ARTICLE IN PRESS
Journal of Thermal Biology 32 (2007) 383–387
www.elsevier.com/locate/jtherbio
Seasonal changes and wind dependence of thermal conductance in
dorsal fur from two small mammal species (Peromyscus leucopus and
Microtus pennsylvanicus)
Justin G. Boyles, George S. Bakken
Department of Ecology and Organismal Biology, Indiana State University, Terre Haute 47809, USA
Received 20 March 2007; accepted 18 April 2007
Abstract
(1) We measured the thermal conductance of dorsal pelage from meadow voles (Microtus pennsylvanicus) and white-footed mice
(Peromyscus leucopus) during summer and winter.
(2) Thermal conductance was lower in the winter pelage of both species, but the seasonal change was greater in meadow voles.
(3) The form of wind speed dependence was determined by fitting a nonlinear curve of the form a+buc to data recorded at five wind
speeds. The most appropriate exponent c was between 0.908 and 0.987, depending on species and season. These values are common
and suggest that thermal and dynamic forces are important.
r 2007 Elsevier Ltd. All rights reserved.
Keywords: Heat loss; Insulation; Meadow voles; Pelage; Rodentia; Thermoregulation; White-footed mice
1. Introduction
Many mammals have seasonal changes in the quality of
their fur due to changes in the density, diameter and/or
length of hair which probably result in lower thermal
conductance in the winter (Huestis, 1931; Sealander, 1951;
Harris et al., 1985; Jacobsen, 1980; Walsberg, 1991;
Reynolds, 1993; Bulgarella and de Lamo, 2005). During
winter, well-insulated mammals may have more freedom in
habitat selection and in the timing of activities than do
poorly insulated mammals. This thermoregulatory advantage may increase survival or allow the exploitation of
unoccupied niche space.
However, particularly long and dense fur incurs energetic and nutritional costs for synthesis (e.g. Reis and
Schinckel, 1963; Reis, 1965; Murphy and King, 1982, 1984)
and may impair mobility. Such considerations may explain
why some small (o50 g) mammals (e.g. Peromyscus spp.)
Corresponding author. Tel.: +812 237 2561.
E-mail address: [email protected] (J.G. Boyles).
0306-4565/$ - see front matter r 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jtherbio.2007.04.007
show little or no increase in pelage thickness or density in
winter. The possibility of locomotor impairment is
suggested by a possible size threshold at which increased
winter insulation is advantageous, as lemmings (Dicrostonyx groenlandicus), roughly four times heavier than
Peromyscus, double their fur depth and density (fibers/
area) during winter (Reynolds, 1993).
If it exists, the size threshold for seasonal variation in fur
quality likely occurs for a body mass p50 g. Unfortunately, most published data on the thermal conductance of
fur are for larger mammals (e.g. Scholander et al., 1950;
Hammel, 1955; Treagear, 1965; Chappell, 1980; Reynolds,
1993), although there are some data on small mammals
(Hart and Heroux, 1953; Hart, 1956; Jofré and CaviedesVidal, 2003).
Therefore, to better understand the relation of body
mass to increased winter insulation, we have measured and
compared the thermal conductance (K) of summer and
winter dorsal fur from two rodent species differing by ca.
30% in mass found in the same area, white-footed
mice (Peromyscus leucopus) and meadow voles (Microtus
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pennsylvanicus). Because small mammals may be exposed
to wind and the effect of wind speed is little studied, we
included wind as a variable. We predicted that K would
decrease during winter to reduce heat loss due to colder
weather, and that the difference between the seasons would
be greater in the heavier meadow voles than in whitefooted mice. Because the mice we used are semi-arboreal,
we predicted that their fur might be less sensitive to wind,
than the fur of meadow voles.
Fig. 1. Schematic diagram of the apparatus used to measure the heat
transfer coefficient (K) of fur. The apparatus is modified from Bakken
et al. (2006).
2. Methods
2.1. Study animals
2.3. Apparatus
We used the white-footed mouse and the meadow vole.
White-footed mice are primarily a forest and forest edge
species, and are semi-arboreal. Meadow voles are prairie or
grassland-adapted species found in meadows and hayfields,
and are completely non-arboreal (Whitaker and Hamilton,
1998).
To minimize geographic variation, all mice used in this
study were kill-trapped in three neighboring counties in
northwestern Indiana during the summer of 2005 and the
winter of 2005–2006. We considered summer to be
June–August and winter to be December–February. We
only used fur from adults to avoid ontogenetic variation
(McClure and Porter, 1983). We followed the guidelines of
the American Society of Mammalogists (Animal Care and
Use Committee, 1998) in all aspects of this study and all
methods were approved by the Indiana State University
Institutional Animal Care and Use Committee under
Protocol # 3-4-2005:JOW/HB.
We mounted the fur samples on an apparatus (Fig. 1)
consisting of a heated aluminum plate and a thin-film heat
flow sensor (HFS-4, Omega Engineering, Stamford, CT,
USA). The apparatus was placed in a wind tunnel with a
cardboard ramp attached such that air flowed smoothly
parallel to the lay of the fur. We calculated thermal
conductance (K; W/m2/1C) by dividing the heat flow (W/
m2) by the temperature difference (1C) between the heat
plate and air. Therefore, we report overall thermal
conductance, i.e. the combined effect of heat transfer
within the fur and heat transfer from the outer fur surface
by radiation and convection. Thermal conductance of each
fur sample was measured at five wind speeds (0.04, 0.45,
1.48, 2.37 and 3.32 m/s). The first wind speed approximates
still air, but minimizes unstable readings that result from
pure free convection. The first two wind speeds are realistic
for non-arboreal mammals while the last three will only be
experienced when the animal is higher than 10 cm off the
ground. Each wind speed was maintained for 40 min to
allow the apparatus to equilibrate. To account for
resistance of the slide and contact interfaces, we subtracted
K of bare slides from K of the slide and fur sample using
the equation
2.2. Fur preparation
We excised pelts from partially frozen mice by cutting
ventrally and peeling the skin around the legs and from the
dorsal surface. We did not use completely frozen mice
because the skin tends to stretch or tear and we did not
allow mice to completely thaw because of the difficulty in
keeping body fluids off the pelt. Each pelt was glued to a
standard microscope slide using a thin layer of commercial
cyanoacrylate adhesive (The Original Super Glue, Pacer
Technologies, USA). Pelts were allowed to dry completely
and the excess was trimmed from the microscope slide
using a razor blade. Care was taken in all steps of the
process to avoid touching the dorsal fur, which tends to
cause the fur to lie irregularly. We used only dorsal fur
samples because this is the area most consistently exposed
to the environment, and because it is difficult to obtain
suitable samples of ventral fur. The conductance of dorsal
and ventral fur may differ (McClure and Porter, 1983;
Conley and Porter, 1986).
K fur ¼ 1=ð1=ktotal 1=kslide Þ.
2.4. Analysis
We evaluated the data for differences in K between species,
seasons and wind speeds using a mixed model analysis of
variance. Species and season were fixed factors and wind
speed was a random factor. Individual was included in the
model as a covariate. We included the simple effects and the
(species)(wind speed) and (species)(season) interactions.
To provide a model of fur conductance for heat transfer
calculations and comparison with other studies of fur or
feather insulation and wind, we fitted data for each species
and season with the model Kfur ¼ a+buc (Bakken, 1991).
We estimated the predictive value of the resulting regression as the ratio of the F value for the regression to the
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critical value of F for p ¼ 0.01 (Draper and Smith, 1981).
Larger values indicate better predictive value.
3. Results
We measured K of pelts from 30 meadow voles (15
summer:15 winter) and 24 white-footed mice (13 summer:11 winter). Depending on wind speed, there is a
16–29% decrease in K during winter in meadow vole pelts
and a 1–8% decrease in K of white-footed mice pelts
(Fig. 2). The species simple effect (p ¼ 0.05) and the
(species)(season) interaction (po0.005) were both significant, but the (species)(wind) speed interaction was not
(p ¼ 0.645). The thermal conductance of summer pelts was
similar between the two species, but was much lower for
winter pelts of meadow voles than white-footed mice
(Fig. 2). Both the season (po0.005) and wind speed
(po0.005) simple effects were significant. As expected,
K was lower during the winter for both species at all wind
speeds (Fig. 2). There was no significant difference among
individuals (p ¼ 0.31).
Thermal conductance increased significantly as wind
speed increased, and for winter pelts from both species, was
roughly 43% higher at the highest wind speed than the
Summer P. leucopus
Winter P. leucopus
Summer M. pennsylvanicus
Winter M. pennsylvanicus
18
16
K
14
12
10
8
0.0
0.5
1.0
1.5
2.0
2.5
Wind Speed (m/s)
3.0
3.5
Fig. 2. Mean thermal conductance (K)7SE (W/m2/1C) of dorsal pelts
excised from Microtus pennsylvanicus and Peromyscus leucopus during
summer and winter.
Table 1
Value of coefficients for the nonlinear curve Kfur ¼ a+buc describing the
effect of wind on heat loss from the dorsal pelage of Microtus
pennsylvanicus and Peromyscus leucopus
N
a
b
c
F/F0.01
Microtus
Summer
Winter
15
15
9.96
8.32
2.26
1.30
0.987
0.945
11.95
15.68
Peromyscus
Summer
Winter
13
11
9.42
9.39
2.43
1.87
0.908
0.968
68.28
73.58
385
lowest wind speed. The slopes of the best-fit nonlinear
models (Table 1) were higher in both species during
summer than during winter and higher in white-footed
mice than in meadow voles. The regressions for whitefooted mice have higher F/F0.01 values than those for
meadow voles, indicating that the mouse samples were less
variable in both seasons (Table 1). The best-fit models are
essentially linear, with values for the exponent c varying
from 0.908 to 0.987.
4. Discussion
As predicted, K was lower in winter pelts than in summer
pelts of both species at all wind speeds (Fig. 2). The thermal
conductance of winter meadow vole pelts was 16–29% less
than that of summer pelts (depending on wind speed)
compared to a maximum decrease of 8% in white-footed
mice. This agrees with studies that found the summer and
winter pelts of Peromyscus spp. to be structurally more
similar than the summer and winter pelts of larger
mammals (Huestis, 1931; Sealander, 1951; Steudel et al.,
1994). Meadow vole pelts were considerably thicker during
winter than during summer. Hair density (number of hairs/
cm2) increases less than 17% from summer to winter in
white-footed mice (Huestis, 1931; Sealander, 1951) compared to winter increases of up to 47% in field voles
(Microtus agrestis), which are only a few grams heavier
than white-footed mice (Al-Khateeb and Johnson, 1971).
The wind speed exponent c was slightly less than 1 for
both species in both seasons. Values near 1, as found in this
study (Table 1), are most common (Campbell et al., 1980),
and indicate an important role for both thermal and
dynamic processes in the fur. Convective heat loss from the
fur surface varies as u0.5, and the dynamic force of moving
air which forces air through the fur and rearranges its
structure varies as u2 (Bakken, 1991). For example, c is
near 2 for the very soft fur of jackrabbits, indicating that
dynamic processes such as fur displacement dominate
(Harris et al., 1985; Bakken, 1991). In contrast, c is near 0.5
in American goldfinches with stiff feathers, indicating that
dynamic processes are unimportant and pure convection
dominates (Bakken, 1991).
Contrary to our expectation, the thermal conductance of
white-footed mice fur is proportionately more affected by
increasing wind speed than is that of meadow voles,
probably because their thin pelt means that the external
boundary layer plays a more important role in overall
conductance than it does for the better-insulated vole pelt.
The semi-arboreal nature of white-footed mice means
they are exposed more often to high winds than are
terrestrial meadow voles. One possible explanation for
higher thermal conductance of mouse fur is that long,
dense fur may impair arboreal locomotion more than
terrestrial locomotion, and thus imposes costs that select
against the addition of winter pelage. Alternatively, whitefooted mice forage extensively on the ground, and most of
the time in trees is spent in nests where they are protected
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from the wind. Thus, wind may be important only during
brief periods of arboreal activity, and so has little effect on
overall thermoregulatory costs.
We speculate that Peromyscus may be very near the
threshold where the physical size constraint effectively
limits structural characteristics of fur. Extreme northern
populations of deer mice (Peromyscus maniculatus) showed
a relatively large 21% increase in insulation in still air
during winter (Hart and Heroux, 1953; Hart, 1956). This
suggests that the magnitude of seasonal pelage changes
may be constrained by both size and thermal environment,
with the balance set by the severity of winter conditions.
Wind had a strong effect on the thermal conductance of
our fur samples. Therefore, future studies of fur conductance should measure wind effects, particularly for
arboreal or semi-arboreal species that may be frequently or
routinely exposed to significant wind. Future studies on the
seasonal change in thermal conductance should address
whether very small mammals highly reliant on locomotor
agility may be unable to increase pelage insulation because
it impairs movement. Two studies are needed. First, the
hypothesis that fur with good insulation properties impairs
locomotion, and therefore impairs foraging and predator
avoidance, should be tested directly in laboratory experiments similar to those done with arboreal (e.g., Higham et
al., 2001; Spezzano and Jayne, 2004; Vanhooydonck et al.,
2006) and terrestrial reptiles (Jayne and Ellis, 1998;
Irschick and Jayne, 1999). Second, the existence of
interacting locomotor and thermal factors needs to be
tested using a data set from a large number of species with
varying mass and reliance on agility found in a range of
habitats. We would predict that, within subgroups of
similar species occupying similar microclimates, there
should be a distinct mass threshold above which fur
conductance decreases in winter and below which it does
not. Further, this threshold should be lower in colder
microclimates.
Acknowledgments
We thank M. Dunbar, D. Judy and J. Storm for help
with preparing samples and taking measurements. H.
Brookhart and J. Sheets trapped the animals used herein.
D. Sparks and M. Dunbar provided comments on earlier
drafts of this manuscript.
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