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This is to certify that the

thesis entitled

THERI‘DRFIIJIATION IN THE MUSKRAT (ONDATRA
ZIBEI'HICUS): THE USE OF REGIONAL I-IEI'EROIHERMIA

 

 

presented by

Frank E. Fish

has been accepted towards fulfillment
of the requirements for

M. S. Zoology

degree in

X/WW

Major professor

 

 

Date November 18, 1977

 

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THERMOREGULATION IN THE

MUSKRAT (0NDATRA ZIBETHICUS):

 

THE USE OF REGIONAL

HETEROTHERMIA

By

Frank E. Fish

A THESIS

Submitted to
Michigan State University
in partial fulfullment of the requirements
for the degree of

MASTER OF SCIENCE
Department of Zoology

1977

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ABSTRACT

THERMOREGULATION IN THE MUSKRAT (0NDATRA ZIBETHICUS):
THE USE OF REGIONAL HETEROTHERMIA

 

BY

Frank E. Fish

Regional heterothermia, metabolic rates, and whole-body
insulation were studied in six muskrats (0ndatra zibethicus),
restrained in air and in water at temperatures of 20, 25, and 30°C.
Appendicular temperatures were found to approach ambient temperatures
for all temperatures in water and at 20 and 25°C in air. In air at
30°C, appendicular temperatures increased above ambient temperature
after an average colonic temperature of 39°C was attained. metabolic
rates were higher in water than in air, while values of whole-body
insulation were higher in air than water. High peripheral temperatures,
due to vasodilation, decrease whole-body insulation and allow for
increased heat dissipation, while peripheral temperatures approaching
ambient temperature, due to vasoconstriction or counter-current heat
exchanges, increase whole-body insulation maximizing heat conservation.
The causative factor, for the differential responses of muskrats in air
and water, was considered to be the higher thermal conductivity of

water than air.

ACKNOWLEDGMENTS

I wish to express my appreciation to the members of my
committee, Dr. Richard W. Hill (chairman), Dr. Rollin H. Baker, and
Dr. Ralph A. Pax, for their advice, constructive criticism, and support
during this study. I also wish to thank Dr. Charles Cress for his
statistical advice, Dr. Harold H. Prince for use of facilities, and
Dr. James Edwards for his advice and encouragement.

I am grateful to the Department of Zoology and the MSU Museum
for financial support and use of facilities provided during this study.
The State of Michigan, Department of Natural Resources and Rose Lake
Wildlife Research Station are gratefully acknowledged for allowing the

collection of muskrats.

ii

TABLE OF CONTENTS

Page
LIST OF TABLES . . . . . . . . . . . . . . . . . . iV
LIST OF FIGURES . . . . . . . . . . . . v
INTRODUCTION . . . . . . . . . . . . . 1
METHODS . . . . . . . . . . . . . . . . 3
Experimental Animals . . . . . . . . 3
Experimental Procedure . . . . . . . . . . . . . 3
Temperature . . . . . . . . . . . . . . . 4
Weight-Specific Metabolic Rate . . . . . . 5
Whole-Body Insulation . . . . . 7
Statistical Procedures . . . . . . . 8
RESULTS . . . . . . . . . . . . . . . . 9

Regional Body Temperatures . . . . . . .
Weight-Specific Metabolic Rate . . . . l4
Whole-Body Insulation . . . . . . 19
Correlation Analyses . . . . . . . . . . . . . 22
DISCUSSION . . . . . . . . . . . . . . . 24
APPENDIX A. REGIONAL BODY TEMPERATURE . . . . . . . . . . . . 36
LITERATURE CITED . . . . . . . . . . . 37

iii

Table

LIST OF TABLES

Results of correlation analyses between whole-body
insulation and regional body temperatures for each
body region of muskrats exposed to environments of
air and water . . . . . . . . . . . . . . . . . . . . . .

Mean regional body temperatures (i one standard

error) for all muskrats exposed to environmental
media of air and water at Ta's of 20, 25, and 30°C . . . .

iv

Page

23

36

LIST OF FIGURES

Figure Page

1. Mean regional body temperatures, T , plotted against
ambient temperature, T , for all skrats in air and
in water I O O O O 0 Ca. 0 O O O O O O O O O O O O O O 0 0 11

2. Regional body temperatures of a restrained muskrat
during exposure to a T8 of 30°C, starting 2 hours
after the beginning of the experiment . . . . . . . . . . 16

3. Resting metabolic rate for all muskrats as a function
of the ambient temperature, Ta’ in air and in water . . . 18

4. Whole-body insulation for all muskrats plotted as a
function of the ambient temperature, Ta’ in air and
in water . . . . . . . . . . . . . . . . . . . . . . . . . 21

INTRODUCTION

The sparsely haired appendages of various mammals may act as
potentially major sites of heat loss (conduction, convection, radiation)
due to their relatively high surface-to-volume ratio and sparse pelage
insulation. These sites of heat loss may thus be of serious consequence
to mammals that maintain a semi-aquatic existence. Since water has a
high heat capacity and is at least 25 times more conductive than air at
the same temperature (Weast, 1971), these homeotherms are confronted
with heavy thermal demands.

Physiologically, semi-aquatic mammals may cope with the high
thermal conductivity of water by allowing the temperature of sparsely
haired appendages to fall close to ambient temperature. Because heat
is lost in direct relation to the thermal difference between the surface
of the skin and the environment (Bartholomew, 1972), there is a
reduction in the rate of heat dissipation from the appendages by
permitting the appendage to approach ambient temperature. Conversely,
excess heat may be lost through the skin of the appendage by increasing
peripheral blood flow from the body core. Hammel (1968) has stated,
that in endotherms with core temperature greater than ambient, the
"control of blood flow to the periphery can readily regulate the flow

1

of heat from core to skin, and is the only controllable way to
distribute internal heat to the skin." The phenomenon in which
different temperatures are maintained in different parts of the body
is termed regional heterothermia (Hill, 1976). This response has
been found to be common in both aquatic and terrestrial mammals.

The purpose of this study was to examine the role of regional
heterothermia in the thermoregulation of a semi—aquatic mammal with
regard to changes in whole-body insulation, and differential responses
to environments of air and water. For this study, the muskrat (0ndatra

zibethicus) was selected as the experimental animal, due to its

 

semi-aquatic nature (Johnson, 1925; Errington, 1962) and sparsely
haired appendages which comprise less than 10% of the total surface
area (Johansen, 1962a). It was hypothesized that there is (i) a
difference in regional body temperatures (gag., tail, feet) of muskrats
in water and in air over the same temperature range, (ii) an increase
in the metabolic rate for muskrats in water over those in air, and a
decrease in the whole-body insulation for animals in water compared

to those in air, and (iii) an inverse correlation between the

temperature of the appendages and whole-body insulation.

METHODS

A. Experimental Animals

 

Four male and two female muskrats (Ondatra zibethicus) were

 

live-trapped in Ingham and Clinton Counties, Michigan, during the
spring and summer of 1976. They ranged in weight from 485 to

1152 g (mean: 869 g) during the period of testing. The animals were
initially maintained outdoors in an open-air enclosure for a period
of one week after capture to acclimate them to captivity. The
enclosure was equipped with an artificial pond, with running water,
and a nest box with wood-shaving bedding. A diet of cattail

(Typha sp.) roots and Wayne Lab-Blox was provided. Following the
initial one-week period, the muskrats were housed indoors in separate
metal cages (51x36x31 cm), with wood-shaving bedding. water and food
were supplied ad libitum, with the food being Wayne Lab-Blox supple-
mented with dog food (Perk Food Co.), carrots, and apples. Average

air temperature in the colony was 21°C, and the light cycle was natural.

B. Experimental Procedure

 

Regional body temperatures (Tb), resting metabolic rate (V0 ),
2

and whole-body insulation of each muskrat were examined in environmental

3

media of air and water at ambient temperatures (Ta) of 20, 25, and 30°C.
Mbskrats were tested individually in a metabolic chamber, while under
restraint. During tests in air, sealed cartons were placed within the
chamber to reduce the chamber air volume and corresponding equilibrium
time, as calculated by the formula of Lasiewski 25 al. (1966). In no
way did the cartons interfere with movements by the muskrat. For tests
made in water, the chamber was filled with water to 742 of its volume.
Each muskrat was fasted for at least 24 hr prior to testing to
establish a post-absorbtive state. The muskrat was anesthetized with
Metophane (Pitman-Moore Inc.), and secured to a Plexiglas restraining
board. Three leather straps fastened to the board were positioned to
restrain the cervical, thoracic, and pelvic regions of the muskrat.
The board was shaped to allow the legs to hang freely, while small
holes in the board allowed for the free movement of water or air

between the under-surface of the muskrat and the board.

C. Temperature

 

Regional body temperatures of the dorsal skin (center of dorsal
abdomen; Tds), foreleg (posterior surface of lower wrist; Tfl)’ hindfoot
(plantar surface; Thf), proximal tail (4 cm from the base in dorsal
keel; Tpt), and distal tail (4 cm from tip in dorsal keel; Tdt) were
measured using thermocouples constructed from 36-guage, Teflon-insulated
capper and constantan wires (Omega Engineering Inc.). Thermocouples
were implanted subcutaneously by first forcing a 20-gauge hypodermic
needle through a fold in the integument, then threading the wires

through the needle and removing the needle. Colonic temperature (12 cm

into the colon; Tc) was measured using a thermocouple constructed
from 30-gauge copper and constantan wires soldered at the tip and
threaded through polyethylene tubing (2.08 mm OD). All body
temperatures were monitored continuously with a 12-point Honeywell
Electronik 15 potentiometer. Ta's were monitored with a thermistor
probe connected to a Yellow Springs Instruments Tele-Thermometer

Mbdel-43, located in a corner of the metabolic chamber 10 cm above

the floor.

D. Weight-Specific Metabolic Rate

 

The metabolic chamber was constructed from a 70.4 liter glass
aquarium and was fitted with a removable Plexiglas lid. The inner
dimensions of the chamber were 75.3x31.5x29.7 cm. The lid was fitted
with inflow and outflow tubes for air flow and ports for the passage of
thermocouple wires and thermistor proble. A flexible rubber gasket was
attached to the rim of the chamber and petroleum jelly applied to form
an air-tight seal with the lid. The lid was clamped in place using
braces. Brackets, inside the chamber, supported the restraining board
and muskrat, with the animal's head angled 11° upward from the hori—
zontal. This arrangement allowed the experimental animal to breathe
while, during some tests, the majority of the body was submerged in
water. During all tests in water, a Beckett N-lOO submersible pump
was employed to circulate water in the chamber at a rate of 122 1/hr.
The metabolic chamber was kept inside a Sherer Model CEL 25—7 Controlled

Environmental Chamber to control the T .
a

Weight-specific oxygen consumption (V02), as a measure of
metabolic rate, was monitored using an open-circuit system conforming
to condition B of Hill (1972). The oxygen content of dry, COz-free air
flowing out of the metabolic chamber was monitored continuously with a
Beckman G-2 paramagnetic oxygen analyzer and recorded on a Honeywell
Electronik 15 potentiometer. Ascarite (A.H. Thomas Co.) and Drierite
(W.A. Hammond Co.) were used to absorb CO2 and water vapor, respectively,
from the air flow. The rate of air flow entering the metabolic chamber
was measured with a calibrated Gilmont Model 1300 flowmeter. The
average flow rate ranged in different tests from 1803 to 3061 cc/min
for dry air at STP. Before entering the metabolic chamber, the air
flow was passed through a copper coil immersed in a water bath inside
the environmental chamber. This allowed the air flow to equilibrate
to the desired Ta. Oxygen consumption was calculated by the procedure
of Depocas and Hart (1957) and Hill (1972) and expressed as cc 02(STP)/
g/hr.

The experimental animal remained in the metabolic chamber after
placement of the thermocouples for a period of at least 1 hr prior to
testing to allow for the effects of the anesthetic to diminish and for

adjustment to Ta, which had been established previously. V0 and Tc

2
were monitored until the muskrat had reached a steady state condition.
The steady state condition was considered to be attained when there was

no net change in Tc and V Before data were recorded after steady

o O
2
state had been reached, the air in the metabolic chamber was allowed
time to mix with incoming air at an equilibrium level of 902, as
calculated by the formula of Lasiewski gt 2;. (1966). The chamber

equilibrium time for each environmental medium tested was 40 min in air

or 20 min in water. The average total time that the muskrat spent in
the metabolic chamber was 4 hr with the time until equilibrium had been
attained ranging from 1 to 2 hr.

The Winkler method of measuring dissolved oxygen (Welch, 1948)
was employed to determine if diffusion of oxygen between the air flow
and water contributed a possible error in the measured oxygen con-
sumption. Water samples were drawn prior to and immediately after
testing, and the difference in oxygen concentration between the two
samples calculated. The net oxygen exchange between air and water
was found to be less than 0.5% of the 602 of the muskrat, and was

considered to represent no significant error and was not corrected

for.

E. Whole-Body Insulation

 

The whole-body insulation was calculated following the method of
Scholander_g£.§l. (1950), in which insulation 8 (Tc - Ta)/TOZ. The
insulation was corrected, by the method of Dawson and Schmidt-Nielsen
(1966) for net changes in Tc during the test period, indicating a change
in the heat content of the body. The change in the total heat content
of the body was calculated after adjustment of the body weight by
subtracting the weight of the appendages, which had temperatures
approaching Ta' The net change in the heat content of the body was
computed by the product of the adjusted weight of the body, the net

—1
change in Tc’ and the specific heat of the body of 0.83 cal g °C .
The change in heat content was subtracted from V02, when the net change

in Tc was positive, and was added to V02, when the net change in TC was

negative.

F. Statistical Procedures

 

Statistical comparisons were made for data on body temperatures
with a split—plot, randomized block design on a 2(environmental media)x
3(Ta) factorial, one-way analysis of variance (AOV), and for 002 and
whole-body insulation with a randomized block design on a 2x3 factorial,
one-way AOV. Individual contrasts were made using Student-Newman-Keuls'
test (SNK). Correlations between whole-body insulation and the

regional body temperatures were calculated using correlation analysis.

Differences were considered significant at Ps.05.

RESULTS

A. Regional Body Temperatures

 

The mean temperatures for each of the six body regions (Tb)
in relation to ambient temperature (Ta) in air and in water are
summarized in Figure 1 and listed in Appendix A. Using a one-way
AOV, it was found that the interaction of Ta and environmental medium

as factors affecting T was statistically significant (P<.001),

b

inferring that Tb's were dependent on both Ta's and environmental
media. Due to the magnitude of the interaction, the effects of Ta and

environmental media on Tb were examined independently. The Tb's of all

the body regions were found to increase in direct response to increases
in Ta’ regardless of the environmental medium. However, the temperature
responses for each of the body regions showed significant differences
between the environments of air and water (P<.001).

Tc and T s responded similarly to all treatment combinations.

d

A maximum difference of 1.1°C between the mean body tenperatures of

Tc and T occurred in air at 20°C Ta. Only slight rises in

ds

temperature were recorded for the colon and dorsal skin from 20 to 30°C

T in air and from 25 to 30°C in water. Exposure to 20°C in water
a

10

Figure 1. Mean regional body temperatures, Tb, plotted against
ambient temperature, Ta, for all muskrats in air and in
water. The dashed lines are lines of equality between

Tb and Ta'

11

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12

depressed mean Tc and Td8 to values of 33.6 and 33.4°C, respectively,
which represented a sharp decline from values of 36.4 and 36.1°C at a
T8 of 25°C. In one case, one individual muskrat maintained a steady
state Tc of 28.5°C in water at 20°C Ta‘ Such results are similar to
those observed by Hart (1962), in which the Tc for unrestrained muskrats
tested in water fell at Ta's of 20°C and below. The depressed Tc for
muskrats in water at 20°C was presumed to indicate that the animals had
attained a hypothermic state.

Appendicular temperatures, as represented by foreleg, hindfoot,
proximal tail, and distal tail in Figure 1, varied substantially over
the range of Ta's for both air and water. These Tb's were found by SNK
to increase significantly as T8 increased (P<.05) and were significantly
different by SNK from Tc and Tds under all conditions (P<.05). Sub-
stantial increases of appendicular temperatures above T8 at certain Ta's
were assumed to indicate increased peripheral blood flow due to vaso-
dilation at such Ta's. Johansen (1962a) demonstrated experimentally
that tail temperatures of approximately 35°C were due to increased
peripheral blood flow caused by vasodilation.

In air, Tfl remained significantly higher than the other
appendicular temperatures at Ta's of 20 and 25°C with means of 27.1:

1.5 and 30.9:1.2°C, respectively (P<.01). Sample calculations, based
on rough estimates of foreleg surface area and temperature distribution
using the formulas of Calder and King (1974) for conductive and con—
vective heat transfer and a thermal conductivity coefficient of tissue

of 0.0011 cal s'1 cm.-1

"C-l (Schmidt-Nielsen, 1975), indicated that heat
conduction from the body to the foreleg would not be sufficient to

maintain a high Tfl against heat loss due to free or forced convection.

13

Heat transfer by conduction through the appendage was calculated to occur
at a rate of 0.065 cal/min in air at 20 C Ta’ while under these
conditions the rates of heat loss from the surface of the skin by free
convection and forced convection at a wind velocity of 20 cm/sec were
0.258 and 0.973 cal/min, respectively. A probable explanation is that,
at all Ta's in air, blood flow persists to the foreleg supporting at
elevated Tfl by conductive and circulatory convective heat transfer.

The mean Thf at 20°C in air was 23.3i2.5°C. The elevation of this
temperature above Ta was produced by the response of a single muskrat,
which maintained an average Thf of 35.5°C. Exclusion of this individual
would yield a mean Thf of 20.9i0.4°C, which would be only slightly
higher than Tpt and Tdt for the same conditions. The two tail
temperatures remained close to T8 for tests in air at 20°C. Although
only small increases above T8 were observed for mean Thf’ Tpt’ and Tdt
in air at 25°C, one individual demonstrated peripheral warming with an

elevated Tpt of 32.7 and T t of 31.9°C.

d
In air at 20 and 25°C, no large fluctuations were observed in

Tb's before or during the attainment of steady state by muskrats tested

in the metabolic chamber. However, prior to the experimental animals'

reaching steady state in air at 30°C T Tc increased gradually, while

a’
Thf’ Tpt’ and Tdt remained slightly above Ta' At some point after Tc
had risen to a mean of 39.0°C, all appendicular temperatures were
observed to increase rapidly, while Tc remained relatively constant or
showed a slight decrease. The appendicular temperatures exhibited small
fluctuations after Tc had ceased to increase. The temperature record

for a typical muskrat in air at 30°C illustrating the relationship of

the central body temperatures with the increased temperature of the

14

appendages is shown in Figure 2. Tfl’ Thf’ Tpt’ and Tdt for all
muskrats ranged from 5.4 to 7.2°C above Ta’ and these elevated
temperatures are believed to be the result of increased peripheral blood
flow due to vasodilation. Of particular interest is that peripheral
vasodilation in muskrats was only elicited when animals had a Tc of at
least 39°C. This is consistent with the data reported by Johansen (1961)
in which tail temperature increased to 35 to 37°C after muskrats had
been subjected to a positive heat load or exercise, and circulation of
the tail kept rectal temperature below 39°C.

In contrast to tests in air, all appendicular temperatures for
muskrats tested in water were very similar and closely approximated all

Ta's, with a maximum difference of O.7°C for Tf at 30°C.

1

B. Weight-Specific Metabolic Rate

The results on V02 for muskrats in air and in water are

summarized in Figure 3. AOV showed a significant interaction between

the environmental media and Ta's (P<.01). Therefore, V02 varied in
response to T8 and the environmental medium. Restrained muskrats in
water had a significnatly higher 602 than animals in air over the
same range of Ta (P<.001). In water, T02 ranged from 91% higher than

V0 in air at 25°C to 342 higher at 30°C. The V0 observed for a T8
2 2
of 30°C in water was revealed by SNK to be significantly lower than

the other values in water (P<.Ol), and represented a reduction of 0.34

cc 02/g/hr from the value reported for 25°C Ta' In contrast, the

values for V0 in air remained relatively stable for all Ta's, with no
2

significant differences between values.

Figure 2.

15

Regional body temperatures of a restrained muskrat
during exposure to a T8 of 30°C, starting 2 hours after
the beginning of the experiment. Temperature changes
of the colon (O O), dorsal skin (o----o), foreleg
(l—l), hindfoot (D---- D), proximal tail (A—A), and
distal tail (An-A) are recorded in 10—min intervals.
Note the sharp rise in appendicular temperatures, in-
dicating peripheral vasodilation, with a simultaneous
decrease in the temperature of the colon and dorsal

skin.

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17

Figure 3. Resting metabolic rate for all muskrats as a function
of the ambient temperature, Ta, in air (0—0) and in
water (o----o). Symbols represent means for each

treatment combination; vertical lines represent + one

standard error (SE).

18

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Figure 3

19

C. Whole-Body Insulation

 

Whole-body insulation plotted against T8 in air and in water
is illustrated in Figure 4. The insulation was dependent on both the
Ta and environmental medium examined as indicated by AOV (P<.001). The
range of insulative values for muskrats restrained in water was
significantly lower than those values calculated for air for all
Ta's tested (P<.001). This appears to be the direct result of the
different thermal conductivities and convectivities of the two media.
At 20 and 25°C Ta’ the difference in whole-body insulation between
air and water was essentially constant at 11.21 °C/cc OZ/g/hr. This
value represents a difference of 128% for the insulation of muskrats
in air over the insulation for the same animals in water. At 30°C
Ta in air, the mean whole-body insulation was 11.25 i 0.3 °C/cc 02/g/hr,
which represents a reduction of 422 from the insulation of 25°C in air.
It is noteworthy that under these particular conditions, there was a
corresponding increase in the temperature of the appendages. Although
the 302 in air did not significantly change between 25 and 30°C Ta’
the colonic-ambient temperature differential, Tc - Ta’ decreased, thus
resulting in a smaller calculated whole-body insulation. No similar
reduction for insulation was recorded for animals in water at a T3 of
30°C and, correspondingly, increased vasodilation of the appendages was
not indicated. Whole-body insulation decreased at a constant rate in
water as T8 increased, with a reduction of 2.3 °C/cc 02/g/hr for the

range of Ta's tested.

Figure 4.

20

Whole-body insulation for all muskrats plotted

as a function of the ambient temperature, Ta’ in air
(0—0') and in water (O----O). Symbols represent means
for each treatment combination; vertical lines represent

i one standard error (SE).

21

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mafia 33380.. 392.52.. 381mg

 

Figure 4

22

D. Correlation Analyses

 

The results of correlation analyses between whole-body
insulation and regional body temperatures for muskrats exposed to
environments of air and water are presented in Table 1. With the
exception of Tc and Tds in water, all Tb's in air and water were
significantly correlated with whole-body insulation (P<.05). In
water, all appendicular temperatures had higher coefficients of
correlation as compared to the two central body temperatures, while
in air, only Thf’ Tpt’ and Tdt were higher. The negative coefficients
of correlation for all Tb's except Tc in water, indicate that there is
a decrease in the whole-body insulation with increasing Tb. From these
results, it is apparent that changes in the temperature of the
appendages are inversely associated with changes of the whole-body
insulation of muskrats, and are at least partially responsible for
the lability of the insulation. For muskrats in air, increases in
appendicular temperatures, indicating increased peripheral blood flow,
apparently allow for increased heat dissipation through the appendages,
decreasing the over-all insulation of the body. Since no vasodilation
is apparent in water for the Ta's studied, only a slight reduction in
whole-body insulation occurs with increasing appendicular temperatures
are correspondingly lower (but still significant), with the conservation

of heat being maximized

Table 1. Results of correlation analyses between whole-body

insulation and regional body temperatures for each body

region of muskrats exposed to environments of air and

water.

 

Body Environmental

Region Medium

Coefficient of
Correlation r

 

 

Air -0.547*
Colon

Water 0.009

Air -0.686**
Dorsal Skin

Water -0.013

Air —0.638**
Foreleg

Water -0.584*

Air -0.722**
Hindfoot

Water -0.592**

Air -0.878**
Proximal Tail

Water -0.588*

Air -0.905**
Distal Tail

Water -0.591**

* P < 0.05

**P < 0.01

DISCUSSION

Irving and Krog (1955) demonstrated that peripheral cooling was
not a characteristic of the entire body surface, but rather a property
of the extremities for well furred northern mammals. The lability of
temperature for the appendages has been well documented for a variety
of aquatic mammals, including the muskrat (Johansen, 1961, 1962a;
Shcheglova, 1964).

In the present study, restrained muskrats tested in environ-
mental media of air and water at Ta's of 20, 25, and 30°C demonstrated
that the temperatures of various body regions were highly variable
and under a certain amount of vasomotor control. Of particular
importance were the sparsely haired appendages, which proved to be
the most labile in their temperatures. For animals tested in air, Ta
increased from 20 to 30°C, and appendicular temperatures increased by
8.6 to 16.4°C. Correspondingly, mean Tc rose from 37.1 to 39.2°C, while
the mean Td8 was held to within 1.1°C of Tc' In air at 20°C, the tail
was found to have a temperature approximating Ta’ but Tfl and Thf
remained 7.1 and 3.3°C higher, respectively. Vasodilation of the
appendages as indicated by a significant increase in appendage
temperature above Ta, was observed for all muskrats tested in air at

24

25

30°C Ta' However, vasodilation in the appendages was only apparent
after the animals had attained an average Tc of 39°C, before which
Thf’ Tpt’ and Tdt approached Ta' After vasodilation in the appendages,
TC was observed to stabilize or decrease. In water, no vasodilation
was observed over the range of Ta's tested, and all appendicular
temperatures remained close to Ta' Mean Tc and Tds were found to be

depressed in water at 20°C T being 33.6 and 33.4°C, respectively,

a’
and remained below 39.0°C for the other Ta's.

Johansen (1961) found rectal temperatures in muskrats to be
between 37 and 39°C with no peripheral warming at T3 ranging from 0 to
20°C. At Ta's above 25°C the tail temperature rose to 35 to 37°C, while
blood flow increased by a factor of 100-180. In a later study, Johansen
(19623) found tail blood flow during vasodilation to increase by a
factor of more than 400. The white rat in air has been shown to
vasodilate the tail at Ta between 27 and 30°C, with blood flow rising
from less than 5 ml to 40 ml of blood per 100 m1 of tissue per min
(Rand_et‘al., 1965). This increase in blood flow to the tail was
responsible for the dissipation of 25% of the total heat production.
Johansen (1962a) stated that at Ta of approximately 20°C, the tail
temperature of the muskrat fluctuated spontaneously and rapidly
between 20 and 35°C. In the present study, tail temperatures were not
observed to fluctuate, but remained close to a T8 of 20°C in both air
and water. The increase in tail blood flow and corresponding
temperature increase of muskrats in air stimulated to exercise or
subjected to a positive heat load, observed by Johansen (1962a), were

considered to be responsible for the prevention of heat accumulation in

the body due to the high insulatory properties of the pelage. In

26

muskrats in air at 18-20°C, when the tail was immersed in ice water,
tail skin temperature exhibited a rapid decline from over 30°C to 1°C.
Johansen believed that such a response reduced heat dissipation as
indicated by the stability of the rectal temperature. Shcheglova (1964)
reported steady increases in the tail temperature of the muskrat from
5.7 to 24.4°C in water, and from 6.8 to 26.9°C in air as Ta's increased
from 0 to 35°C. MacArthur (1974) monitored body temperatures in
free-living muskrats during the summer and observed that the deep

body temperature increased during swimming and feeding activity. The
body temperature in an adult male muskrat was reported to be as high

as 39.9°C, and usually over 39.0°C during activity. This rise in

deep body temperature was believed caused by the accumulation of

excess metabolic heat due to activity of the skeletal muscles and

the pelage insulation which facilitated heat storage. However, during
swimming and diving for periods of 10 minutes or more in winter,
muskrats showed a net decline in body temperature with only short-term
increases during bursts of activity.

The thermoregulatory significance of heterothermic appendages
of aquatic mammals has been studied by a number of investigators.
These appendages, with their large surface area in proportion to the
total body surface, represent a major avenue for the dissipation of
excess heat from the well insulated body. In tests made on a single

beaver (Castor fiber) it was concluded that the naked tail had a

 

secondary function of controlling heat dissipation (Steen and Steen,
1965). As Ta increased from 16 to 25°C in air, the beaver was

observed to increase rectal temperature from 37.0 to 39°C, and the

27

skin temperature at the tail tip increased from 16 to 35°C.
Hyperthermia in air at 25°C was avoided when the tail was placed in
water at 6°C. Heat loss from the tail to the water accounted for 20%
of the total heat production. Morrison et 31. (1974) estimated that

heat loss through the paws of the sea otter (Enhydra lutra) could

 

account for the dissipation of two-thirds of the heat load in water at
26°C and four-fifths in air at 22°C. Whittow 25 a1. (1972) concluded
that due to the high proportion of the total surface area represented

by the flippers of the California sea lion (Zalophus californianus),

 

they would be important in the control of heat loss. Irving 35 a1.
(1962) found that a considerable amount of heat was dissipated through

the flippers of fur seals (Callorhinus ursinus) after being driven

 

overland. Conversely, heat was conserved when flipper temperatures
were found to be, at most, 4°C above the water temperature of 9°C for
submerged seal pups. The dorsal fin of two species of dolphin has also
been shown to function both for heat conservation and dissipation
(McGinnis et 31., 1972).

The weight-specific metabolic rates, F02, of muskrats in water
were shown to be significantly higher than metabolic rates in air over
the range of Ta’ with differences ranging from 0.27 to 0.67 cc 02/g/hr
at 30 and 25°C, respectively. 902 for animals tested in air remained
relatively stable for all Ta's. Conversely, tests in water showed a
marked decrease of 24% as Ta increased from 25 to 30°C.

The thermoneutral zone of fed muskrats in air has been reported
to range from 10 to 25°C (McEwan et a1., 1974), while in water the lower

critical temperature was reported to be 30°C (Hart, 1962). Although

only three Ta's were tested in the present study, no detectable limits

28

to the thermoneutral zone were observed for tests in air, so that the
restrained muskrats were believed to be in thermoneutrality at all test

Ta's. However, for an equitable comparison with the data of McEwan

.e£_§l. (1974), a mean V of 0.81 i 0.03 cc 02/g/hr for Ta's of 20

02

and 25°C was computed. This value was 17% lower than the V0 of 0.97
2

cc 02/g/hr reported by Hart (1971) for muskrats in air. However,

MCEwan.e£_al. (1974) reported mean resting metabolic rates in the
thermoneutral zone as 83 kcal/kg/day for unfasted muskrats and 60
kcal/kg/day for 24-hr fasted animals. Recalculation of these values
using a caloric conversion factor of 4.8 kcal/liter of oxygen at STP
produces values of 0.72 cc OZ/g/hr for unfasted and 0.52 cc OZ/g/hr for

24-hr fasted muskrats, which are exceeded by the present Vo by 11 and
2

35%, respectively. Since all muskrats in this study were fasted at
least 24-hr prior to testing, the discrepancy may be due to the effect
of the implanted thermocouples and restraint on the experimental

animals. The V0 in the present study was found to be comparable to
2

Hart's (1962) data on muskrats in water at 30°C. Shcheglova (1964)
found that the level of metabolism for muskrats in water was 18 to

30% higher than in air at Ta's of 0 to 35°C. In the present study,

the difference in the mean Vo between air and water exceeded these
2

values, with the V in water being 34 to 91% higher than than in air

02

at Ta's of 30 and 25°C. One muskrat was, however, found to have a

V0 in water exceeding that in air by only 4% at 30°C Ta. Such
2

differences are probably due in part to the higher thermal conductivity

of water compared to air. Both the platypus, Ornithorhynchus anatinus

 

(Smyth, 1973), and sea otter, Enhydra lutra (Morrison et 31., 1974) had

 

a higher metabolic rate when exposed to water than air. Harbor seals

29

(Phoca vitulina), however, were found to have metabolic rates which

 

were equal in both water and air (Irving and Hart, 1957; Hart and
Irving, 1959). Such differences in the metabolic responses of
semi-aquatic mammals may be due partly to differences in body size and
to effects of non-wettable fur versus blubber for insulation.

The whole-body insulation of muskrats was found to be
dependent on the Ta and environmental medium, and corresponded to
changes in the temperature of the appendages. In water, the insulation
was found to decrease slightly as Ta increased. Thf’ Tpt’ and Tdt were
found to be positively correlated with T8 and exhibited an inverse
relationship to whole-body insulation in water. In air, a 42%
reduction in whole—body insulation occurred between Ta's of 25 and 30°C.
This reduction corresponded to the significant increase in appendicular
temperatures, indicative of peripheral vasodilation. All appendicular
temperatures were highly and inversely correlated with whole-body
insulation in air. Values of whole-body insulation were found to be
59 to 139% higher in air than in water. These differences are believed
to be the result of the higher thermal conductivity of water than air.
Immersion of the muskrat in water would also tend to reduce insulation
by compression of the air layer trapped in the non-wettable fur. This
would in effect decrease the length of the thermal gradient between
the skin and the environment, causing a reduction in the effective
insulation of the fur. Johansen (1962b) has shown that muskrats
depleted of the insulative air layer lose heat at a faster rate than
normal muskrats in water. Morrison 35 a1. (1974) stated that sea otters
in warm water showed a loss of buoyancy, indicating that water had

penetrated the fur, facilitating heat transfer. Examination of muskrats

30

after the present tests in water showed that the air layer in the fur
was maintained, except in regions in direct contact with the restraint
apparatus.

As has been demonstrated for muskrats, various other semi-aquatic
homeotherms have shown differences between the whole-body insulation
measured in air and in water. Morrison 35 a1. (1974) found that the
minimum thermal conductance for sea otters in water at a critical
temperature of about 7°C was 2.1 times greater than that in air at a
critical temperature less than -19°C. In the present study, maximal
insulation for muskrats in air was found to be 2.4 fold over that in
water at 25°C. The total insulation of harbor seals during the summer
was reported to be 2.1 times greater in air than in water at lower
critical temperatures of 2 and 20°C, respectively (Hart and Irving,

1959). Both the Adelie penguin (Pygoscelis adeliae) and Gentoo penguin

 

(F. 23223) were shown to have insulations in air at 0°C approximately
1.5 times greater than those in water at 5°C (Kooyman et 31., 1976).
Morhardt;e£_§l. (1975) demonstrated that the rate of heat loss for
small birds (Junco hyemalis, Passer domesticus) and rodents (Rattus

norvegicus albino, Spermophilus beldingi, Heteromys desmaresteanus)

 

 

immersed in water were 5 to 10 times as great as in air. The greater
augmentation of heat loss from these animals, compared to semi-aquatic
animals, would be expected due to the absence of specific adaptations
of insulation to minimize the cooling effect of water. The water shrew

(Sorex palustris), with a thermal conductance in water 4.5 times that

 

in air, was found to differ in conductance from other shrews and small

rodents only as a function of body size (Calder, 1969).

31

During testing, some of the muskrats were found to have tail
temperatures which remained close to T3 for times of 5 hr or more. I
am hesitant to believe that all blood flow is curtailed to the appen-
dages for extended periods of time when their temperatures are equal
to Ta' Although the heterothermic tissues of the appendage are still
viable at low Ta's (Miller, 1970), and operating at a lower metabolic
rate, it might be advantageous to allow circulatory exchange with the
body proper to occur. Circulation to the extremities could persist to
allow for metabolic exchange while preventing undue heat loss by the
use of a counter-current heat exchanger. This type of system for
the muskrat would be similar in principle to the heat exchanger
described by Scholander (1957). In such a system, arteries and veins
run in close proximity to one another, thus allowing heat to be picked
up from the arterial blood by the venous blood and short-circuiting the
transfer of heat to the distal part of the appendage. This permits the
retention of body heat without significant loss to the environment
through the poorly insulated appendages. Further, heat may be
dissipated across the appendages when appropriate by shunting warm
blood from the arteries to superficial veins. This by-passes the heat
exchanger and promotes heat transfer with the environment. Scholander
and Schevell (1955) described such an arrangement in the flukes of
porpoises. In this case, the counter-current exchanger consisted of a
central artery with a surrounding ring of veins. The arrangement is
such that when a large heat load must be dissipated, the blood pressure
rise increases the diameter of the central artery, collapsing the venous
ring, and reducing the effectiveness of counter-current heat exchange.

The warm arterial blood is forced to return to the body through

32

superficial veins near the skin, which are normally constricted.
Similar circulatory patterns have been described in the flippers of the
northern fur seal and harbor seal, with thermoregulatory implications
(Tarasoff and Fisher, 1970).

Irving and Krog (1955) were first to propose the existence of
a counter-current heat exchanger in the tail of the muskrat. They
based their conclusion on the occurrence of a sharp temperature
gradient in the insulated base of the tail after the tail had been
immersed in cold water. Thorington (1966) demonstrated that
counter-current heat exchangers were common in the tails of a variety
of rodents. Morphological characteristics in rodent tails, which were
interpreted to function in thermoregulation, are the presence of shunts
and anastomoses between arteries and veins, juxtaposition of arteries
and veins, the presence of superficial and deep routes of venous
return, and the distribution of valves in veins and arteriovenous
anastomoses. The juxtaposition of arteries and veins would allow for
the establishment of a heat transfer mechanism with heat exchange
between the arterial and venous blood flows, retaining heat in the
body. Arteriovenous anastomoses would function to shunt warm arterial
blood to the superficial veins allowing for rapid heat dissipation.
Although Thorington did not study the tail of the muskrat, because of
the commonality of counter-current heat exchangers in a variety of
diverse rodents, it would be logical to assume that such a morphological
system exists in the muskrat. Latex injections which I performed on
the arterial and venous systems of the muskrat tail have shown a
similar configuration of the vascular network to the configurations

in tails described by Thorington (1966). Of particular interest is the

33

presence of juxtaposition arteries and veins. Two central caudal
veins were found to be dorso-lateral to the ventral caudal artery and
in direct contact with the artery along the caudal vertebrae in the
well insulated section of the tail. Numerous veno-venous shunts
occurred between the two veins across the ventral side of the artery.
The arterial system was elaborate with numerous branches and shunts
along the length of the tail, while the venous system was shown to
have superficial routes. The preceeding anatomical evidence hints at
the possibility of a counter-current heat exchanger present in the
muskrat tail, although further morphological research is necessary.

The results of this study indicate that changes in the
temperature of various body regions, especially the appendages, are
inversely associated with changes in whole-body insulation.
Appendicular temperatures approaching Ta tend to maximize the insulation
of the body by reducing the rate of heat loss per unit of surface area.
High appendicular temperatures, such as those observed in air at 30°C,
indicated increased peripheral blood flow, and probably accounted for
the sharp reduction in insulation, facilitating heat loss. This was
most likely in response to the high central body temperatures
representing a large heat load acquired by the muskrat. Such a situation
may arise naturally due to high Ta’ or increased metabolic heat
production and storage during exercise, in which heat loss to the
environment would occur through the appendages with a reduction in the
over-all insulation. The higher thermal conductivity of water over
air was surmised to be the causative factor in lower regional and

central body temperatures, decreased whole-body insulation, and

34

increased weight-specific metabolic rates for muskrats in water as
compared to the same animals in air.

Thus regional heterothermia, as occurs in the appendages of the
muskrat, appears to serve as a heat regulator in which high peripheral
temperatures, due to vasodilation, allow for increased heat dissipation,
and low peripheral temperatures, because of vasoconstriction or
counter-current heat exchangers, maximize heat conservation. This is
important in that the sparsely haired appendages, as a result of their
relatively large surface area, represent a major avenue for heat
transfer from the body with its highly insulative pelage. Therefore,
it would appear that regional heterothermia plays a necessary role in
the thermal ecology of the muskrat, as a semi-aquatic homeotherm, by
contributing to changes in whole-body insulation in response to a
variable environment.

In summary, it has been demonstrated that there is a difference
in the response of regional body temperatures of muskrats in air and in
water, as well as an increase in the metabolic rate and decrease in the
whole-body insulation in muskrats in water compared to those in air, and
an inverse correlation between the temperature of the appendages and the
whole-body insulation. Although it has often been inferred that
changes in the temperature of the appendages may act to change the
insulation of the body, this phenomenon has never been demonstrated
for a semi-aquatic homeotherm in relation to its environment. It is
presumed that the higher thermal conductance of water over that of air
is responsible for the difference in the physiological adjustments

made by the muskrat in that the pelage insulation alone is

35

insufficient to prevent general body cooling. Conversely, the pelage

is capable of retarding heat loss from the body at high ambient
temperatures in air and during exercise when heat storage would be
deleterious to the muskrat. Thus the appendages of the muskrat appear
to serve in thermoregulation allowing for both heat conservation and
dissipation as required by the thermal state of the animal and the
environment. The results of this study, while reinforcing the findings
of previous studies, have increased our understanding of the role of
regional heterothermia for a small semi-aquatic mammal, for which little

is physiologically known.

APPENDIX A

REGIONAL BODY TEMPERATURE

 

 

 

Table 2. Mean regional body temperatures (i one standard error) for
all muskrats exposed to environmental media of air and water
at Ta's of 20, 25, and 30°C.

T

Body Environmental a
Region Medium 20°C 25°C 30°C

Air 37.1 i 38.0 i 0. 39.1 i 0.2
Colon

Water 33.6 i 36.4 t 0. 37.4 i 0.4

Air 36.0 i 37.4 i 0. 38.8 i 0.3
Dorsal Skin

Water 33.4 i 36.1 i O. 37.3 i 0.5

Air 27.1 i 30.9 i 1. 35.7 i 0.5
Foreleg

Water 20.3 i 25.5 i 0. 30.7 i 0.3

Air 23.3 i 25.9 i 0. 35.4 i 0.8
Hindfoot

Water 20.1 i 25.2 i 0. 30.1 i 0.1

Air 20.8 i 27.1 i 1. 37.2 i 0.3
Proximal Tail

Water 20.2 i 25.3 i 0. 30.1 i 0.1

Air 20.2 i 26.4 i 1 36.5 i 0.3
Distal Tail

Water 20.2 i 25.2 i 0. 30.1 i 0.1

36

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