SEASONAL CHANGES IN BODY MASS, COMPOSITION, AND
ORGANS OF NORTHERN RED-BACKED VOLES IN
INTERIOR ALASKA
GERALD
L.
ZUERCHER, DAN[EL D. ROBY, AND ERIC
A.
RExSTAD
Department of Biology and Wildlife, Institute of Arctic Biology, and Alaska Cooperative Fish and
Wildlife Research Unit, University of Alaska Fairbanks, Fairbanks, AK 99775
Present address of GLZ: Kansas Cooperative Fish and Wildlife Research Unit, Division of Biology,
205 Leasure Hall, Kansas State University, Manhattan, KS 66506
Present address of DDR: Oregon Cooperative Fish and Wildlife Research Unit,
Department of Fisheries and Wildlife, 104 Nash Hall, Oregon State University,
Corvallis, OR 97331
Northern red-backed voles (Clethrionomys rUlilus) undergo a pronounced arumal cycle in
body mass and are heaviest in summer and lightest in winter. We trapped voles throughout
1994 to determine how changes in body composition and organ size contributed to this
cycle. Body mass peaked in summer for females and spring for males. Seasonal changes
in body mass were primarily due to changes in lean mass. Body mass was 30-50% lower
in winter than summer, and water content of lean mass was lowest in winter. Total body
fat was low throughout the year but peaked (as with body mass) in spring (males) or early
summer (females). Energy reserves in the fonn of fat depots are apparently most crucial
during the breeding season. A low relative ash content in early summer was possibly due
to a cation imbalance in the diet. Absolute and relative sizes of different body components
contributed to the annual cycle in total body mass. All body components (except brown
adipose tissue) declined in absolute mass, dry mass, and percent water during autumn, with
skeletomuscular components contributing most to loss of total body mass. Most body components declined in proportion to declines in total body mass. However, liver, reproductive
tract, and muscle mass of males declined proportionally more than total body mass; heart,
brain, and bone declined proportionally less. Whole body analyses suggest that the annual
cycle of body mass in C. rutilus is driven by seasonal changes in optimal body size.
Component analyses are consistent with the hypothesis that the primary selective force
driving seasonal changes in body components is the enhanced overwinter survival of C.
rutilus with relatively small body size.
Key words: Clethrionomys rutilus, red-backed voles, body composition, body mass, components, seasonality, Alaska
pared with strict folivores (Hansson, 1990).
Declines in body mass of voles from summer to winter also have been attributed to
declines in total body water associated with
reduced water fraction of lean tissues
(Evans, 1973). In C. rutilus. a dissociation
between turnover of body water and metabolic rate occurs in winter, suggesting reduced ingestion of free water (Feist, 1984;
Holleman et al., 1982). The effect on body
mass of declines in body water, coupled
Microtine rodents, and other small Arctic
mammals, exhibit seasonal changes in sizes
of body and, various organs (Churchfield,
1981; Zegers and Merritt, 1988). Such
changes in body composition are adaptive
by enhancing overwinter survival through
reduction of energy requirements at a time
when food energy is limiting (Fuller, 1969).
Among microtines, greater declines in body
mass have been observed in mixed folivores-granivores and strict granivores COffiJournal of Mammalogy. 80(2):443-459. 1999
443
444
JOURNAL OF MAMMALOGY
with declines in protein, has been documented in several rodents (Sawicka-Kapusta, 1974; Virgl and Messier, 1993).
Despite the presumed adaptive significance of fat depots for overwinter survival,
there is disagreement over the importance
of fat as an energy reserve for small mammals. Fat stores in mouse-sized mammals
are too small to meet energy requirements
for maintenance for >2 days (Bronson et
aI., 1991). For microtines in captivity,
amount of body fat can vary daily depending on the feeding schedule (Bronson,
1987). As a result, it is difficult to detect
seasonal differences in fat reserves. Batzli
and Esseks (1992) document no significant
differences among seasons in the percent
body fat of brown lemmings (Lemmus trimucronatus). Further, fat reserves in winter
were lower in Microtus agrestis despite
their higher energy requirements (Evans,
1973). Fat was the most variable constituent
of body composition in CLethrionomys
gLareo/us, but there was no clear pattern of
seasonal change in fat reserves (SawickaKapusta, 1974).
We documented the annual cycle of
change in body mass and body composition
in C. rutilus. Which body components contribute to recession of body mass in autumn
and increase in spring is unknown. Our hypothesis was that all tissues and organs retained their relative mass in the organism as
body mass changes through the annual cycle. In other words, the exponent of the allometric relationship between log component mass and log body mass was 1.0. Our
alternative hypothesis was that as body
mass changes, relative sizes of various body
components also change. Allometrically,
the exponent of the equation relating log
component mass and log body mass is > 1.0
or < 1.0. Scaling of various organs to body
mass has been investigated in detail for
mammals (Schmidt-Nielsen, 1984), and allometric equations have been derived using
empirical data from a variety of mammals
of differing body mass. For example, liver
mass scales to the 0.87 power and kidney
Vol. 80, No.2
mass to the 0.85 power of body mass. Heart
mass and blood volume scale to the 1.0
power of body mass in a variety of mammals. Metabolic rate, on the other hand,
scales to the 0.75 power of body mass, and
masses of some organs or tissues might be
expected to follow metabolic rate (SchmidtNielsen, 1990). Consequently, an explanation for changes in relative mass of a body
component as total body mass changes
could reside in problems of scaling-a fundamental physiological constraint.
Alternatively, the change in relative mass
of body components with change in body
size may reflect adjustment or acclimatization to different sets of environmental conditions or selective forces in summer as opposed to winter. This would predict that
changes in relative mass of body components are adaptive by reallocating resources
during a particular season. In a highly seasonal environment, the body plan that maximizes fitness is likely to change dramatically with change in season.
The population of northern red-backed
voles used in our study has been studied
previously, and individual weight loss from
summer to winter is well documented
(Whitney, 1976, 1977). The first goal of
this study was to investigate how changes
in the composition of carcasses of voles
contribute to seasonal changes in total body
mass. To accomplish this, we tested the following hypotheses: 1) body composition
(percentage of water, fat, ash, and ash-free
lean dry mass) does not change with season
or in relation to change in total body mass;
2) seasonal patterns of change in body mass
and composition do not differ between sexes; and 3) body composition in summer
does not differ between subadults and
adults.
Our second objective was to describe
seasonal changes in body components as
they relate to the annual cycle in overall
body mass and composition of C. rutilus.
Seasonal changes in size of various body
components were examined in terms of absolute mass, relative mass, and percent wa-
May 1999
ZUERCHER ET AL-BODY COMPOSITION OF VOLES
ter. We sought to identify body components
primarily responsible for the annual cycle
in total body mass and body composition in
C. rutilus. We also sought to detennine if
seasonal changes in percent water of total
lean mass were a product of changes in water content of a few body components, or a
generalized pattern for all tissues. If relative
size and composition of some body components were not conserved throughout the
annual cycle of body mass, we hoped to
gain some insight into the potential adaptive significance of those differences. We
were interested particularly in how those
changes relate to survival and reproduction
of a small endotherm in a highly seasonal
environment.
MATERIALS AND METHODS
Free-ranging C. rutilus were trapped during
each of six predetermined phases of the annual
cycle in 1994 (late winter, 21 January-16 February; spring, 21 March-25 April; early sununer,
25 May-25 June; late summer, 15 July-IS August; autumn, 20 September-lO October; early
winter, 1 December-30 December) on the campus of the University of Alaska Fairbanks in interior Alaska (64°N, 14rW). Habitat at trap sites
was a boreal forest mixture of black spruce (Picea mariana), white spruce (P. glauca), paper
birch (Betula papyrijera), and alder (Alnus crispus). During spring, early and late summer, and
autumn, 5- by 6.25- by 16.5-cm Shennan live
traps and 6- by 8- by 24-cm U gglan multiple
capture live traps were baited with a mixture of
peanut butter and oatmeal and examined twice
daily (0600 and 1800 h). Newly trapped voles
were weighed with a Pesola spring scale (±0.5
g). In the laboratory, voles were euthanized with
Halothane, weighed on a Mettler analytical balance (±0.1 mg), and placed in a freezer at
- 20°C until di$section and body composition
analyses could be performed. During early and
late winter, snap traps baited with a mixture of
peanut butter, oatmeal, and vegetable oil were
set and examined three times daily (0600, 1300,
and 2000 h).
Reproductive activity in females was determined by the presence of embryos. lactation, or
open vagina. Active males were determined by
descended testes (McCravy and Rose, 1992) of
445
>5.0 rom in length. Although that index to reproductive activity in males was somewhat arbitrary, few reproductive males (6 of 63) had
testes 4.5-5.5 tnm. For those individuals, comparison of morphological measures (i.e., body
length and mass) to other males caught during
the same trapping period and at the same trapping site aided in determination of reproductive
status. Also, Whitney's (1976) criterion for distinguishing subadults « 17 g) from adults (2: 17
g) during early and late sununer was used. All
protocols involving live animals were approved
by the Institutional Animal Care and Use Committee at the University of Alaska Fairbanks.
Wet mass before dissection was recorded
(::to.1 mg) using a Mettler analytical balance.
and each carcass was dissected into 17 components (brain, head, heart, liver, kidneys, stomach,
small intestine, cecum, large intestine, reproductive tract, right hind quarter, muscle of left hind
quarter, bone of left hind quarter, integument,
subcutaneous white adipose tissue, brown adipose tissue, and the remaining carcass). Each
component was placed in a pre-weighed aluminum pan and weighed on a Mettler analytiCal
balance to detennine wet mass (±0.1 mg). Each
component was then placed in a forced-air convection drying oven (ca. 60°C), dried to constant
mass, and reweighed to detennine dry mass.
Water content of each component was calculated
from the difference between wet and dry masses. For each component, absolute wet mass, absolute dry mass, relative wet mass (percent lean
body mass), and relative dry mass (percent lean
dry body mass), as well as percent water in each
component were calculated.
Dissected components were combined and
ground using a mortar and pestle. Each ground
carcass was divided into 2-4 subsamples, each
of 2.0-2.5 g, so that the entire carcass was extracted to determine total body fat. Total fat was
extracted from samples using a Soxtec HT-12
soxhlet apparatus (Tecator, Inc., Herndon, VA)
with petroleum ether as the solvent system (Dobush et al., 1985). Lean body mass (LBM) was
determined from the difference between total
body mass (measured immediately after death)
and total body fat. The remaining lean dry matter was placed in a glass scintillation vial and
burned in a muffle furnace (ca. 500°C for 24 h)
to determine ash content. Absolute values and
percentages of total body mass for water, fat,
ash, and ash-free lean dry matter (mostly pro-
446
Vol. 80, No.2
JOURNAL OF MAMMALOGY
TABLE I.-Comparisons of seasonal body mass of male and female Clethrionomys rutilus trapped
on the campus of the University of Alaska Fairbanks during 1994. Due to absence of significant
differences, voles caught during early and late summer sessions were combined into "Summer" and
those caught during early and late winter sessions were combined into "Winter." Body mass is given
as mean ± SD (n).
Analysis of Variance
Body mass (g)
Season
Males
Spring
Summer
Autumn
Winter
23.00 ± 1.92 (6)
21.09 ::t 2.66 (14)
18.04 ::t 1.92 (5)
15.00 ± 1.94 (14)
F-statistic (dJ.)
Females
20.42 :t:: 1.92
30.58 :!:: 1.20
19.24 ± 2.10
14.71 ± 0.62
tein), and percent water of lean mass were calculated for each carcass.
Results from the analysis of whole carcass attributes were used to investigate how changes in
body composition contribute to changes in total
body mass. Analysis of variance (ANOVA) was
used to determine differences in body mass between sexes for each season. Twelve variables
describing whole animal composition were analyzed for differences among seasons, sexes, reproductive statuses, and their interactions. Five
variables were analyzed using ANOVA: total
body mass; total body water; total ash-free lean
dry mass; total body ash; and total body fat.
Seven percentage and index variables were analyzed using analysis of covariance (ANCOVA)
based on recommendations by Packard and
Boardman (1988): water as a percentage of lean
mass; water as a percentage of total body mass;
ash-free lean dry mass as a percentage of total
body mass; ash as a percentage of lean dry
mass; ash as a percentage of total body mass;
total fat:lean dry mass (fat index); and total body
fat as a percentage of total body mass. A square
root of the arc sine transfonnation (Zar, 1984)
was applied to all percentages before analyses.
When ANOVA or ANCOVA revealed significant seasonal differences, seasonal means were
compared using SAS Proc GLM and Duncan's
multiple range test (SAS Institute Inc., 1993).
Duncan's test was selected based on an evaluation by Canner and Swanson (1973). For all
Duncan analyses, degrees of freedom (d./) were
5, 33 for females and 5, 42 for males and sample
sizes (n) were 39 for females and 48 for males.
Analyses of change in seasonal body composition were performed on adults only and were
separated by sex. Subadults were analyzed only
during early and late summer because they could
(9)
(10)
(16)
(13)
7.630
35.53
1.091
0.125
(1,13)
(1,22)
(1,19)
(1,25)
P
0.016
< 0.001
0.124
0.727
not be distinguished in other seasons. ANOVA
and Duncan's tests compared body mass and
body composition between adults and subadults
for early and late summer only.
Results from the analysis of body components
were used to infer how changes in different
components contributed to changes in total body
mass. Each component was analyzed using ANCaVA to detennine differences related to seasons, sex, reproductive status, and interactions
among those three categories. All overwintering
individuals were considered adults for those
analyses. Changes in body components among
seasons were investigated using SAS Proc GLM
and Duncan's multiple range test (SAS Institute
Inc., 1993). Absolute wet mass, absolute dry
mass, relative wet mass, relative dry mass, and
percent water for each component were tested
for seasonal differences. Contribution of each
component to the decline in body mass from late
summer to early winter was detennined by calculating the percent change in total body mass
due to the change in each component. The log
of component mass was regressed on the log of
total body mass to detennine allometric relationships of brain, liver. muscle of hind quarter, bone
of hind quarter, and brown adipose tissue components to total body mass. Data on body components were separated by sex in these analyses.
Statistical significance was set at P < 0.05 for
all tests.
RESULTS
Whole body composition.-Mean seasonal body mass differed between sexes in
spring and early and late summer but not
autumn and early and late winter (Table 1).
Sexes differed seasonal in mean total body
ZUERCHER ET AL-BODY COMPOSITION OF VOLES
May 1999
A)
c
B
___A"-___ -2-.
~
J5
,
10
~
,,
,
, ,
,
b
b
0
•
DWaterDAFLDM .Ash 0 Fat
~
0
f-
')
35
-
c
- B
A
C
30
"
20
..
15
10
,
a
c
a
c
a
b
c
oU-~~~~~~~~~L
Late Spring Early Late Autumn Early
Summer
Winter
Winter
FIG. l.-Seasonal mean body mass of adult
A) female and B) male Clethrionomys rutilus
separated into constituents (fat, ash, ash-free
lean dry mass, and water). Capital letters indicate Duncan's multiple comparisons of total
body mass; lower-case letters indicate Duncan's
multiple comparisons of the four constituents.
mass (females, F ~ 34.54, P < 0.0001;
males, F ~ 17.07, P < 0.0001; Fig. I). Seasonal patterns in total body mass were different between sexes. Mean total body mass
of females increased from late winter to a
peak. in early'Summer, followed by a decline
to early winter. Total body mass of females
in early summer was roughly twice that of
females in early winter. Total body mass of
males increased from late winter to a peak
in spring. Although not significantly different, average total body mass of males in
early summer was lower than in spring, followed by a significant decline in total body
447
mass (ca. 30%) from late summer to early
winter, as in females. Total body masses of
both sexes in early winter and late winter
were not different but were distinguishable
from body mass in all other seasons. Total
body mass of subadults was lower than
adults for both sexes during early and late
summer (Table 2). Adult females weighed
nearly twice that of subadult females, but
adult males weighed ca. 20% more than
subadult males.
Seasonal differences in total body water
were apparent for both sexes (females, F =
33.59, P < 0.0001; males, F ~ 18.11, P <
0.0001; Fig. 1). Duncan groupings showed
the same pattern of seasonal change as in
total body mass. Seasonal changes in total
body mass were primarily a function of seasonal changes in total body water. Water as
a percentage of lean mass also showed seasonal differences in sexes (females, F =
6.98, P < 0.0001; males, F ~ 9.41, P <
0.0001). The ANCOVA for water as a percentage of lean mass, and the remaining six
whole body composition variables resulted
in a non-significant interaction effect (body
mass X season; P > 0.05). Patterns for seasonal change in water as a percentage of
lean mass were similar to the patterns of
change in total body mass, with peaks in
early summer and lows in early winter (Table 3). To determine the percentage of loss
in total body mass from late summer to early winter that was due to loss of water content in lean tissues, a comparison was made
between actual body water content and potential body water content, had water as a
percentage of lean mass remained constant.
The difference between actual and potential
body water content for females was 0.75 g,
which accounted for only 4.5% of the decline in total body mass from summer to
winter. The difference for males was 0.60
g, which accounted for only 9% of the decline in total body mass. Seasonal differences in percent water of total body mass
for sexes differed (females, F = 7.81, P <
0.0001; males, F ~ 5.70, P < 0.0001; Fig.
2).
448
JOURNAL OF MAMMALOGY
Vol. 80, No.2
TABLE 2.-Comparisons of body mass and body composition between adult and subadult Clethrionomys rutilus during summer. AFLDM = ash-free lean dry mass. Sample sizes for each class
within season are in parentheses. Mean:!: SD provided.
Body composition
Season-class
Body mass (g)
% water
% AFLDM
% ash
% fat
30.62 ± 4.91
12.13 ± 1.05**
74.68 ± 2.06
73.58 ± 0.82
20.38 ± 1.59
21.16 ± 0.92
4.05 ± 0.67
4.52 ± 0.67
4.23 ± 1.77
3.80 ::!: 1.26
20.97 ± 2.17
16.49 ± 1.23*
73.13 ± 0.79
72.43 ± 1.89
21.46 ± 0.13
21.47 ::!: 1.58
4.43 ± 0.68
4.75 ± 0.28
4.22 ± 1.75
5.88 ± 1.83
30.51 ± 4.15
15.46 ± 1.46**
73.89 ± 2.48
71.76 ± 1.84
18.48 ::!: 0.55
19.94 ± 1.55
7.19 ± 2.33
7.72 ± 1.31
2.37 ± 0.80
2.49 ± 1.07
21.27 ± 3.65
16.57 ± 1.95*
71.57 ± 0.91
71.85 ± 1.71
19.47 ± 0.54
19.71 ± 1.62
8.37 ± 1.32
7.68 ± 1.76
2.51 ± 0.46
3.26 ± 1.52
Early summer
Females
Adults (9)
Subadults (4)
Males
Adults (6)
Subadults (6)
Late summer
Females
Adults (5)
Subadults (11)
Males
Adults (4)
Subadults (8)
* P < 0.05 and ** P < 0.01 for comparison of adults and subadults by sex within a season using a (-test.
Seasonal differences in ash-free lean dry
mass (mostly protein) were significant for
both sexes (females, F = 31.94, P <
0,0001; males, F = 10,98, P < 0,0001; Fig.
1). Seasonal patterns in ash-free lean dry
mass for females were the same as for total
body mass and total body water, with peaks
in early summer and minima in winter. In
males, mean ash-free lean dry masses also
exhibited the same seasonal trends as total
body mass and total body water, but there
was slightly more overlap in Duncan's multiple comparisons. Although differences occurred, ash-free lean dry mass as a percentage of total body mass remained fairly
consistent among seasons for both sexes
(females, F = 2.53, P < 0.0240; males, F
= 3.08, P < 0.0053; Fig. 2).
Seasonal differences occurred in total
body ash for both sexes (females, F == 6.56,
P < 0.0002; males, F = 4.53, P < 0.0002;
Fig. 1). The seasonal pattern in total body
TABLE 3.-Summary of body composition of male and female Clethrionomys rutilus indicating
seasonal changes in: water as a percentage of lean body mass (LBM), ash as a percent of lean dry
mass (LDM), fat index (total body fat [TBF}:lean dry mass), brown adipose tissue (BAT) index (total
BAT:lean dry mass). Sample sizes (n) were 39 for females and 48 for males.
Water as % LBM
Ash as % LDM
Fat index
BAT index
Season
M
F
M
F
M
F
M
F
Late winter
Spring
Early summer
Late summer
Autumn
Early winter
p,
68.73
71.56
73.13
71.57
70.85
67.49
<0.01
69.71
69.43
74.68
73.89
71.19
68.31
<0.01
28.67
26.89
17.07
29.98
26.53
31.61
<0.01
27.19
28.47
16.49
27.43
24.23
33.26
<0.01
0.155
0.156
0.150
0.176
0.105
0.055
0.003
0.154
0.137
0.141
0.166
0.081
0.054
0.005
0.Q15
0.Q11
0.006
0.004
0.008
0.007
<0.01
0.018
0.008
0.005
0.004
0.005
0.007
0.015
• P-values for the effect of
~eason
from the analysis of covariance for each body composition variable.
May 1999
ZUERCHER ET AL.-BODY COMPOSITION OF VOLES
AJ
5
100
:§ 4
1;
,..
~
80
m 2
60
•• 40
:.•
,..
"m
II0
D%Water D %AFLDM
.%Ash D %Fat
~
i
Pregnant
Non Pregnant
or Lactating and Non Lactating
Females
I
Males
Reproductive C lass
BJ
FIG. 3.-Total body fat in three reproductive
classes (pregnant or lactating females, non-pregnant and non-lactating females, and males) of
c
• 100
~
~
••
0
0
0
I0
.'!
•
20
]
Cl
•
•
•
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0
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."
0
449
Clethrionomys rutilus.
SO
60
40
20
O U-~~~~JLL-~L-~L-~
Late Spring Early Late Autumn Early
Wi nter
Summer
Winter
FIG. 2.-Relative composition of adult A) female and B) male Clethrionomys rutilus by season. Lower-case letters indicate Duncan's multiple comparisons of the four constituents.
ash was similar between sexes, with maxima in late summer and minima in early
summer and late winter. In early summer,
the minimum values of total body ash between sexes were noteworthy because total
body ash was opposite of peaks in total
body mass, total body water, and ash-free
lean dry mass during that season (Fig. 1).
Ash as a percentage of lean dry mass differed among' seasons between both sexes
(females, F = 6.45, P < 0.000 I; males, F
= 3.62, P < 0.0017; Table 3), peaking in
early winter and lowest in early summer.
Percent ash of total body mass (Fig. 2) differed among seasons (females, F = 8.00, P
< 0.0001; males, F = 5.24, P < 0.0001)
and exhibited the same seasonal pattern between sexes.
Seasonal means for total body fat were
consistently low « 1.0 g) with low variance
throughout the year, except for pregnant or
lactating females that had relatively high total body fat. There were seasonal differences in total body fat between sexes (females, F = 6.31, P < 0.0003; males, F =
7.19, P < 0.0001; Fig. 1). Total body fat in
females peaked in early summer, but fat
content in males peaked in spring. Seasonal
minima in total body fat occurred in early
winter for both sexes. The fat index, the
ratio of total body fat to lean dry mass, also
showed seasonal differences (females, F =
3.90, P = 0.0021; males, F = 3.46, P <
0.0022; Table 3), with seasonal peaks in
late winter for females and in spring for
males. Both sexes had the lowest seasonal
means in early winter. Fat as a percentage
of total body mass showed seasonal differences for both sexes (females, F = 3.74, P
= 0.0025; males, F = 3.05, P < 0.0056;
Fig. 2) with high values early in the calendar year and lower values later in the calendar year. Total body fat was plotted
against different reproductive classes (pregnant or lactating females, non-pregnant and
non-lactating females, and males) to investigate potential correlations (Fig. 3). Only
450
JOURNAL OF MAMMALOGY
pregnant or lactating females contained
> 0.75 g of fat.
Body mass and composition of subadults
were compared, using a t-test, with those of
adults only in sununer. Differences occurred in body mass but there were no differem:e s in body composition between
adults and subadults within sex (Table 2).
Contribution of different organs.-The
ANCOV A for different organs resulted in
nonsignificant interactions (body mass and
season; P > D.OS). Most organs changed
seasonally but remained proportionally the
same (bead, kidneys. stomach, small intestine, cecum, large intestine, integument,
subcutaneous white adipose tissue, and the
remaining carcass).
Seasonal differences occurred for sexes
in wet mass of the muscle of the hind quarter (females, F = 16.95, P < 0.0001; males,
F = 20.19, P < 0 .0001 ; Fig. 4) and percent
water of the muscle of the hind quarter (females, F = 4.45, P = 0.0009; males, F =
8.43, P < 0.0001). Percent water was highest in early summer and lowest in early
winter for both sexes. Relative wet mass of
leg muscle showed seasonal differences (females, F = 2.37, P = 0.0342; males, F =
7.36, P < 0 .0001). Relative muscle mass
was highest in spring and early summer for
females and in spring only for males. Lowest relative muscle mass occurred in early
winter for both sexes. The allometric equation relating log mass of hind quarter muscle to log body mass for females had an
exponent tbat was not different from 1.0 (bo
= 0 .9906, SE = 0.0739). The allometric
equation for males had a slope significantly
greater than 1.0 (bo = 1.3782. SE =
0.0929) . That indicated that seasonal
changes in mu scle mass of males were proportionally greater than changes in total
body mass; seasonal changes in muscle
mass of females were proportional to
changes in total body mass.
Seasonal differences in wet mass of bone
in hind quarters were apparent for females
(F = 6.04, P = 0.0004) and males (F =
3.40, P = 0.0110; Fig. 4). However, there
Vol. 80, No.2
A)
1
o
DMuscle WaterDMuscle Dry Mass
• Bone Water 0 Bone Dry Mass
B)
0.2
OUL~~~~~~~~
Late Spring Early Late A utumn Ea rl y
WI nter
Summer
Winter
FiG. 4.-Mean water and dry matter content
of hind quarter muscle and bone in adult A) female and B) male Clethrionomys rutilus by season. Lower-case letters indicate Duncan's multiple comparisons.
were no seasonal differences in percent water of bone for either sex. Sexes showed
seasonal differences in relative wet mass of
bone (females, F = 14.91, P < 0.0001;
males, F = 2.99, P = 0.0082). The allometric equation relating log bone mass to
log body mass had an exponent significantly < 1.0 (females, bo = 0.4453, SE =
0.0570; males, bo = 0.5274, SE = 0.0820),
indicating that seasonal changes in bone
mass were proportionally less than changes
in total body mass.
Of the four internal organs examined
May 1999
ZUERCHER ET AL.-BODY COMPOSITION OF VOLES
(liver, heart, kidneys, and spleen), only liver
showed a decline in mass that accounted for
>5% of the overall decline in total body
mass in autumn. The liver also was the largest internal organ, regardless of season. Declines in liver mass from late summer to
early winter accounted for 8% of the decline in overall total body mass for females
and 7% for males. There were seasonal differences in wet mass of liver for females (F
= 16.50, P < 0.0001) and males (F = 6.08,
P = 0.0002). Percent water of liver showed
no seasonal changes in either sex. Relative
wet mass of liver differed among seasons
in females (F = 2.26, P = 0.0426) but not
in males (F = 1.62, P = 0.1324). Relative
wet mass of liver was highest in early summer and lowest in late winter for females,
but there was no clear seasonal pattern for
males. The allometric equations relating log
liver mass to log body mass were different
between the sexes. The exponent of the allometric equa~ion for liver mass of females
(b o = 1.5027, SE = 0.1198) was significantly > 1.0 and indicates that seasonal
changes in liver mass were proportionally
greater than changes in total body mass.
The exponent of the allometric equation of
liver mass of males was indistinguishable
from 1.0 (b o = 0.9094, SE = 0.1230), indicating that seasonal changes in liver mass
were proportional to changes in total body
mass.
The decline in mass of reproductive organs accounted for 15% of the decline in
total body mass for females in autumn and
9% of the decline for males (Table 4).
There were seasonal differences in wet
mass of reproductive tracts for females (F
= 55.38, P < 0.0001) and males (F =
23.36, P < 0.0001; Fig. 5A and 5B). Seasonal changes in mass of reproductive tract
were accompanied by changes in percent
water for females (F = 7.36, P < 0.0001)
and males (F = 4.63, P < 0.0002). Percent
water in reproductive tissues was highest in
early summer for both sexes. Lowest percent water in reproductive tissues was in
late winter for females and in early winter
451
TABLE 4.-Relative contribution of different
body components to the overall decline in body
mass of Clethrionomys rutilus from late summer
to early winter. The skeletomuscular components include head, hind quarter, muscle of the
hind quarter, bone of the hind quarter, and the
remaining carcass; the gastrointestinal components are the stomach. small and large intestines, and cecum; skin includes the pelage.
Percentage of
change in total mass
Body component
Females
Males
Skeletomuscular components
Gastrointestinal components
Reproductive tract
Liver
Skin
42
9
9
7
15
36
IS
15
8
7
for males. Seasonal differences in relative
wet mass of reproductive tract also were
observed (females, F = 3.54, P = 0.0039;
males, F = 36.33, P < 0.0001).
Wet mass of the brain differed among
seasons for females (F = 18.16, P <
0.0001) and males (F = 18.76, P < 0.0001;
Fig. 5C and 5D). Brain mass was highest
in summer and lowest in winter for both
sexes. Seasonal changes in brain mass were
associated with changes in percent water of
the brain (females, F = 2.58, P = 0.0231;
males, F = 20.78, P < 0.0001). Percent water of the brain was highest in early summer
for both sexes and lowest in early winter
for females and late winter for males. Relative wet mass of brain also differed among
seasons (females, F = 37.80, P < 0.0001;
males, F = 18.66, P < 0.0001). Relative
wet mass of brain, however, was highest in
early winter (both sexes) and lowest in early summer for females and in spring for
males. Thus, relative brain mass peaked at
about the time when absolute brain mass
was at a minimum. The allometric equation
relating log brain mass to log body mass
had an exponent significantly <1.0 (females, bo = 0.3088, SE = 0.0372; males,
b o = 0.3041, SE = 0.0856), indicating that
seasonal changes in brain mass Were pro-
JOURNAL OF MAMMALOGY
452
A
I~=:~""'I
AJ
1
Vol. 80, No.2
BJ
1
A
0.8
0.6
-
B
~
Cl
/J)
/J)
OS
==
....
0.'
C
C
C
0.2
0.2
0
0
B
B
B
C
CI)
C
0
Co
E
CJ
L~
0.7
A
AB
OJ
C
CD
A
AB Be
-
0
• Brain Dry Mass
o Brain Water
0
(J
Late Spring Early late Autumn Early
Winter
Summer
Winter
late Spring Early Late Autumn Early
Winter
Summer
Winter
FlO. 5.-Mean water and dry matter content of A) female and B) male reproductive tracts of
Clethrionomys nttilus and wet and dry mass of C) female and D) male brains of C. rutilus by season.
Capital1etters indicate Duncan's multiple comparisons for mean wet mass. Lower~case letters indicate
Duncan's multiple comparisons of brain dry mass and water content.
portionally less than changes in total body
mass. Seasonal changes in brain mass also
were proportionally less than apparent
changes in metabolic rates of the whole animal; the exponent of the allometric equation relating log brain mass to log body
mass was significantly less than that of the
equation relating log metabolic rate to log
body mass (0.75-Schmidt-Nielsen, 1990).
Absolute mass of brown adipose tissue
(BAT) was higher during the combined
winter seasons than during the combined
summer seasons. The BAT index (BAT
mass:lean dry mass) showed seasonal differences (females, F = 6.92, P < 0.0001;
males, F = 2.78, P = 0.0097; Table 3). For
both sexes, seasonal peaks occurred in late
winter and seasonal lows occurred in late
summer. The allometric equation relating
log BAT mass to log body mass had a negative exponent (females, b o = -0.3305, SE
= 0.1372; males, bo = -0.3063, SE =
0.1456), indicating that BAT mass was relatively greater in smaller individuals.
DISCUSSION
Whole body composition.-The observed
annual cycle of body mass (Fig. 1) for C.
rutilus supports the conclusions from earlier
studies on this species in interior Alaska
(Whitney, 1976, 1977). Although part of
the apparent decline in total body mass
from late summer to early winter results
from an influx of young individuals in the
May 1999
ZUERCHER ET AL.-BODY COMPOSITION OF VOLES
population, all individuals decline in body
mass from late summer to winter (Whitney,
1976). The adaptive significance of this
phenomenon has been discussed earlier
(Boyce, 1978; Ellison et al., 1993; Merritt
and Zegers, 1991), but the absence of data
on body constituents that contribute to this
decline has made interpretation difficult. A
prevailing theory is that reduction of body
mass allows a decrease in total energy requirements of the individual, despite the increase in mass-specific metabolic rate due
principally to increased thennostatic costs
(Fuller, 1969). Smaller body size also reduces absolute quantity of resources required during potential periods of food limitation (Boyce, 1978). This applies not only
to rodent species in northern boreal forests
but also to rodents in highly seasonal temperate forests (Ellison et al., 1993).
The difference in body mass during summer between adults and subadults is expected because body mass is a factor in distinguishing these two classes (Whitney,
1976). Surprisingly, there were no differences in body composition between the two
age classes, suggesting that the selective
forces driving seasonal changes in body
composition, such as quality and availability of food, impinge on young-of-the-year
soon after weaning.
Seasonal fluctuations in total body water
of C. rutilus mimic seasonal patterns in
overall body mass. Duncan's multiple comparisons of water as a percentage of body
mass indicated that individuals in winter
had lower relative water contents than in
summer (Fig. 2). This may be related to
lower body water turnover in C. rutilus during winter stemming from lower intake of
free water (Holleman et al., 1982).
Dehydration of small mammals in winter
has been reported previously (Churchfield,
1981; Hayward, 1965; Myrcha, 1969). Hayward (l965) noted declines in water as a
percentage of lean mass in six species of
Perornyscus from summer to winter. He
considered that trend to be a result of increased pelage mass in winter, reflected in
453
an increase in percent protein. Water content of C. glareolus in Poland exhibited a
similar seasonal pattern but was not considered significant (Pucek, 1973). Declines in
water content and protein content are considered the most influential components of
overall declines of body mass in C. glareolus (Sawicka-Kapusta, 1974). In Microtus agrestis, water content was lowest in
winter and coincided with lowest body
mass (Evans, 1973).
Declines in body mass of shrews (Sorex)
in winter also were attributed to dehydration (Churchfield, 1981; Myrcha, 1969).
According to Myrcha (1969), lower hydration state in shrews is adaptive and associated with a reduction in cellular metabolism. Nonetheless, Churchfield (1981) concluded that although body water contents
are statistically lower in winter, their reduction is of insufficient magnitude to enhance
fitness. For C. rutilus in this study, loss of
hydration in lean tissues accounted for only
4.5% of the total decline in body mass of
females from late summer to early winter
and 9% of males. Thus, although lean tissues of C. rutilus had a lower water content
in winter compared with summer, changes
in water content are relatively minor in the
context of total body mass, which was reduced by 30% in males and >50% in females (Table I).
Changes across seasons between ash-free
lean dry mass and water observed in this
study were similar to those for protein and
water in muskrats (Ondatra zibethicusVirgl and Messier, 1993). For this reason,
total water is considered a good predictor
of total protein. Seasonal changes in those
two components explained nearly all seasonal variation in total body mass of rodents (Sawicka-Kapusta, 1974; Virgl and
Messier, 1993; this study).
Ash content did not follow the same patterns of seasonal change as for water or ashfree lean dry mass (Fig. 1). The observed
decline in ash content in early sununer for
both sexes likely was due to the mineral
content of the diet. Diets of C. rutilus in
454
JOURNAL OF MAMMALOGY
late spring and early summer include the
new growth on twigs of quaking aspen
(Populus tremuloides) and horsetail stalks
(Equisetum pratense-Grodzinski. 1971).
New plant growth is known to be high in
K+ (Weeks and Kirkpatrick, 1976). An excess of K + is thought to disrupt the balance
of Na+ and other cations by interfering with
Na+ retention in kidneys and promoting increased fecal loss of Na+ (Weeks and Kirkpatrick, 1976). The similar spring-early
summer decline in total content of body ash
reported in muskrats (Virgl and Messier,
1992) appears to be a response to diets consisting largely of new green foliage.
Seasonal fluctuations in fat content suggest that energy reserves were more important for breeding and rearing of young than
as a source of energy during winter. This is
emphasized by the presence of >0.75 g of
fat only in pregnant or lactating females
(Fig. 3). In C. mtiIus, fat reserves of males
peaked in spring (Fig. IS), coincidental
with maximum total body mass at a time
when male-male aggression should be intense. The seasonal peak in fat reserves of
females occurred in early summer when
pregnancy was most prevalent (Fig. lA).
Fat reserves of females in late summer, a
period of pregnancy and lactation, were
lower than early summer-a decline likely
due to the high proportion of lactating females, similar to the findings of other studies on rodents (Virgl and Messier, 1992).
This is supported by the relatively low energetics cost of pregnancy compared with
lactation (Robbins, 1983).
Fat reserves in mouse-sized animals are
too small to offer significant energy in winter (Bronson et al., 1991). Fat reserves in
M. agrestis in winter also are low (Evans,
1973). When maintained at moderately cool
temperatures (22°C and 11°C) and allowed
only nocturnal feeding opportunities, female laboratory mice (Mus musculus) exhibit dramatic daily fluctuations in fat reserves (Bronson, 1987).
Total body fat is considered an indicator
of nutritional condition because fat reserves
Vol. 80, No.2
are related to overall energy balance (Robbins, 1983). Moreover, fat storage should be
favored by natural selection if food shortages are regularly experienced (Batzli and
Esseks, 1992). Changes in fat reserves accounted for 45% of variability in body mass
of California voles, with no clear seasonal
pattern of overall body size or total body
fat (Lidicker and Ostfeld, 1991). Thennoregulatory costs to voles increase dramatically as ambient temperatures decline
(Feist, 1984), and these costs must be
matched by increased food consumption or
catabolism of endogenous reserves. If an
individual has allocated surplus intake to fat
deposition, it will have an advantage in
coping with extreme temperatures (Bronson, 1987).
The difference in fat reserves from early
winter to late winter suggests that although
stored fat is not a major energy source during winter, fat reserves may be influenced
by changing conditions beneath the snow.
Changes in snow cover alter the subnivean
environment, affecting temperature regimes
(Marchand, 1991). A deep insulative snow
cover might promote higher fat reserves
compared with a shallow snow cover.
In conclusion, the observed annual cycle
in body mass of C. mtilus resulted primarily from changes in lean body mass. Body
water and ash-free lean dry mass declined
from early summer to early winter, especially in females, contributing to the autumn
decline in body mass. Subsequent increases
in body mass during spring were likewise
driven by increases in body water and ashfree lean dry mass. Body masses of males
peaked in spring when male-male competition for mates may be intense (Vii tala,
1987); body masses of females peaked during summer when pregnancy and lactation
occur. The decline in total body water in
autumn was associated with a decline in
water as a percentage of lean mass. Total
body ash remained nearly constant across
seasons, except for early summer when K+
content of new green forage may have a
negative effect on cation retention. This ap-
May 1999
ZUERCHER ET AL.-BODY COMPOSITION OF VOLES
parent imbalance, indicated by the decline
in ash content in early summer, was reversed by late summer. Body fat varied independently of the three constituents of
lean mass. Peak fat content in males occurred in spring, possibly as an energy reserve for breeding. Fat reserves of females
peaked in early summer when all adult females in the sample were pregnant. Finally,
the seasonal pattern of change in total body
mass was associated with changes in body
composition that differed between sexes but
not between subadults and adults.
Contributions of different organs.Changes in mass of certain body components in response to changes in photoperiod, temperature, food quality, and snow
depth have been described for several species of rodents. Changing photoperiod is
known to lead to changes in body composition and physiology of voles and mice
(Blank and Ruf, 1992; Feist and Feist,
1986). Specifically, the reproductive tract of
female northern red-backed voles (c. rntiIus) regresses when stimulated by short
photoperiod in laboratory studies (Feist and
Feist, 1986). Regression of reproductive tissues before winter pennits reallocation of
resources to maintenance and activity.
The investigation of seasonal dynamics
in mass and water content of different body
components revealed several distinct trends
in relation to body mass. These trends indicate that the largest body components
(skeletal muscle, gastrointestinal tract, skin,
liver) contributed most to seasonal changes
in body mass (Table 4). All components followed the seasonal pattern of change in total body mass by declining in autumn and
increasing in spring, with the exception of
BAT. For example, brain and heart showed
seasonal changes in mass but contributed
little to the annual cycle in overall body
mass chiefly because of their small relative
sizes.
Seasonal changes in total mass of skeletal muscle were indicated by changes in
muscle of the hind quarter and remaining
carcass. Acclimatization to winter condi-
455
tions is associated with declines in the size
of muscle tissue (red and white muscle fibers) in small rodents (Wiclder, 1981). This
is important because muscle tissue is the
site of shivering thennogenesis and a contributor to non-shivering thermogenesis
(Jansky and Hart, 1963), Results of regressions of log muscle mass of the hind quarter
versus log body mass indicated that
changes in muscle had a proportionally
greater effect on the overall changes in
body mass for males compared with females.
Declines in bone mass through resorption
have been described mainly for crania but
also are known to occur in trunk vertebrae
(Hyviirinen, 1984). Decline in cranial mass
has been described as a response to the decline in brain size (Quay, 1984). Results of
regressions of log bone of the hind quarter
versus log body mass indicated a conservation of bone mass relative to body mass
despite seasonal changes in C. rntilus.
The seasonal decline in the five combined skeletomuscular components (head,
hind quarter, muscle of the hind quarter,
bone of the hind quarter, and remaining carcass) contributed 36% to the decline in total
body mass for adult females and 42% for
adult males. in autumn (Table 4). Comparison between declines in muscle mass of the
hind quarter and bone mass, relative to declines in mass of hind quarter, indicated that
muscle represented 85-95% of the decline
in mass of the hind quarter. Skeletal muscle
contributed more to the decline in skeletomuscular components and total body mass
than bone. The seasonal pattern of change
in skeletomuscular components was very
similar to that of total body mass.
Seasonal patterns in liver mass of voles
have been documented previously (Hyvarinen, 1984; Sealander, 1969), Results from
our study were similar to those of Sealander
(1966), who showed relative and absolute
declines in liver mass of C. rutilus in autumn. Hyvannen (1984) documented absolute declines in liver mass of C. glareolus,
but noted that relative to body mass, the
456
JOURNAL OF MAMMALOGY
liver remained stable through all seasons.
Results of regressions of log liver mass versus log body mass indicated that seasonal
changes in liver mass in females were proportionally greater than changes in total
body mass.
The regression of reproductive organs in
winter, whether stimulated by decreasing
temperature or decreasing photoperiod, is
well-documented in many rodents (Blank
and Ruf, 1992; Feist and Feist, 1986). In
our study, dramatic seasonal changes in size
of reproductive organs delimit the breeding
season (Fig. 5A and 5B). These results
agree with the appearance and disappearance of secondary sexual characteristics
(i.e., open vagina, lactation, and descended
testes). Increased thennogenesis, through
reallocation of resources towards BAT, is a
benefit of gonadal regression in small rodents (Blank and Ruf, 1992). Another benefit of gonadal regression is a decrease in
aggressive behavior, which creates more socially tolerant animals and allows huddling,
a behavioral method of heat conservation in
C. ruti/us (West, 1977).
Analysis of seasonal changes in brain
mass of C. rutilus indicated similar seasonal
trends noted for total body mass. Absolute
mass and water content of brain decline
from summer to winter (Fig. 5C and 5D).
Yaskin (1984) reported a decline in brain
mass from summer to winter of > 10% in
C. rutilus from western Siberia. Similar dynamics of brain mass were reported for
shrews in Poland (Pucek, 1965). There also
were seasonal differences in dry mass of
the brain. A possible explanation for this
loss of dry mass is the declining significance of particular senses, such as sight, in
the subnivean space. Results of regressions
of log brain mass versus log body mass indicated a conservation of brain mass in
winter when total body mass and most body
components declined. Declines in brain
mass in autumn were proportionally less
than declines in total body mass. Decline in
brain mass in autumn is adaptive because
energy consumption by the brain constitutes
Vol. 80, No.2
a large proportion of the total energy requirements of an individual (Yaskin, 1984).
This seasonal decline in energy requirement
by the brain may be of value to the individual as energy requirements for thermoregulation increase in winter.
Brown adipose tissue was the only body
component that increased in absolute mass
from summer to winter. BAT is an important site of non-shivering thermogenesis in
small overwintering mammals (Feist, 1983;
Feist and Feist, 1986). The winter increase
in BAT (present study) was similar to those
described in other studies of C. rutilus
trapped from the same location (Feist,
1984; Sealander, 1972). Peak mass of BAT
occurred in late winter when temperatures
were lowest and thennostatic costs were
highest (Sealander, 1972). BAT showed a
similar increase in small overwintering
shrews (Myrcha, 1969).
Patterns of seasonal change in absolute
size of body components were in most
cases similar to changes in overall body
mass and composition of C. rutilus. Declines in total body mass during autumn resulted primarily from proportionate declines in mass of skeletomuscular, gastrointestinal, and integumental components but
also from disproportionate declines in reproductive tract and liver components (Table 4). Notably, changes in skeletomuscular
components, particularly muscle, contributed most to the annual cycle in total body
mass, particularly in males. Changes in gastrointestinal components, principally small
intestine, also made major contributions to
seasonal changes in total body mass. Increases in body mass and body water content of females in spring can be explained
in part by the increase in size of reproductive organs and the high water content associated with pregnancy. Sexual differences
in seasonal peaks in body mass can be explained by different patterns of change in
particular components. Males, which
peaked in body mass in spring, showed different seasonal patterns in component mass
compared with females, which peaked in
May 1999
ZUERCHER ET AL.-BODY COMPOSITION OF VOLES
summer. Among these components, muscle
of the hind quarter, which is likely indicati ve of all skeletal muscle, increased to a
peak in spring for males and in SUmmer for
females. Seasonal change in body water
content can be accounted for mostly by
changes in water content of skin, decline in
mass of the reproductive tract (a water-rich
component), and generalized loss of water
content in all remaining components.
Lack of seasonal changes in relative
mass of components of the gastrointestinal
tract indicated that those components
changed size in concert with body mass.
However, several components (i.e., reproductive tract, liver, brain, heart, bone, and
BAT) showed seasonal changes disproportionate to changes in total body mass. Exponents of allometric equations for liver
(females only), heart, bone, BAT, and brain
differed significantly from 1.0, indicating
that the observed seasonal changes in these
components represent adjustments or acclimatization to different sets of environmental conditions or of selective forces. Exponents for these five components also differed significantly from 0.75 and thus did
not scale with metabolic rate.
In conclusion, seasonal changes in component mass throughout the annual cycle
generally supported the null hypothesis that
a proportionate scaling down of the whole
body and its various components occurs as
the animal enters winter. Liver and reproductive tract, however, showed greater proportionate changes than body mass, indicating that their relative importance to the
animal was less during winter than in summer. However, heart, bone, and brain exhibited proportionally smaller changes than
body mass, indicating constraints on downsizing or enhanced function in winter as indicated by conservation of absolute mass
and increases in relative mass compared
with other components in winter-acclimatized animals. These findings are consistent
with our alternative hypothesis, namely that
relative size of various body components
changes with changes in total body mass.
457
Furthermore, these are consistent with
adaptive explanations for seasonal reallocation of resources. Finally, the importance
of BAT to C. rutilus in winter was indicated
by the higher absolute mass and higher
BAT index in winter compared with summer.
ACKNOWLEDGMENTS
We thank D. Feist and B. Barnes for making
insightful comments during the course of this
study and providing equipment and supplies for
the over-winter trapping. We also thank C. Conroy, B. O'Connell, and M. Zuercher for assistance during trapping. We thank three anonymous reviewers for their comments, which significantly improved this manuscript. This research was supported by an award from the
President's Special Project Fund at the University of Alaska Fairbanks and a Multi-user Biological Equipment Grant from the National Science Foundation (BIR-9317916).
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Submitted 25 January 1997. Accepted 12 July 1998.
Associate Editor was Robert K. Rose.