the injection. The metabolic
response to Injections of either NA or saline was measured in
a randornised order.
Body temperature
T b was measured in the voles using a beaded thermistor attached to
a calibrated digital display unit (Digitronl, On each occasion, the
thermistor was lubricated (Petroleum Jelly, BP) and inserted to
a depth of 15-20mm for about 40s or until T; had stabilised. T b
was measured after each determination of BMR. Since we did not
Wish to miss the onset of a metabolic response to NA, T; was not
measured immediately after measurements of either NAVO, or
SA Val. Instead, duplicate injections of both NA and saline were
made in the same voles, in random order, whilst the thermistor was
inserted rectally and T b was measured within 30 s of the injection or
when it had become stable. This was usually done within 24 h of the
Initial metabolic measurements.
Statistical analysis
Differences in BMR, BM and T b within each seasonal cohort were
compared using paired Student's r-tests. Seasonal variation in all the
parameters were also analysed by analysis of covariance (AN­
CaVA), with BM as a covariate, using the statistical package
Miniiab (Ryan et al. 1988). All data are presented as means j Sf).
Results
Noradrenaline-induced metabolic response in
M. aqrestis
There was no significant difference between BMR
(1.41±0.14ml·min- t ) and SAV02 (1.36 ± 0.27 rnl :
min -1) in the winter-acclimatized voles and both were
significantly lower (P:<;:; 0.01) than NAV02 (3.46 ±
0.22 mI· min - I). In the summer-acclimatized voles,
SA Val (0,98 ± 0.22 mi· min - t) was not significantly
different from BMR (1.06 ± 0.27 rnl min - 1) but both
were significantly lower (P < 0.01) than NA Val
(2.57 ± 0.28 mi· min -t) (Table 1). There was a signifi­
cant increase in BMR in M. aqrestis in response to NA
in both winter-acclimatized and summer-acclimatized
voles (Table 1). Both BMR and NA Val were signifi­
cantly higher in winter-acclimatized compared with
summer voles (P :<;:; 0.05 in each case). These signifi­
cant within-season and between-season relationships
.,
R.M McDevitt and J.R. Speakman: Summer acchmanzauon
4
Table 1 Body mass. metabolic rare and T bin winter- and summer­
(/I = 81. Body temperature was recorded
after BMR dcterrninanons and after a duplicate injection of NA and
saline, respectively (see text for detuilsj.Non-shivering thermogenesis
(NST) was determined as the difference between BMR and NAVO l .
Metabolic rates are expressed in both whole animal and mass­
specific terms. Data are mean ± SD
..
-c
4.0
a
a
0 ......
Oil
30
4il:l
0
(11 = 8)
Body mass (g)
20J
Metabolic rate
(ml'min-')
BMR
Saline V0 2
1.41
1.36
3.46
2.05
NST
(ml02· h - 1 ' g " )
BMR
NAVpr-~
NST~ - , . g
r, ('C)
BMR
Saline
NA
;;.
Summer
acclimatized
-e
z
0
20 ]
± 4.8"
a
..
..
0
(n = 8)
28.0
0
0
0
0
10
0.6
14
1.2
0.8
1.6
BMR (rnl-min " i
NAV0 2
.0.--,
± 3.1
the licld vole
'jO
acclimatized M. aqrcst is
Winter
acclimatized
In
j}
± 0.J4'
± 0.27
± 0.22'(
± 0.24'
1.06
0.98
2.57
1.51
± 0.27
± 0.22
± 0.28(
± 0.49
10 l
0.5
"-
"
-e
~
3.58 ± 0.38
9.25 .t 1.83"'"
6.23 ± 0.71'
2.29
5.51
3.26
± 0.46
± 0.94";.\
± l.05
.~
00
...
0
~
I
l
II
~
0
II
III II
37.4
39.2
± 0.9
± 0.4'"
37.6
37.5
38.0
± 1.1
± 0.8
± O.~
remained significant when the data were expressed in
mass specific terms (Table I).
There was no significant relationship between BMR
and NAV0 2 in each seasonal group of voles when the
data were treated separately. However, there was a sig­
nificant positive relationship between BMR and
NAV0 2 when the data were pooled across both sea­
sons (F = 6.00; P ~ 0.05). This relationship was best
described by the equation; log BMR = 0.934 +
0.725 log NAV0 2 which explained 25% of the vari­
ation in BMR (Fig. 1a). Using the residuals from the
relationship between ~'02 and BM, there was no signifi­
cant relationship between mass-independent BMR and
mass-independent NAV0 2 when the data were pooled
or treated separately (Fig. 1b). The difference between
BMR and NA V0 2 , which has been termed regulatory
NST (Jansky 1973), was significantly higher (P ~ 0.05)
in winter-acclimatized (2.05 ± 0.24 ml min -t) com­
pared to summer-acclimatized voles (1.51 ± 0.49 ml
min -1) (Table I). This seasonal difference remained
significant when NST was expressed in mass-specific
terms (Table I). In winter-acclimatized voles NA VO 2
was significantly higher than BMR by a factor of 2.5
(P ~ 0.00 1). In summer-acclimatized voles NA V0 2
was significantly greater than BMR by a factor of 2.4
(P ~ 0.0(1). There was a highly significant inverse rela­
tionship between NAV0 2 and time in both winter and
summer voles, i.e. NA V0 2 decreased with increasing
0
0
0
(0.5)
;;.
0
z
(10)
II
(15)
b
Paired Student's r-tesi:
, P s: 0.05, "P s: 0.01, ." P s: 0.001: between-season differences
(p S; 0.05, lol P s; 0.0 I: ;-}j P s: 0.00 J: within-season differences
II
0
-e
3H ± 1.3
o
II
I
(04)
(02)
,
0.0
0.2
0.4
BMR residuals
Fig. la, b The relationship between (a) BMR and NAVO: and
(b] mass-independent BMR and mass-independent NAV0 2 in win­
ter- (solid symbols) and summer-acclimatized (open symbols) M.
aqrestis. There was a significant positive relationship between BMR
and NAV0 2 but not between mass-independent BMR and NAV0 2
time post-injection of NA. In winter voles this relation­
ship was best described by the least-squares fit regres­
sion equation, NA V0 2 (ml- min - I) = 3.08 - 0.02
Time (min) which explained 43.0% of the variation in
NAV0 2 (F = 54.5; P ~ O.(X>l). In summer voles the
relationship was best described by NAV0 2
(ml min - I) = 2.68 - 0.02 Time (min) which explained
30.7% of the variation in NAV0 2 (F = 27.12;
P s 0.001). Neither BMR nor SA V0 2 had a significant
relationship with time in either winter or summer voles
(Fig. 2).
Seasonal variation in body mass in M. aqrestis
BM in summer-acclimatized voles was significantly
higher than in winter-acclimatized voles (P::O; 0.01)
(Table I). In the latter there was a significant positive
relationship between BM and NAV0 2 (F = 5.76;
P .:; 0.05). This relationship, which explained 40.5% of
the variation in NA V0 2 was best described by the
equation NA V0 2 = - 8.82 + 3.99 log BM (Fig. 3a). In
summer-acclimatized voles there was a significant
positive relationship between NA V0 2 and EM which
,.1"ocvLtt and J.R. Speakman: Summer acclimatization
In
the held vole
400
50...----­
4.0
-
•
:'IAVOl
390
c9'"
0
c
E
s-;
.H)
•
••
380
0
E
.0
BMR
,
20
0
E-
o
1!l!!!!!!!I!!·~liil!lii·1II
;,
10
37.0
0
36.0
0.0 + - - - - - , - - - , - - - - - , - - - - , - - - - - - j
200
o
80
160
40
120
•
0
0
•
•
0
0
00
.
.
••
0
0
0
o.
••
0
35.0
0.00
100
1.00
3.00
400
5.00
Time (min)
Fig. 2 Metabolic rate in an individual M. agrestJJiU'Ill:llSll,red-ll
seasons, winteO(solid squares) and summe acclimatiz
(open
squares). The relationship between BMR, NAVO z an . AVO z with
time are shown. There was a significant inverse relationship between
NAVO l and time but both BMR and SAVO z were independent of
time in both winter- and summer-acclimatized voles. Note that the
time axis was not actually continuous in real time
0
40
0
0
e
0
;,
0
0
3.0
E
0
..: •
20
0
10
••
0
•
0.0
a
15
20
25
30
35
Mass (g)
5.0
4.0
-c
o
'5
!
3.0
o
20
0;,
o
0
10
b
.
•
'"
•
.",
0.0
15
20
25
30
35
Body temperature
T b , recorded immediately after an injection of NA in .
both winter~39.2±OA "C) and summer-acclimatized:~
voles (38.0 ± d.9 DC), increased significantly (P :::; 0.05 in
both cases) compared with that recorded after deter­
minations of BMR which were 37.6 ± 1.3 and 37.6 ±
1.1 DC, respectively (Table 1). There was no significant
change in T b after a saline injection compared with that
recorded after BMR determinations in either seasonal
group of voles. There was also no significant difference
in T b measured after determinations of BMR between
the winter-acclimatized and summer-acclimatized
voles. However, the T b measured after the duplicate
NA injections in the winter-acclimatized voles was sig­
nificantly higher than that recorded in the summer­
acclimatized voles (t = 4.53, P:::; 0.01) (Table 1). T b
was not a significant predictor of either BMR or
NAV0 2 in winter-acclimatized or summer-acclimatiz­
ed voles. However, when the data were pooled across
all seasons and V0 2 measurements, T; was a signifi­
cant predictor of V0 2 (P :::; 0.01). This relationship was
best described by the least squares fit regression; V0 2
(rnl min - I) = -15.0 + 0.448 T b (DC), which explained
15.8% of the variation in V0 2 (Fig. 4).
50
-c
Fig. 4 The relationship between T; and V'Oz in winter- (closed
circles) and summer-acclimatized (open circles) M. aqrestis. There
was a significant positive relationship between T band V'Ol when all
the data were pooled across the seasons
40
Mass (g)
Fig. Ja, b The relationship between V0 2 and BM in (a) winter­
and (b) summer-acclimatized M. aqrestis. There was no significant
relationship between BMR (solid circles) and mass in either summer­
or winter-acclimatized voles. There was a significant positive
relationship between NAVO z (open circles) and mass in both
seasonal groups of voles
was best described by the equation: log NA V0 2 =
- 2.27 +0.961 log BM, which explained 44.6% of the
variation in NA V0 2 (Fig. 3b). There was no significant
relationship between BMR and BM in either winter- or
summer-acclimatized voles.
Seasonal changes in BMR and BM in M. aqrestis
Summer-acclimatized voles unexpectedly showed a sig­
nificant decrease in BMR compared with winter-accli­
matized voles. This contrasts with other previously
published studies on seasonal acclimatization in win­
ter-active small mammals which have recorded an
increase in BMR in summer-acclimatized animals
(Wunder et al. 1977; Heldmaier 1989; McDevitt and
Andrews 1995). It has been suggested that animals with
R.M. McDcvrtt and l.R. Speakman: Summer acclimalizatlon In the tield vole
a high BMR may have J greater reproductive potential
in that they have the potential for a higher level of
biosynthesis which allows them to produce and sustain
more offspring (Me Nab 1980). This suggests, therefore,
that a summer increase in BMR may enable increased
reproductive effort and, conversely, that a summer de­
crease in B1\1R may lower the reproductive potential.
However, Hayes et al. (1992a) found no link between
BMR and reproductive potential in mice and Derting
and McClure (1989) found no link in cotton rats. In
voles, therefore, the lower BMR in summer may not
have reduced their potential for reproductive output
but may simply be a metabolic compensatory response
to having an elevated BMR in the winter. The BM of
M: agrestis in the present study increased during the
process of seasonal acclimatization to naturally in­
creasing photoperiod and T a • As the voles were being
fed ad libitum the increase in BM may simply have
been a response to the ad libitum food supply. How­
ever, the changes in BM recorded here parallel exactly
the seasonal trend found in free-living voles taken from
the same population. That is, the minimum BM was
recorded in winter and the maximum in summer
(McDevitt and Speakman 1994a).
In the present study, winter-acclimatized M. agrestis
maintained a higher BMR compared with summer­
acclimatized voles, thus incurring greater energy costs.
Since there was a positive relationship between BMR
and NA VOl in the voles, a high BMR meant that M.
agrestis was always primed to respond thermogenically
to a thermal challenge, i.e. was more cold tolerant. This
implies that M. agrestis was also able to remain active
throughout the winter (Wunder et al. 1977). These data
suggest that there may be two alternative over-winter­
ing strategies in small endotherms that remain active
over the winter. One strategy is the "energy minimisa­
tion" strategy, characterised by a winter decrease in
BMR and BM seen in many species (Wunder et al.
1977; Heldmaier 1989; Andrews and Belknap 1993;
McDevitt and Andrews 1994). An alternative strategy
may be the "therrnogenically primed" strategy with
a high winter BMR which facilitates a prompt response
to thermal challenges, as in M. agrestis. As an obligate
herbivore M. agrestis does not face the same shortages
in food availability as seed- or insect-eating mammals,
but since its food (almost exclusively grasses) has a rela­
tively low digestibility it must forage on a more regular
basis and is therefore exposed to the cold to a greater
extent (Wunder 1985). In other species, notably the
microtine M. ochrogaster (Wunder 1984), M. brandti
(Liu Zhi-Long et al. 1993) and in the pouched mouse,
S. campestris (Ellison et al. 1992) the same seasonal
trend in BMR has been recorded. As micro tines living
in a similar habitat type to M. agrestis, the same pres­
sures, low food digestibility and long foraging times in
thermally challenging conditions, are likely to be oper­
ating on M. ochrogaster and M. brandti. Saccostomus
campestris, on the other hand, is capable of spontane­
ous torpor in response to low T a and therefore can
afford to have an elevated winter BMR due to the
energetic savings of controlled hypothermia (Ellison
and Skinner 1992). All three species of vole which show
a winter increase in BMR also display a winter reduc­
tion in BM which would reduce energy costs and help
offset the elevated BMR (Wunder 1984: Liu Zhl-Long
et al. 1993; present study).
~
Seasonal changes in NST and thermogenic capacity in
M. agrestis
The capacity for NST in M. agrestis was greater in
winter-acclimatized voles. This was also reflected in the
greater T'; in winter voles in response to NA compared
to summer voles. The rise in T'; that always accom­
panies NA-induced metabolic responses is believed to
contribute to overall heat production by speeding up
the metabolism of the tissues involved in the ther­
mogenic process (Heldmaier et al. 1982; Ellison and
Skinner 1990). We have also found significant seasonal
differences in UCP concentration and cytochrome-c­
oxidase activity in BAT from winter- and summer-ac­
climatized M. agrestis from the same population of
voles (McDevitt and Speakman 1994a). The winter­
acclimatized voles had significantly higher levels of
UCP per BAT depot and per mitochondrial mass com­
pared to the summer-acclimatized voles, which con­
firmed that they had a significantly higher thermogenic
capacity, i.e. potential for increased NST. The same
seasonal trend in acclimatization, i.e. that NST is re­
duced in summer-acclimatized animals compared to
winter-acclimatized animals has been previously re­
ported (Heldrnaier et al. 1982; Feist and Feist 1986;
Klaus et a1. 1988; Haim et al. 199\). In M, agrestis,
having a high NAVO l in winter is required since
a greater capacity for heat production is necessary
when faced with an unavoidably high level of foraging
activity. In the summer, there was probably less call for
the same level of thermogenic response and the energy
saved by switching NST down may perhaps be re­
directed towards reproduction.
Between 40 and 45% of the variation in NAVO l in
M. aqrestis from either group of voles was explained by
variation in BM whilst there was no significant rela­
tionship between BM and BMR. This implies that there
is some component of BM which contributes signifi­
cantly to NAVal but not to BMR. BAT is the major
site for NST in mammals (Heldrnaier and Buchberger
1985) and increases in BAT mass have been linked to
increases in NST in other winter-active endotherms
such as Sorex araneus (Pasanen 1971) and Phodopus
sunqorus (Heldrnaier and Steinlechner 1981). The rela­
tionship between NAVal and BM in the present study
may thus be attributable to the influence of BAT mass.
We have previously found that BAT mass was posi­
tively linked to BMR in M. agrestis from the same
R.M. Mc Ocvn t and J.R. Speakman: Summer acclirnatrzuuon
In
the field vole
population of voles (McDevitt and Speakman 1994a).
In M. aqrestis, a volume-matched dose of saline did not
produce either a thermogenic effect nor an increase in
activity over and above that recorded during BMR
determinations. Thus. the increase in V0 2 observed in
response to NA injection was as a direct result of an
increase in thermogenesis, rather than an effect of in­
creased activity due to handling or the process of ad­
ministering the s.c. injection. The negative relationship
between NA V0 2 and time showed that the stimulation
of NA VOz by NA was only temporary and that per­
haps a sub-optimal dose of NA was given. However,
despite this, clear significant seasonal differences in the
metabolic response to NA were found in M. agrestis in
this study.
grateful to the comments of R. Buffenstein and two anonymous
referees on an origmal draft of tillS manuscript
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Acknowledgements RMM was supported by Natural Environ­
history linked? Funct Eco1 6: 514
mental Research Council project grant NERC G R3/789 L We are