COMPARATIVE PHYSIOLOGY
OF TEMPERATURE REGULATION
PART 2
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JOHN P. HANNON
ELEANOR VIERECK
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ARCTIC AEROMEDICAL LABORATORY
FORT WAINWRIGHT
ALASKA
1962
COMPARATIVE PHYSIOLOGY
OF TEMPERATURE REGULATION
PART 2
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JOHN P. HANNON
ELEANOR VIERECK
QP
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ARCTIC AEROMEDICAL LABORATORY
FORT WAINWRIGHT
ALASKA
1962
THE HETEROTHERMOUS CONDITION OF THE
TISSUES OF WARM-BLOODED ANIMALS
Laurence Irving
Appreciation for the universality of physical laws Degan to de-
velop toward the close of the eighteenth century as the metabolic
production of animal heat was ascribed to combustion. Lavoisier
(1777) estimated that the heat caused by formation of the carbon di-
oxide expired by a rabbit was nearly equivalentto the heat which the
animal gave off to a calorimeter, and he confidently attributed the
production of heat by animals to processes of oxidation.
In 1840 Julius RobertMayer, a young physician in Java, followed
the then prevailing custom of bleeding sailors as they arrived in a
tropical port. When he observed that the venous blood appeared ar-
terial red he consulted with a colleague and was informed that in
Java venous blood appeared arterial in color. His imagination led
him to think that the diminished need for metabolic heat in a tropi-
cal climate brought about less reduction of oxygen in the venous
blood than was usual in a colder climate. Reflecting upon this dubious
explanation, he was led to produce comprehensive physiological and
astronomical illustrations of the transformation of energy, from
which he developed the general view of the conservation of energy
(Tyndall, 1898). Mayer's explanation of the color of venous blood
does not sound valid, however, for people in warm and cold climates
have about the same basal production of heat, adjusting the elimina-
tion of heat to the climate by varying the circulation and temperature
in their skin.
ARCTIC CLIMATE
Cold northern climates are advantageous for studying thermal
reactions of animals because the winter weather is so much cokier
than the bodies of warm-blooded animals. Over the northern interior
of Asia and America extreme seasonal changes occur. At Allakaket
133
IBVING
in the Koyukuk Valley of interior Alaska just north of the arctic cir-
cle the lowest temperature during the mild winter of 1959 was -59
G, and the warmest day in June was +29 C. On April 3, -36 G was
recorded, and on April 11, the temperature rose to +13 G (U, S.
Weather Bureau, 1960). Residents of the Arctic encounter large an-
nual variations and precipitous rise of temperature in spring.
Stable Physiology of Arctic Populations
History indicates the presence of Eskimo people in the American
arctic for 1,000 years before the first Norse settlers described them
in southwest Greenland. Archaeological study of flint implements in-
dicates that an Eskimo type of culture has been in the American Arc-
tic for 2,000 years, and the ancestry of the Eskimo race in Alaska is
probably as old as the traces of its culture. The stability of these
people shows that their arctic existence was not uncertain and that
it was secured by good adaptation to arctic life.
Relics of mammals indicate that species now living have been
stable in form for several hundred thousand years. In the last part
of this period drastic climatic changes have occurred; 6,000 years
ago the north was warmer than now, and some 20,000 years ago most
of Ganada and much of Alaska was thickly covered by great ice
fields. The ancestors of arctic animals have been exposed to pro-
nounced variations in climate during a few thousand years. Although
many generations succeeded each other in that time, the evolution of
new species is not apparent. The arctic species must have long pos-
sessed physiological characteristics which were adaptable without
evolutionary change inform to the recent climatic variations through
which they have successfully passed.
Although relics of animals of the past provide little direct evi-
dence about their physiology, systematic comparisons of physiologi-
cal characteristics indicate that the principal mamm alian and avian
thermal processes have been stable since nearly the origin of the
warm-blooded habit. In arctic Alaska JohnKrogandl (1954) found a
fair sample of thefewspeciesof arctic mammals and resident birds
and observed that their body temperatures did not differ significantly
from those of animals of warmer climates. In fact among all of the
134
HETEROTHERMY IN HOMEOTHERMS
WORLD
CLIM4TES
• RANGE OF
ADAPTATION
,:: T
200 • IHOS
... i
TV'
Figure 1. Temperature ranges for which warm-blooded animals
are physiologically adapted compared with those of the world's cli-
mates. Redrawn from Figure 16. page 33, 'TBI rds of Anaktuvuk Pass.
Kobuk, aal Old Crow." BuUetln 217, U. S. National Museum. 1960.
Figure 2. Mean body temperature of arctic and subarctic birds
and mammals. Figure 6, page 677, "Body Temperatures of Arctic
and Subarctic Blnls and Mammals." JAP. 6(ll):667-680. 1954.
135
IRVING
species of mammals that regulate their temperature well when at
rest, there is a differenceof only afew degrees. Body temperatures
do not now differ geographically, and the comparative view indicates
that little scope for variation in warm body temperature has oc-
curred in the courseof evolution. There maybe evidence for ancient
separate development of warm body temper atiore in birds and mam-
mals, but the heat producing machines of the two warm-blooded
classes operate at nearly the same temperature. The reptilian meta-
bolic system was already so elaborately developed that its evolution-
ary modification for warmer operation was limited within a narrow
range of temperature (Fig. 2).
Economy of Heat Among Arctic Animals
Watching the caribou inwinter in Alaska, I have been impressed
by the large amount of time that they expend resting and carrying on
individual and social activities that bring them no food, for while liv-
ing in warmer climates I had thought that arctic mammals must feed
diligently in order to combat the arctic cold with metabolic heat. But
Scholander and I (1950a) found at the Arctic Research Laboratory
that even in the coldest temperatures the warmth of well- insulated
arctic birds and mammals could be sustained with metabolism at the
resting rate. Because of this economy the cost of maintaining bodily
heat for existence in arctic cold does not exceed the metabolic cost
of living in warm climates. Insulation adaptive to the vicissitudes of
the arctic climate opens the north for occupation by warm-blooded
animals without economic handicap.
Natural populations of birds and mammals including man engage
in a great variety of time-consuming individual and social activities
which organize their societies in order to pursue their annual pro-
grams. Although these programs differ to suit seasons in various
environments, the organization of avian and mammalian populations
demands so large a share of each individual's time that only limited
periods can be utilized for feeding without endangering the structure
of the population, which is as complex in the arctic as in milder cli-
mates.
136
HETEEOTHERMY IN HOMEOTHEBMS
The Variable Insulation of Arctic Animals
The thick fur of arctic animals is obviously an insulator that
protects them from excessive loss of heat (Scholander et al., 1950b).
In fact fur is so effective an insulator that a man clothed in winter
caribou (Rangifer tarandus) fur becomes overheated when he walks ,
and we do not yet know how animals with thick fur get rid of the heat
generated by their long, swift running. A portal for the exit of sur-
plus metabolic heat is provided by the thin covering of the limbs and
noses. When active, these extremities become nearly as warm as the
body, but at rest their skin cools. We found that the bare skin of the
toe pads of arctic sled dogs and the hooves of caribou at rest might
be near the freezing temperature. The large webbed feet of Alaskan
Glaucous- winged Gulls (Larus hyperboreus) arenearly ascold as the
icy water in which they swim (Irving and Krog, 1955). When we tried
to measure the heat emitteci to cold water from the extensive webbed
foot of an Arctic Gull, the amount was so small that at first we re-
garded the results withsuspicion(Scholanderetal., 1950b) (Fig. 3).
Effective conservation of heatby cold skin is shown by the cold-
ness of the entire surfaces of swine (Sus scrofa) in Alaskan winter
weather (Irving, 1956). Thevalue of their cool skin as an insulator is
apparent in the practicability of raising hogs outdoors in Alaska,
where our estimate indicated that they consumed about the same a-
mount of food as in temperate climates (Irving, Peyton, and Monson,
1956).
An even more impressive indication of the insulating effective-
ness of changing the temperature ofbare skin was shown by the hair
seals (Phoca vitulina and P. groenlandica) that J. S. Hart and I ex-
amined in winter atSt. Andrews, N.B. (Irving and Hart, 1957). In ice
water their skin was only a degree warmer than the surrounding
water, and their metabolic production of heat was little greater than
in warm air. Thus cooling of bare skin provides insulation against
excessive loss of heat in arctic waters , which have the greatest ca-
pacity of any inhabited environment for removing heat. This thermal
economy allows great numbers of seals, walrus, and narwhals to live
throughout the year in the icy arctic seas.
137
IRVING
GULL
4.9° TO 0 0'
4.8°T0 26'
Figure 3. Topographic distribution of superficial temperatures in the leg of a
gull (Larus glaucescens). Figure 9, page 361, "Temperature of Skin in the Arctic
as a Regulator of Heat," JAP. 7(4) :3 55-364. 1955.
138
HETEROTHEBMY IN HOMEOTHERMS
It is an interesting indication of the general pattern of climatic
adaptability of animals that while land animals shed fur in summer,
northern harbor seals (Phoca vitulina) lose part of their physiologi-
cal insulation in warm summer water at Woods Hole (Hart and Irv-
ing, 1959). As furcovered mammals vary the thickness of their coats
to suit the season, seals reduce the effectiveness of their physiologi-
cal insulation inwarm weather. A number of examples illustrate that
thermal adaptations of individuals are reduced as well as enhanced
to suit seasonal climates.
Varying temperature of superficial tissues can thus efficiently
adapt warm-blooded heat producing machines to operate economic-
ally in a variety of environments. In fact heat producing machines
cannot work without thermal gradients. Until we examined arctic ani-
mals, however, I did not appreciate the extent of the swift changes in
the thermal gradients of the tissues of warm-blooded animals. Now
I find this variability in tissue temperature to be one of the most in-
teresting characteristics of warm-blooded life, and Isuspectthat it
is the primary insulator of the warm-blooded mechanism and that
fur and feathers are secondary developments.
At the start of intense activity in cold weather bare skin may
suddenly warm to nearly 40 C and then cool when rest is resumed.
From measurements of thermal gradients extending for 6 to 8 cm
beneath the skin surface in swine and seals, we have found that large
masses of tissues are frequently involved in extensive thermal
changes. In the temporal and topographic variations of superficial
temperature, the warm-blooded animals differ fundamentally from
the cold-blooded kinds. In warm-blooded forms only the center is re-
latively homeothermous, while the organism is heterothermous .
Variations With Temperature in Activities of Cold- and Warm-
Blooded Animals
In summer on the tundra near the arctic coast of Alaska at Bar-
row, I noticed that when the sun shone intermittently through the
clouds, the flies (Grensia) which I was pursuing escaped by flying.
When the sun was covered by a cloud the flies became grounded,
slow, crawling insects that I could easily catch. I inserted fine ther-
mocouples in several of the flies and found that in shade they were
139
lEVING
o o
about 8 C and in sunshine they warmed to 12 C. The change of a
few degrees converted the flies from slow, crawling to alert, flying
organisms.
Not only do habits of living change critically in cold-blooded ani-
mals at certain temperatures, but many measurable physiological
frequencies and velocities of their activities commonly double in
warming 10 C. Aquatic cold-blooded animals do not usually survive
the quick changes through which heterothermous tissues of northern
warm-blooded animals rapidly and frequently pass, but some north-
ern terrestrial insects can survive large and swift changes in tem-
perature. If their activity changed continuously from 0 C to 40 C
with the common Q of two, it would increase 16-fold, but the dis-
continuity in activity seen in the tundra flies shows that critical tran-
sitions in their cold-blooded activity occur at certain temperatures
and drastically alter their manner of living.
The physiological systems of cold-blooded animals do not oper-
ate consistentlyoverwide ranges of temperature, but the heterother-
mous superficial tissues of birds and mammals act in continuous
coordination with the homeothermous centers so that each animal
steadfastly remains one individual operating in its characteristic
manner. This integrated action of heterothermous tissues maybe the
most informative distinction between warm- and cold-blooded life.
CXir knowledge about processes in the heterothermous tissues of
warm-blooded animals is too sparse to provide profitable speculation
on how they are integrated in the continuous life of individual organ-
isms, but I can add some examples of heterothermous operation in
the adaptative reactions to cold of people living in northern climates.
Cooling of Hands and Feet of People Adapted to Cold
A few years ago I was fortunate in making the acquaintance of
members of a sect accustomed to going with light clothing and bare
feet in Alaska. Two of their members who were university students
have helped us to understand some thermal reactions by their ability
to manifest and describe their adaptation to cold (Irving, 1959). While
140
HETEROTHERMY IN HOMEOTHERMS
one student was sitting for 100 minutes in sparse clothing in a room
at 0 G, a toe cooled, in 40 minutes, below 10 G and then warmed in
two typicalslowwarmingcycles.Thetoesofthe other student cooled
to 5 G at 65 minutes and were colder for the remainder of the 100
minute test period. Duringthetests the students studied for examin-
ations and neither expressed or showed much disturbance by the
o
cold. At 6 G the toes of one became insensitive to light touch, but
both individuals remained sensitive and alert to small thermal
o
changes when their toes were 8 G. One of them notified me that a
certain toe was rewarming while its change was recorded from
0 o
10.0 G to 10 .2 G and remarked upon similarly small cooling before
the change was recorded. 1 suspect that their peripheral circulation
is carefully monitored through alert sensations of temperature. Ex-
posure to cold must train the conscious and unconscious observation
of temperature for precise and vigorous reaction to meet temporal
and topographic requirements (Fig. 4).
In the same condition and similar scant clothing, the toes of a
young airman, who had been for two years an assistant in the Aero-
medical Laboratory at Ladd Air Force Base, Alaska, cooled to 10
C in eight minutes and were very uncomfortable. At 14 minutes they
were very painful, and his general discomfort became so great in
41 minutes that 1 asked him to give up for fear that his violent shi-
vering would be injurious (Fig. 5) .
1 was at first unimpressed when one of the students told me that
he had noticed sweating in his armpits while he was exposed to cold.
When the adhesive tape holding thermocouples to a finger and toe
were removed after his cold test, he pointed to droplets of sweat on
rewarming fingers that had not yet reached 20 G, Airman Henson
also looked for and showed me droplets of sweat on his fingers and
toes as he was rewarming but still shivering. The paradoxical ap-
pearance of sweat on cold skin may give a clue to a common process
of regulation in the simultaneous sweating and warming of cold tis-
sues.
In their two years in Alaska the two students had developed the
ability to work undisturbed while exposed to cold that we could not
stand. Although they felt no pain in fingers and toes so cold as to be
extremely painful for a person unpracticed in exposure, their
141
IRVING
Figure 4. Temperature on skin of a young man accustomed to light clothing,
bare feet and hands. Figure 1, "Human Adaptation to Cold." Nature. 185(4713):
572-574. 1960. Macmillan and Co., St. Martins Street, London, W. C. 2.
JC"
^'-'^'' ———<< ^
SHIVER ,^^/\
,WAVWWVVA^
10'
FmuR „
TOE
^^
0'
--^^
OnmmtIO 20 30 40
Figure 5. Temperature on skin of a young airman
accustomed to regular military clothing. Figure 2,
"Human Adaptation to Cold." Nature. 185(4713) :57 2-
574. 1960.
142
HETEROTHERMY IN HOMEOTHERMS
thermal sensations were not numbed but remained alert. Their toler-
ance of cold appears to be an active accomplishment and not the re-
sult of insensitivity. I think it is right to say that they are adapted to
cold, because their accurately developed reactions enable them to
achieve the simplicity and comfort that they seek by wearing light
clothing.
Reactions of Eskimos' Hands to Cooling
Since we are biologists we should look for adaptation as a f\mc-
tion of populations and not look merely in the samples of young men
whom we usually test. But it is hard enough to make observations on
vigorous young men when they are exposed to cold, and experimental
exposure to cold might appear to be cruel treatment of delicate wo-
men and frail children. Since 19 47 1 have of ten enjoyed the good com-
pany and been aided by the intelligent appreciation of arctic life of
the vigorous Nunamiut Eskimos who live by hunting caribou in the
mountains of arctic Alaska. While we were visiting with Simon Pan-
eak and his pleasant family at Anaktuvuk Pass last March, Keith knd
Jo Ann Miller and I were able to examine the reactions of a sample
of the population to cold. The men wear warm fur clothing while
traveling, hunting, and working. Their small children set out to play
in warm clothing, but in excited enjoyment of their strenuous sport
they may play for hours after they have lost their mitts and after
their disordered clothing becomes infiltrated with snow. It was no
problem to get them to sit outside in air temperatures just below
freezing with bare hands while we observed them from the comfort
of the sod house (Figs. 6-11).
The hands of five Eskimo men and two young ladies remained a
little warmer than those of three white men and two ladies. I think it
is significant that the hands of the adult Eskimos showed marked re-
warming reactions earlier than the white people, for we had noticed
that when immersed in cold water the hands of Indian men at Old
Crow began to rewarm earlier than the hands of the white men whom
we tested there (Eisner, Nelms, and Irving, 1960). The tiny fingers
of the tough little Eskimoboys cooled rapidly and very quickly began
rewarming cycles which continued at short intervals as lively as
their play. The boys' hands were often colder than 10 C.
143
IRVING
Figure 6. Nunamiut Eskimo camp at Chandler Lake, Brooks Range, Alaska,
November, 1947. Photo by Laurence Irving.
Figure 7. Nunamiut Frank Rulland, Simon Paneak, and Jesse Ahgook with P. F.
Scholander, Chandler Lake, November, 1947. Science. 107(2777): Cover. Photo by
Laurence Irving, 1515 Massachusetts Ave., NW Washington .S. D. C.
Figure 8. Nunamiut boys with Jo Ann Miller at Anaktuvuk Pass, March, 1960.
Photo by Keith Miller.
144
HETEROTHERMY IN HOMEOTHERMS
^
Figure 9. Nunamiut boy at play, Anaktuvuk Pass, March, I960. Photo by Keith
Miller.
^^^
Figure 10. Nunamiut boy after losing gloves at play, Anaktuvuk Pass, March,
I960. Photo by Keith Miller.
Figure 11. William Tobuk with hands exposed for cold test, Bettles, March,
1960. Photo by Keith Miller.
145
IRVING
Another important difference was in the expression of pain. Most
white people find fingers around 10 C painful, and our white subjects
spoke very plainly about the cold as disturbingly painful. The two Es-
kimo young ladies said their fingers pained a little. The Eskimo men
and boys did not openly express or demonstrate pain or appear anxi-
ous to terminate the test as did the white people; but on questioning
two of the nine said their fingers became a little painful. Most of the
Eskimos said, however, that their hands became very cold. Keith
Miller is now analysing records obtained at the Arctic Research
Laboratory, Barrow, during exposureof hands to justbelow freezing
air in 12 Eskimo men, 4 women, 15 children, and 14 white men, 7
of whom were accustomed to work outdoors. His records substan-
tiate with details the general impressions gained from Eskimos at
Anaktuvuk Pass.
With fingers so cold that the pain would have disturbed us the
Eskimos seemed undisturbed. But the lively thermal reactions of the
Eskimo boys showed that their vasomotor regulation was sensitive.
After they had been happily and noisily at play for several hours
their hands were so cold as to appear beyond our safe tolerance. Al-
though they do not appear to depend upon warning by pain they
cannot be insensitive to cold, for when the children's fingers verge
upon dangerous cold conscious and unconscious attention for re-
warming must be especially accurately controlled in order to pro-
tect the little fingers with their relatively feeble supply of heat.
Eskimos cannot safely expose their hands to severe arctic cold
longer than a few minutes; therefore this adaptation of part of the
surface of Eskimos is small in comparison with the degree and ex-
tent of the adaptation of the extremities of arctic animals. But even
this small adaptation extends their ability to work sufficiently to al-
low for many essential acts which can only be performed with hands
unencumbered by mitts. That frostbite is so rare among Eskimos
is the result of their keen conscious and unconscious appreciation
for the limits of time and intensity of cooling that they can endure.
Oberservations on the Integration of Heterothermous Tissues
For individual existence to be coherent it must be continuously
related to information about its internal condition and external cir-
cumstances. Apparently an individual must always appreciate certain
146
HETEBOTHERMY IN HOMEOTHEBMS
physical dimensions in absolute terms. For example, the force re-
quired to move the mass of alegdoes not change with temperature,
but physiological processes involved in sensory detection of physical
forces do change with temperature. Mammals and birds ap-
pear to differ from the cold-blooded animal, however, in the large
inconstancy of temperature in superficial tissues and in the integra-
tion of individuality in this heterothermous condition.
After seeing that the fingers of people adapted to cold were use-
fully coordinated when very cold, I have been trying to find a per-
tinent measure for their sensitivity. It seemed to me that terrestrial
animals would need constant appreciation for force and mass in
order to move. Stimulation by impact is a convenient test because
mass and the distance through which it falls can easily be varied and
measured.
Cabbage seeds selected for uniform weight, about a miligram,
were found detectable after falling about 20 mm onto the ball of the
warm mid- finger. The impact of a seed of double the size was no-
ticeable after falling 10 mm, or the threshold for stimulation varied
about as the kinetic energy of the impact. Other parts of the skin
differed in sensitivity, and as the skin was cooled, a heavier weight
or longer fall was required for the impact to be detectable.
It was easier to discharge mercury droplets weighing from 1 to
3 mg by Scholander's micrometer burette which, with a plunger 1.59
mm in diameter, measured volumetrically the drop discharged
through a hypodermic needle to within a few hundredths of a milli-
gram. The kinetic energy of the impact on the ball of my middle fin-
ger that I could just detect increased rather regularly about eight
times as my finger was cooled from 35 C to 20 C (Fig. 12).
Keith Miller is now using small steel ballbearings for weights
and finding that when measured as kinetic energy of detectable im-
pact the threshold stimulus increases regularly in a trained subject
as the skin cools. Individuals differ in sensitivity and in the rate of
diminishing sensitivity with cold. We have not discovered whether
this measure of sensitivity of cold fingers will distinguish differ-
ences in the people accustomed to cold whom we regard as adapted.
147
IBVING
r300 ERGS/G-
200
-100
20
__L_
Figure 12. Change in threshold with temperature for detection of impact on the
ball of one individual's finger. Abscissa:temperature of skin of fingertip. Ordinate:
impact of falling droplet of mercury. Unpublished.
148
HETEROTHEPMY IN HOMEOTHEEMS
The report of sensation involves complex neural mechanisms
which we cannot analyze physiologically. Since only part of the hand
or of a finger is cooled and we cannot control effectively the amount
of tissue cooled, we suspect that the regular thresholds observed in
day after day tests indicate that cooling of the hand affects the local
peripheral agents of sensation. But we are still only measuring a
threshold and not the sensation that is involved in our estimation of
the physical dimensions of stimulation. It is nevertheless interesting
to consider this test an illustration of the integration of heterother-
mous tissues in an individual organism. Certain characteristics of
the external world must be appreciated in constant dimensions, and
yet the signals for those dimensions are submitted through peripher-
al transducers that change characteristics as the tissues which con-
tain them warm and cool.
In comparison with thenaturaladaptationof animals to cold, the
best physiological adaptation developed in people is only of small
magnitude, and cultivated human habits and economy provide the
main protection from cold. Some people resident in cold climates
are motivated to utilize to the utmost their small physiological a-
daptability to cold. They find it worthwhile to practice exposure that
seems very unpleasant for us who are accustomed to sheltered urban
life. We face the test of cold with anxiety and respond in the irregu-
lar manner that characterizes untrained physiological reactions.
Power and equipment from foreign sources are used to relieve
soldiers and transient workers in the north from adaptation to its
cold climates. In each successive war in history power and tech-
nology have improved the protection of armies from cold and en-
abled them to live and move effectively in any climate and on any
terrain. In spite of improving protection from the weather it is sur-
prising that in every war winter cold blocks operations in the field
and continues to be a major cause of injury. The reason lies in de-
pendence upon power susceptible to accidental disruption. Military
tactics aim to damage the enemy's vulnerable heating system or to
lead him into a position where its effectiveness diminishes. Then
troops accustomed to shelteringwarmth are immobilized by the pro-
tection that has left them inexperienced in cold, while those less de-
pendent upon artificial warmth may retain a small but decisive abil-
ity to maneuver.
149
IRVING
The necessity for independence requires Eskimo populations
to utilize their adaptability inwinter. Even the limited human physi-
ological adaptation is important in the natural economy of arctic life,
and it is interesting to see how this adaptation is used by the Eskimo
children for enjoyment of their environment. If it were considered
worthwhile we could doubtless dispense with some of the expensive
protection from cold that complicates living and restricts our ex-
perience. Whether or not physiological adaptation to cold is economi-
cal, I hope that some people will continue to practice ways leading to
adaptation so that by their reactions we can gain insight into the in-
teresting physiological components that appear in human adaptation
to cold.
150
HETEEOTHERMY IN HOMEOTHEEMS
Subject Age Air
(°C)
Rewarming
(Minute)
Pain
(Minute)
Body
White:
LI
65
- 6
J LA
39
-11
NG
22
-15
AB
40
- 7
JAM
26
- 6
Eskimo:
JR
31
- 9
CH
45
-14
RN
36
-12
Robt.P
23
- 5
Ray P
20
- 4
MP
19
- 9
RM
20
- 8
HH
11
-18
GP
11
-16
WT
12
-12
Roos.P
14
-16
9
12
10
17
_6_
10
5
8
10
4
8
5
J_
7
1
0
1
J_
1
10
moderate
Warm
8
severe
Warm
17
moderate
Warm
14
moderate
Warm
3
moderate
Warm
Warm
Warm
Shivering
Shivering
Shivering
17 nnoderate Warm
3, 21 moderate Shivering
Warm
Warm
Shivering
Warm
Table I.
151
LITERATURE CITED
1. Eisner, R., J. D. Nelms, and L.Irving. 1960. Circulation of heat
to the hands of arctic Indians. J. Appl. Physiol. 15(4):662-666.
2. Hart, J. S. and L.Irving. 1959. The energetics of harbor seals in
air and in water with special consideration of seasonal
changes. Can. J. Zool. 37:447-457.
3. Irving, L. 1956. Physiological insulation of swine as bare-
skinned mammals. J. Appl. Physiol. 9(3) :4l4-420.
4. Irving, L. 1959. Human adaptation to cold. Nature 18 5(47 13): 572-
574.
5. Irving, L. and J. S.Hart. 19 57. The metabolism and insulation of
seals as bare-skinned mammals in cold water. Can. J. Zool.
35:497-511.
6. Irving, L. and John Krog. 19 54. Body temperatures of arctic and
subarctic birds and mammals. J. Appl. Physiol. 6(11) :667-
680.
7. Irving, L. 1955. Temperatureof skin in the Arctic as a regulator
of heat. J. Appl. Physiol. 7:355-364.
8. Irving, L., L. Peyton, and M. Monson. 1956. Metabolism and in-
sulation of swine as bare-skinned mammals. J. Appl. Physiol.
9(3):421-426.
9. Lavoisier, A. L. 1777. Experiences sur la respiration des ani-
maux et sur les changements qui arrivent a I'air en passant
par leur poumon. Mem. Acad. Sci. Paris, 1777, p. 185.
(Oeuvres de Lavoisier, vol. 2, p. 174).
152
HETEFOTHEBMY IN HOMEOTHEEMS
10. Scholander, P. F., R. Hock, V. Walters, and L. Irving. 19 50a.
Adaptations to cold in arctic and tropical mammals and birds
in relation to body temperature, insulation, and basal meta-
bolic rate. Biol. Bull. 99(2):259-271.
11. Scholander, P. F., R. Hock, V. Walters, and L. Irving. 1950b.
Body insulation of some arctic and tropical mammals and
birds. Biol. Bull. 99(2):225-236.
12. Tyndall, J. 1898. Fragments of Science, Vol. 1, p. 428, New
York.
13. U. S. Dept. of Commerce. 1959. Climatological data, Alaska,
Asheville.
153
IBVING
DISCUSSION
MILLER: As Dr. Irving stated, Figure 13 summarizes one
aspect of a study made at Barrow late last winter mvolving Eskimo
and white subjects. Several of the whites were normally cold-
exposed to a considerable extent, while others received little if
any cold exposure. In Figure 13 you see finger cooling rates of
Eskimo girls, aged about 11 to 12, Eskimo boys of the same age,
outdoor or cold- exposed whites, and indoor, non- cold- exposed whites
and Eskimo adults with varying degrees of cold exposure. The lines
connect points representing cooling rates of five different fingers
averaged for the individuals in each group. Cooling rates were cal-
culated from temperature determinations made at 30 -second inter-
vals during an initial five- minute cooling period. There appears to
be a definite relationship between hand volume and the initial five-
minute cooling rate. The smaller fingers of the children show a
more rapid initial cooling rate than the adult fingers. Ignoring the
group of indoor or non-cold- accustomed whites for the moment,
it may be seen that the relationship between initial cooling rate and
hand volume among the various groups is approximately linear,
the cooling rate being decreased with increasing hand volume. The
most striking feature exhibited by the slide is the fact that the
indoor non- cold- exposed white group exhibits an anomalously high
cooling rate in comparison with adult Eskimos and cold-exposed
whites. This more rapid cooling rate is most prominent in the little
finger, although it is exhibited to a noticeable degree even by the
thumb. Another point of interest is the degree of variation among
different fingers within each subject group. Variation among cool-
ing rates of different fingers is greatest in the group with the
smallest hand size, the Eskimo girls, and decreases steadily with
increasing hand volume, again with the exception of the indoor
whites. The degree of variation within the whites not accustomed
to cold was almost identical to that of the Eskimo uoys. The fact
that white men not accustomed to cold exhibited a finger cooling
response significantly different from that of Eskimo men, despite
almost identical average hand volumes, would seem to indicate that a
difference in circulatory response to hand cooling is present between
the two groups. Whether this difference, if real, is due entirely
154
HETEBOTHEPMY IN HOMEOTHEPMS
4.0
3.0
<
cr 2.0
100
LEFT LITTLE
INDEX
MIDDLE
INDOOR RIGHT MIDDLE
WHIT^ES (7) " THUMB
GIRLS (4)
OUTDOOR
WHITES (4) A
ESKIMO
200 300
HAND VOLUME (ml.)
J I
400
500
Figure 13. Initial (5 minute) cooling rates of various fingers of Eskimos and
Whites plotted as a function of average hand volume.
155
IRVING
to group differences in regard to previous cold experience, I
would not wish to say atthis time. The exposure temperatures were
from -5° C and -10 C.
EAGAN: Is it possible that whites who worked indoors could
afford more expensive clothing?
MILLER; No, not unless you want to insult all the members of
the Arctic Reseaixsh Lab.
HART: Were the hands exposed in open air?
MILLER: Yes.
MORRISON; Is the larger hand volume characteristic of the
Eskimos?
MILLER: No, it is not significantly larger. There is just a very
slight difference.
MORRISON: It is 10% which would seem to be an appreciable
amount.
MILLER: But it does not appear to be statistically important.
It is a relatively small group.
HUDSON; Are there any changes in blood flow?
MILLER: I did not make any determinations of blood flow, but
other people have correlated blood flow changes with adaptation in
Eskimos by cooling them in water. This is, more or less, a compli-
mentary study, using air cooling.
EAGAN: I would like to ask Dr. Irving one thing: your concept
of peripheral heterothermy, I believe, presupposes an improvement
in sensitivity to all the general factors in the environment at the
same or at a lower temperature. Does this also include the ability
to cool more and yet maintain sensitivity to environment?
156
HETEBOTHERMY IN HOMEOTHERMS
IRVING: Well, there certainly must be improved sensitivity;
that would be the conclusion from the fact that they appear better
able to monitor what is going on outside. That is, they are more
observant of minor temperature changes in exposed skin areas such
as the face and fingers. This is not a reduction in sensitivity or
simply hardiness. Rather, along with the suppression of pain or the
suppression of the impression of pain, there is apparently a more
refined observation of the local temperature condition of the skin.
As yet, we have not successfully demonstrated that sensitivity is
retained at a better level in the cold adapted skin than in the warm
adapted skin. So far we have only used these sensory tests with
people that were unadapted to cold. There are other tests that indi-
cate that the temperature sensitivity is retained better in the cold
skin after the people have been accustomed to exposure.
EAGAN: From the figures you have given on Eskimos, there is
a suggestion that their adaptation is an ability to maintain higher
peripheral temperatures, so that we cannot say that this is in any
way related to peripheral heterothermy as being an economical type
of adaptation.
IRVINGj Well, you have to qualify the statement and say which
Eskimos you are talking about. As Mr. Miller has shown, there is
a real difference between men and children, and yet they are all
normal components of the population. In addition, he also observed
that the skin of the Eskimo children did cool more rapidly and to a
lower temperature during the period of exposure than was true of
any of the adults.
EAGAN: Children do seem to withstand very low hand tempera-
tures even here in Fort Wainwright.
IRVING: I do not know whether it is true of all children or not.
We do not dare to ask parents to lend us their children for experi-
ment, but we have no compunction about asking the Eskimo children
to cooperate. They enjoy it.
EAGAN: Glasser's work with habituation or repeated presenta-
tion of an extreme cold stimulus shows that there is a change in
157
IFVING
the way that the central nervous system handles its appreciation
of this stimulus. Thus, after a series of exposures the organism
appears to gain confidence in itself. There is every evidence that
the discharge of cold receptors proceeds at the same rate, but the
change in the sensation of cold is localized in the sensory cortex;
that is, there is an habituation to cold. This can be suppressed by
anxiety. 1 would think that possibly the central habituation may often
be of much greater importance than peripheral heterothermy as
a mechanism of cold adaptation.
IRVING: I would like to know if anyone has ever demonstrated
that the discharge of the peripheral sensory endings is maintained
during cold exposure.
EAGAN: We only have indirect evidence of this. Dr. Hensel
has not done it, but 1 believe Glasserput on a demonstration before
the Physiological Society. He had a subject who was accustomed
to immersing one finger in ice water six times per day and who
no longer gave any evidence of a pressor response or of a cardiac
acceleration response to this measurement. However, when the
subject was brought up before the group at the physiological meet-
ing, he did show the pressor response and the tachycardia. He has
made other indirect observations on experiments in which they
have induced anxiety in the subject, causing him to show this phys-
iological correlate of pain sensation. Also, he had an argument
which involved the use of tranquilizer drugs, and from all of this
he thought that the simplest explanation was that the discharge of
the peripheral receptors is unchanged.
IRVING: Well, I cannot discount the operation of the central
part of thesystem in habituation, as distinct from peripheral adapta-
tion. I would say that adaptation likely involves change in the phys-
iological behavior of peripheral organs or tissue. I think there is
sure to be some alteration there; for example, the changes in some
of the nerves of the poikilotherms result in the blocking of their
conduction and excitability at a lower temperature after they have
become used to that temperature. That is the sort of thing I am
confidently looking for since we observed that the peripheral nerves
of cold adapted sea gulls conducted at lower temperatures than
when warm adapted.
158
HETEROTHEPMY IN HOME OT HEP MS
PROSSER: It might be that these other more complex inte-
grated functions are superimposed upon peripheral change. 1 do
not think one would expect a single line of defense here, but a
double line of defense.
IRVING: I do not see how the nervous system can possibly work,
anyway. What I mean is, how can it maintain the constancy of appre-
ciation for external conditions through a thermo- labile system
which changes so grossly in many of its velocity and frequency
functions? A gram remains a gram, and that is that. A millimeter
remains amillimeterand that is that.lf the universe changed dimen-
sions as it changed temperature, we would go nuts; we would not be
here.
EAGAN: There was an experiment we did in which four subjects
exposed one hand in a cold box for 12 hours per day for ten consecu-
tive davs, the finger temperatures being maintained between 10 C
and 15 G during the period of exposure. The latter was accom-
plished by having the subject withdraw his finger slightly as the
finger temperature increased or decreased towards 10 Cor insert
it farther into the cold box as it increased towards 15 C. The
subjects complained quite a bit at first, especially as it was getting
toward the 10 C side of things. As the days passed, their cold
tolerance was greatly increased and they would even go to sleep
o
with finger temperature at 10 C, a temperature which was too
painful in the beginning to even consider any sleep. Interestingly
enough, when theydid go to sleep, the finger temperatures invariably
rose; we had to awaken them so that they could shove their hands
into the cold box a little further. In general, I feel that this experi-
ment nicely demonstrates a decrease in the discomfort due to cold
as a result of continuous exposure.
IRVING: I think that is very important. Even though we say
"pain" is not physiologically definable as yet, it is nevertheless
a very important fact. Pain is pretty real, especially pain from cold.
A person unaccustomed to cold just cannot conceal it. I think the
mechanisms responsible for this habituation present a most inter-
esting question. As a result of habituation the re is repression of the
sense of pain, but we do not know whether there is any change in
159
IRVING
the rate, the velocity, the thresholds, or the temperature of cold
block for the actual nerve tissues in the periphery. There must be
some way to get at this question.
PROSSER: What would be the best animal to use? Hensel's
work has been done almost exclusively with cats.
IRVING: People are pretty good.
PROSSER: But you cannot go in and record the nerve impulses.
I want an animal in which you can go in and record the nerve
impulses.
IRVING: I would take a bird, like a gull, because for one thing
they are not pleasing animals; you have no sympathy for them at
all. By just putting blindfolds over their heads you can pretty well
immobilize them, and when so quieted you can readily expose
their long bare legs to cold.
EAGAN: I think a lot could be done by using Irving's and
Miller's ball-bearing test on fingers. When you use bilateral com-
parisons you can so simply compare the adapted side with the
controlled side.
PROSSER: Is this sensory adaptation which may be occurring
due to the temperature per se, or might it be due to changes in
oxygen supply?
IRVING: Temperature, per se, must beafactorin this habitua-
tion. However, since cold does reduce the circulation, then oxygen
supply is also a probable factor.
ADAMS: You can superimpose the effects of anxiety, induced
either by emotional stress or by pain on the cold induced vaso-
dilation response. In some subjects where we have measured cold
induced vasodilation responses, we find that we can prolong the
period of the peripheral vasoconstriction (with the finger surface
temperature at 0 G) up to 25 minutes in the ice bath by super-
imposing the effects of anxiety on the basic pattern of the response.
160
HETEFOTHEPMY IN HOMEOTHEBMS
o
In these studies we found fingertemperatures were about 33 C
when the subject was supine at a room temperature of about 20 C.
After stable measurements were attained at room temperature, the
finger was immersed into a stirred ice bath. At this point, of course,
a typical "Lewis response" occurs; that is, a rapid cooling to
approximately the temperature of the bath, followed by a period
of spontaneous rewarming to about 10 C to 12 G. I think that this
is an almost classical response and anyone can reproduce the
experiment using similar test conditions. This is the t3^e of res-
ponse that we find in all of the subjects in non- anxiety states. In
superimposing the effects of anxiety, however, we can change this
pattern to one where the cooling phase is prolonged to 25 minutes
after the initial immersion of the finger into the ice bath. This is to
be contrasted to the "unstressed" subject, where the spontaneous
vasodilation normally occurs in about 7 minutes. This, I think, would
probably indicate that there is a functional integrity of at least the
efferent nervous components in the peripheral portion of the finger
at these temperatures. Incidentally, the temperature that I am dis-
cussing is, of course, the temperature at the thermocouple taped to
the surface of the finger. It indicates very little, if anything, about
temperatures deeper in the finger where one may expect to find the
sensory endings and where you may also expect some peripheral
vascular changes to come about with mild degrees of adaptation or
cold acclimatization.
We became interested in this phenomenon as a possible test
site for induced variations in peripheral vascular responses with
local chronic cold exposure in the same individual. The condition-
ing phase in our series of experiments consisted of immersing the
same portion of the right index finger in a stirred ice bath for 20
minutes each timefor one month; different groups of subjects under-
went two, three, or four such exposures each day. In the group of
subjects that showed the greatest difference in response to the finger
immersion in stirred ice water, we found the finger temperatures
o 8
cooled to only 10 C in the bath, compared to 0 C in the control
experiments. The first thing that we saw was an earlier initiation
of the rewarming phase after about one week of cold conditioning.
We also carried out digital calorimetric measurements when the
finger was maximally vasodilated in the bath and found a statistically
161
IPVING
significant difference between the heat dissipation to our digital
calorimeter of the control and locally cold conditioned digits.
There is a possibility that this vasodilation, or relatively
reduced vasoconstriction, could be due to the destruction of the
components or functions in the finger that would allow for maxi-
mal vasoconstriction during immersion in the ice bath. That is,
the vasodilation we see developing in the locally cold conditioned
finger may be due to a destruction of vasoconstriction potential.
However, using anxiety again as a variable, we found that with our
subjects, all of whom were either medical or graduate students
and in whom it is very easy to induce anxiety, the induction of
anxiety by verbal suggestion at any point in the phase of vasodila-
tion brought the finger immediately to 0 C, with a cooling pattern
similar to the initial vasoconstriction seen in the control experi-
ments. I do not feel, therefore, that the cold conditioned fingers
have lost the ability to vasoconstrict maximally. The altered CIVD
patterns appear to result from an adjustment in peripheral circula-
tory control rather than a simple destruction of function.
EAGAN: I would like to point out that you have to be very care-
ful in using thermometry to deduce what is happening in the blood
vessels, but you cannot fool a calorimeter if you use exactly bal-
anced systems in testing the two fingers. In similar experiments
of recurrent finger cold exposure we have used plethysmography,
thermometry, and calorimetry concurrently, and we do not see
any of these GIVD differences you report.
ADAMS: I think such calorimeter data are quite acceptable
for showing an increase in digital blood flow. It is possible, how-
ever, that one could have a change in circulation or circulatory
mechanisms, perhaps in an increased blood flow deep in the finger,
that would not be reflected in surface temperatures.
EAGAN; How can you fool a plethysmography Calorimetry
will measure the average response over 30 minutes, if that is the
length of immersion. With thermometry you get something inter-
mediate in capability for detecting vascular change. It is slightly
more sensitive than calorimetry, but nevertheless, in vasocon-
stricted tissue, because of the thermal capacity of the tissue and
162
HETEBOTHEBMY IN HOMEOTHEPMS
because of its lowthermalconductivity,youwillhave a considerable
delay in detection of vasodilation. We have used the mercury strain
gauge, which you can place on the finger and which makes plethysmo-
graphic measurements by using either the olume pulse or the meas-
urement of blood flow but does not interfere with the exposure of the
finger to the environment. And here we have a very sensitive meas-
ure of the most subtle changes in mscular responses. Yet, despite
this we have failed to detect any evidence in favor of a local adapta-
tion to cold insofar as the CIVD response is concerned.
FOLK: I would like to ask Dr. Johansen to comment again on
his work with huskies. As I understand it they showed high body tem-
peratures after being on the trail. If you are talking about some
other animal we might find evidence of cross-acclimatization, but
if I understand it correctly, the husky does not show cold acclima-
tization. Is it possible that there might be heat acclimatization?
JOHANSEN: My studies on the exercising of huskies were
essentially not complete in the sense that I studied all the factors
tnvohed in thermobalance. I did not measure superficial tempera-
tures, for example. I did find, however, that training lowers to some
extent the great increase in temperature that is seen after intense
exercise. I do not know if this will hold up statistically, but I do
think that the effector systems for heat loss in the husky, the wolf,
the fox, and a number of other semi- large arctic mammals are not
effective enough to give a steady statethermalbalance at high levels
of exercise. There seems to be an inevitable accumulation of heat.*
MORRISON: What was the ambient temperature when you were
running those huskies?
JOHANSEN: From 30° C to 40° C below zero.
MORRISON: We ran some similar studies with huskies, and
in two sets of experiments of about an hour each we did not get any
♦Rapid or slow, this heat accumulation is probably related to the whole problem
of fatigue.
163
mviNG
such increase in bodytemperature. These measurements were made
during a normal regime with the team pulling a loaded sled and with '
three to five minute rest breaks every 15 minutes.
IRVING: These were trained?
JOHANSEN: Yes, eventually. They were not trained at the start
of the season, of course, but they were gradually trained during the
course of the winter.
EVONUK: What was your environmental temperature, Dr.
Morrison?
MORRISON: It was in February or March; the temperature was
near 0° C.
JOHANSEN: I have done similar studies on smaller, well- furred
arctic mammals, like the muskrat, and if 1 dispense with their
avenues for heat loss, for instance by occluding the tail as a heat
exchanger, then they show a very high body temperature. In other
words, heat loss through the feet and the nose and panting is not
enough to keep them at a normal body temperature.
ADAMS: There were also some data on beagles* showing that
voluntary exercise terminates at a particular level which seems to
be determined by the body temperature. The rate of body heating
is decreased with training. Untrained dogs will have a more rapid
rate of increase in body temperature when exercised on a tread-
mill, whereas trained dogs will show a slower rate and will reach
a particular rectal temperature in a much longer time.
JOHANSEN: I can tell you that just harnessing up a dog team
makes them quite excited; it is enough to increase their body tem-
perature more than one degree.
HANNON: Dr. Durrer and I have done a lot of work related to
this problem of insulation and metabolism of well- furred, well-
insulated dogs versus those that are not so well insulated. Thus,
* Young, D. R., et al. 19 59. J. Appl. Physiol. 14:839,
164
HETEFOTHERMY IN HOMEOTHEBMS
the daily caloric intake of huskies was measured throughout the
entire year. In addition, the daily caloric intake of beagles was
measured over a period extending from late winter to summer to
early winter again. Contrary to what you might suspect from reports
in the literature, there is a marked seasonal difference in caloric
intake in both groups of dogs— very high rate in winter and low rate
in summer. In the husky this occurred despite a large increase in
winter insulation. The difference between the amount of calories
they took in in summer and winter was in the neighborhood of 60%
in the husky and 70% in the beagle.
The data of Scho lander and Irving's group at Barrow* indicate
that a few arctic animals show no effect on metabolism through a
temperature range. We saw a similar thing in the caloric intake of
huskies during midwinter, when the environmental temperature
made a sudden drop from -7° C to -44 C. This temperature change
had no effect on caloric intake. We did not take a look at this type
of thing in the beagles, but the beagles between winter and summer
showed changes very similar to those seen in the huskies from the
standpoint of caloric intake— a little greater, but not appreciably
so. As a result ofthese observations on caloric intake, we are com-
ing to the conclusion that in these animals the basic response
appears to be metabolic and the insulative change probably serves
to increase their capacity to tolerate even lower environmental
temperatures.
In the husky it is interestingthat early in the winter, in Novem-
ber in particular, his caloric intake is somewhat above that seen
later in the winter. For example, it may go up to 70% above the
summer level and then drop back down to a plateau that is main-
tained for the remainder of the midwinter. This would suggest that
as he picks up his winter insulation he is able to compensate some-
what for the increased caloric demand of the environment. We did
not carry the beagles far enough into the winter to see if there was
a similar sort of reduction in caloric intake. However, no gross
changes in fur insulation were apparent.
*Scholander, P. F., et al. 1950. Biol. Bull. 99:259
165
IBVING
HART: You have an increase in food intake of 50% to 60%'^
HANNON: This is average daily intake on five huskies.
HART: I do not think that you can conclude that this necessarily
represents metabolic temperature regulation. How well did you con-
trol activity, sledding and various things?
HANNON: These dogs were tied with six-foot chains. They were
only released from these chains a few times, in both summer and
winter, to be brought into the laboratory for blood sugar determina-
tions. Furthermore, in the winter the body weight declined, and
in the summer it increased, thus suggesting an inability to precisely
match the caloric intake to the energy demands of the environment.
In other words, in the summer they were eating too much and in the
winter too little to maintain a constant body weight from season to
season.
HART: Is not 60% a large increase in food intake for a well-
insulated animal?
HANNON: It wouM seem so, yes.
MORRISON: Are they rather limited in their activity in the
summer?
HANNON; Grossly, the animals appeared to be most active in the
summer and the least active during periods of extreme winter cokl.
Whether this produced a significant seasonal difference is unknown.
It is my guess, however, that they may be more active in summer,
because there are more people around them.
o
DURRER: It is interesting to note that in temperatures of -35 C
or -40 C the activity is quite reduced. For example, they are even
reluctant to get up and eat and are not as apt to rise in the presence
of people at these extreme winter temperatures as they are in sum-
mer or in the warmer winter temperatures.
JOHANSEN: One factor that has not been mentioned is the
166
HETEROTHERMY IN HOMEOTHEPMS
availability of food to the animal. It is extraordinary when an animal
has more food than he can eat everyday. This is certainly not what
you would expect arctic mammals to be confronted with in his natural
environment.
HANNON: That is true, but if we had attempted to control caloric
intake we would have biased our results by the mere fact that you are
controlling the amount of food available.
IRVING: He is thinking that the dog chooses to eat more when
excess food is available. Why he chooses to eat is a different thing.
MORRISON: I might add that our appetite in cold weather
exceeds the thermoregulatory needs of the body.
HANNON: After the first two or three weeks of over-eatinr:
they reduced their intake and it remained fairly constant from day
to day. However, when you consider these daily intakes over a
period of months the differences between the seasons are signifi-
cant, and there is a significant correlation between temperature
and food consumption.
HART: Have you done this over the whole winter and summer?
HANNON: On the huskies, we have it starting with November
of one year and continuing through November of the following year.
MORRISON: How about the beagles?
HANNON: The reason we used beagles is interesting in itself.
We started these feeding experiments on huskies on the first of
October and commenced our measurements of food intake on
the first of November. As I mentioned earlier, there was a decline
in food intake between November and the later portions of the
winter. This did not seem quite right; so in midwinter we decided
we had better look at dogs that were not so we 11- insulated as the
huskies. Beagles seemed to offer a good choice. They were pur-
chased in California and brought to Alaska, where they were housed
indoors for four weeks. During this period they were allowed two
weeks to adapt to the same diet as the huskies and two weeks
167
IFVING
during which control measurements were made in the laboratory.
They were then subjected to outdoor exposure. When we first put
them out in the cold the temperature was about 0 F. At first they
could not tolerate this cold on their feet and would howl, roll on
their backs and put their feet in the air. During subsequent expos-
ures of gradually increasing duration they evidenced cold injury,
particularly on the feet, ears and mouth. However, within a period
of two or three weeks these injuries began to disappear and they
were eventually able to tolerate temperatures as low as -30 C for
a full 24 hours with no apparent ill-effects. Such continuous expos-
ure was continued through the remainder of the winter, the summer
and into the early months of the following winter, when the experi-
ment was terminated.
MORRISON: Were they eating meat or dog chow?
HANNON: The diet was fairly high in protein; it was a mixture
of dry dog food, powdered milk, and fish meal.
WEST: Did you find any difference in efficiency?
HANNON: Do you mean work efficiency?
WEST: No, efficiency of food assimilation; that is, the utiliza-
tion of the energy that you gave them. Did you get the caloric value
of feces, for example, to see if they were using all this food that
you were feeding them?
HANNON: No, we did not.
KLEIBER: I may have an answer to that, not for dogs but for
baby chicks. There we found a very consistent correlation between
food intake and temperature; namely, as we decreased the tem-
perature from 100 F to 95 F to 80° F to 70° F, there was a
consistent increase in food intake. There was also a decrease in
digestability.
WEST: We found the same decline inefficiency with wiki birds.
I wonder if this is a part of the explanation for this increase in food
intake.
168
HETEPOTHEBMY IN HOMEOTHEPMS
KLEIBER: We measured that and found that there is a definite
increase in caloric output.
HANNON: Well, the magnitude of the change in the beagles, at
least, between this summer and winter is very similar to what
o
you see in rats going into a 5 C cold room, thus suggestmg a
similar caloric demand by the environment. In the cold, rats cer-
tainly exhibit a high rate of heat production, but as far as I know
the efficiency of food utilization has never been measured.
IRVING: To get back to the remarkably high body temperature
that Dr. Johansen spoke about, I would like to inquire whether there
are reports of domesticated animals having reached similar high
temperatures?
KLEIBER: Yes, Kibler and Brody* recorded rectal tempera-
o o
tures in Holstein cows as high as 108 F (42 C). Generally cows
are in bad shape in a hot environment.
FOLK: I might make another comment on continuous feeding of
dogs, since apparently not too many people have heard about it, but
some of the big kennels have been doing that for several genera-
tions. Sometimes, in experiments like those you do with white rats,
you want to have continuous food there. You do not want a perturba-
tion. If they have had food in front of them when they are quite
young they do not overeat. Occasionally there is one dog you will
need to eliminate because it does overeat, but they are rather quick
to learn to take just enough out of a feeder.
HANNON; Our dogs in the study were two to four years old.
Thus, they were adults. Food was placed in front of them and left
for a period of one-half hour. But, as I mentioned earlier, they
would eat a little bit too much in the summer time and too little
in the winter time insofar as the maintenance of a constant body
weight was concerned.
MORRISON: I wonder if the specific dynamic action of the food
* Kibler, H. H. and S. Brody. 1953. Influence of humidity on heat exchange and
body temperature regulation in Jersey, Holstein, Brahman and Brown Swiss cattle.
Univ. of Missouri Res. Bull. 522-.14.
169
IBVING
would produce enough heat to make them uncomfortable in the sum-
mer and if this could modify their intake. Such an effect should not
bother them in winter.
HANNON: We do not know, except that in the winter they have
heavy insulation. In the summer they do not.
MORRISON: They can lie in the snow and dissipate more heat.
HANNON: I believe Dr. Irving has made some measurements
on the amount of heat that huskies dissipate to the snow when they
are lying down"?
MORRISON: Well, how much they can dissipate and how much
they do dissipate depends on whether they are in a heat dissipation
"posture" or not.
HANNON: If dogs are lying in the snow dissipating very much
heat, a melting of the snow should be evident. This does not seem
to occur.
IRVING: There is no melting. John Krog and I measured the
temperature under dogs by putting a grid of thermocouples under
the place where they slept. We found that the temperature at the
surface was not above freezing, and the snow did not melt although
it did become compressed. If the snow had melted, the fur would
have froze to the snow, and you never see any fur frozen in a place
where a normal animal has been bedded down in the snow.
JOHANSEN: If I may switch back to the high temperatures now,
I think that we really need a lot more measurements. The only
really detailed study available is Asmussen and Nielsen's study
of athletes, which showed a rectal temperature of 41 C after long
track running. It may be surprising to you, but it is not to me, that
the husky, with its tremendous insulation, gets such a great in-
crease in temperature.
IRVING: Have you obtained any evidence that he really develops
a better faculty for supporting a high body temperature?
170
HETEBOTHEBMY IN HOMEOTHEBMS
JOHANSEN: No.
IRVING: I think this would be a very valuable thing to deter-
mine, especially when sled-dog running is so well cultivated here;
you might even use such information to get good teams of dogs.
JOHANSEN: Of course I would like to measure running caribou
and, when I get back to Norway, the reindeer, which is domesticated
and used for transportation.
HART : I would like to mention this in connection that even in
the small mammals such as mice and rats body temperatures up
to 40° G or 41° G may be obtained during exercise of 20 or 30
minutes duration. It is commonly possible to do this in a rela-
tively warm environmentaltemperature. However, in a cool environ-
ment, the body temperature may not rise at all.
JOHANSEN: Their insulation of course is poor.
HART: The insulation is markedly inferior. With the husky
dog, you apparently never reach the condition where the tempera-
ture is low enough to cause this effect.
HANNON; Along similar lines it mightbe worth mentioning that
the rectal temperatures of cold acclimatized rats are quite readily
elevated to very high levels when they are injected or infused intra-
venously with norepinephrine. A number of times, for example, we
have observed body tem.peratures as high as 43 C or 44 G in
experiments with this hormone.
JOHANSEN: Of course this concept of heterothermy and the
potential of insulation somewhat invalidates the things we have
been taught in school about the climatic rules. I was wondering
whether Dr. Irving would care to comment about how this might
invalidate Allen's Rule about the length of extremities.
IRVING: I think those rules are useless.
PROSSER: There is still a correlation, just the same.
171
mviNG
IRVING: I am not sure there is among the different caribou;
the smallest of all is also the most northern. You find many excep-
tions to that; and as Scholander says, if this were a matter of a
law of heat you should not find any exceptions. Thus, one exception
would invalidate the significance of such a law. It may be true that
many birds as they go north get longer tails, larger bodies, or
bigger claws. On the other hand, some do just the opposite. I do
not think it has ever been shown that any of these differences in
body dimensions are significant to the heat economy of the animal.
I will go farther and say that the surface of an animal has no rela-
tion to its heat exposure; there is no relation that you or I can
define, because in the first place there is no geometrician who can
define the surface of such an irregular object as an animal. It is
indescribable, mathematically. If it were describable, it would not
be worth the time or the effort, and further, attributing the heat
loss simply to the surface disregards practically all that we know
that is interesting and important with regard to the conservation
and dissipation of heat. In other words, it is not a matter strictly
of surfaces. For example, the circulation through the skin of the
fingers is one hundred times what it is through the skin on the
forearm or on the rest of the body. The variability in the amount
of circulation, the amount of heat exchange, and the temperature
of blood passing through the extremities are far more important
factors than is the extent of the skin surface. And those are the
variable factors in heat economy, while surface, if there be such
a thing, is an invariable function unless the animal chooses to
alter his posture, as he does in sleep.
PROSSER: But still there is a general correlation between
size and distribution; it may have no relation to temperature regula-
tion at all, but it remains as a correlation.
IRVING: That may be, but it is not of any great interest or
importance to physiology.
PROSSER: I am not willingtosaythat.lt may have some mean-
ing which we do not know.
MORRISON: Do you think it is fair to say that a factor has no
significance simply because there are other factors which are
more significant?
172
HETEROTHEFMY IN HOMEOTHEPMS
IRVING: Yes, it has less significance, because it conceals
or disregards the physiologically important and interesting things,
which are the variability in temperature and circulation of the
different areas.
MORRISON: Well, would you then say that the high levels of
hemoglobin in a diving animal are of no significance in the prolonga-
tion of diving, because they would not allow anything like the
observed increases in diving time and because the circulatory
changes are so much more important?Is there not an analogy here?
IRVING: No, I would not say that the oxygen capacity of the
blood is unimportant for the seals. It is very important. It is not
the large factor in the prolongation of their dives, but presumably
if the blood has twice the oxygen capacity it has at least doubled
the transport capacity and the rate of recovery. If you get double
the oxygen capacity and improve the elasticity of the whole vascu-
lar system, then recovery is apparently attributed to those factors.
One of the remarkable things about such diving animals, incidentally,
is not only the prolonged divingbut also the rapidity with which they
can recover and take another dive.
MORRISON: But when we have a factor that is advantageous,
when are we to say that it no longer has any significance as long
as it is in the right direction? Can we not say that it may have
selective significance, even if it is only at the 10% or 5% level?
IRVING: Then you get one of these instances of statistical
significance. You are talking about imperceptible adaptations
which gradually accumulate by some statistical process to become
of visible importance.
JOHANSEN: If you go back to heterothermy, the point here is
that these extremities provide insulation, and if they are larger
they provide more insulation.
MORRISON: If you do not have extremities, insulation (=l/
conductance) is better.
173
IRVING
JOHANSEN: No, such a situation is unrealistic and has no
relevance to the situation.
MORRISON: If you amputate the leg, you are going to lose less
heat from it.
PROSSER: Also, there might be differences which would show
up in a population analysis that would not be of any measurable
advantage to an individual as such. However, they might be of impor-
tance to the whole population.
174
MAXIMAL STEADY STATE METABOLISM AND ORGAN
THERMOGENESIS IN MAMMALS
L. Jansky
The studies of basal metabolic rates in mammals and the rela-
tion of metabolic rates to body weight have been the subject of many
papers and reviewssince the middle of the nineteenth century. These
studies have not confirmed the validity of the "surface area theory"
and have proved that the basal metabolic rates were proportional to
W^*^^ where W is the body weight (Kleiber, 1947).
On the other hand, very few data are available on the upper
limits of metabolic rate that can be sustained for long periods in
different species. It is known that very high rates of heat produc-
tion, up to 100 times the basal level, can be measured in man and
horse under extreme exercise (Brody, 1945). However, these rates
cannot be sustained for long periods and do not result from steady
state effort. Methods of estimating steady state effort and a com-
parison of results in different species varying in body weight will be
considered in this paper. In addition, the total cytochrome oxidase
activity, which can yield values for metabolism which are theoreti-
cally maximal in different species (Jansky, 1961), will also be con-
sidered. This method also provides a means for estimating the theo-
retical maximal values for different organs of the same species and
their relative contributions to the metabolic capacity of the whole
animal.
Maximal Steady State Metabolism
For the purposes of this paper, the upper limit of metabolism
will be called the "maximum steady state metabolism" and will be
defined as the highest oxygen consumption compatible with sustained
aerobic effort when there is no progressive accumulation of lactic
acid in muscles. It is known for man (Wells et al., 1957) rats (Sreter
and Friedman, 1958), and deer mice (Hart and Heroux, 1954) that a
certain level of exercise can be attained without accumulation of
175
JANSKY
lactic acid and that this level of exertion can be sustained for long
periods. In practice, lactic acid is not usually measured, and maxi-
mal steady state metabolism during exercise is determined at the
highest running speed, which can be sustained for about 20-40 min-
utes.
During exposure to cold there is also a marked increase in me-
tabolism which can be maintained for long periods. The question
therefore arises as to whether there is a relationship between the
maximal working metabolism and the highest level of metabolism
that can be obtained in the cold.
Experiments on man have shown that it is possible to attain the
maximal steady state metabolic level only under intensive work con-
ditions and that the effect of coki does not add to the metabolic rate
during work (substitution theory- Lefevre, 1933, 1934). On the other
hand, tests on some small mammals have shown that maximal ox-
ygen consumption is possible with simultaneous application of work
and lowered temperatures, so that the working and cold thermogene-
sis occur at the same time, (addition theory- Chevillard, 1935; Hart,
1950; Hart and Heroux, 1955; Jansky, 1959, a, b, c).
In the tests on small mammals, the measurement of maximal
steady state metabolism during work and exposure to cold is very
difficult, owing to the rapid development of hypothermia which event-
ually causes a decline in heat production. Figure 1 shows a distinct
drop in the oxygen consumption ofwhite mice which started immedi-
ately at the beginning of the work in extreme cold (Jansky, 1959a).
Decline of metabolism presumably due to hypothermia was found at
the lowest temperatures in most of the species investigated.
Since the values obtained on hypothermic animals could not be
considered maximal, it was necessary, therefore, to perform the
tests atvarious temperatures to find the lowest temperature at which
working oxygen consumption was maximal and did notdecrease dur-
ing the test period (40 minutes) .
Results obtained on various small mammals showed that there
were species differences in the effect of work and cold on metabol-
ism. In rabbits and lemmings (Hart and Heroux, 19 55) in white mice
176
OBGAN THERMOGENESIS
^C23g
Figure 1. The time course of working oxygen consumption of the mouse at
DU3 tern
sa; time in minutes. ( Jans ky, 1959a).
various temperatures. Ordinate: oxygen consumption in mlO /hour/animal; Abscis
177
JANSKY
(Hart, 1950; Jansky, 1959 a), and in golden hamsters (Jansky, 19 59c),
kept at laboratory constant temperatures, the working oxygen con-
sumption increased with decreasing temperature. Oxygen consump-
tion during work was added directly to the cold thermogenesis, giving
two parallel curves (Figure 2). These results confirmed the validity
of the addition theory and showed clearly that the highest values of
metabolism could be measured only after simultaneous application
of cold and work.
Contrasting results have been obtained on two wild rodents , the
common vole (Microtus arvalis) and the bank vole (Clethrionomys
glareolus) (Jansky, 1959b), kept for a short period at naturally fluc-
tuating temperatures. Both species are closely related and have the
same average weight (18 gm). In the common vole, the typical addi-
tion relationship between working and resting heat production in the
cold was observed. In the bankvole,onthe other hand, the metabol-
ism during maximal work below the thermoneutral zone did not in-
crease to the same extent as that during rest with decrease in tem-
perature. Therefore the heat production during work partially sub-
stituted for the cold thermogenesis. This was particularly clear when
the maximalrunningspeedsof the two species of voles are consider-
ed (Figure 3). Although there was a slight increase in running speed
with lowering of temperature from 25 C to 5 C, in both species,
there was a decrease in the difference between working and resting
metabolism in the bank vole but not in the common vole (Figure 2).
When the lowest temperature was reached, both the running speed
and the difference between working and resting metabolism were
greatly reduced. The common vole had a greater range for maximal
work than did the bank vole in both heat and cold.
These experiments have shown that the metabolic differences
among various species of mammals do not depend on the weight of
the animals or on their phylogeny. The only obvious difference be-
tween the common vole and the bank vole lies in the ecology of both
species and in their acclimatization to various temperatures. Bank
voles live in forests in deep burrows and build well- insulated nests
and are not, therefore, exposed directly to the effect of low tem-
peratures. Common voles, on the other hand, live in meadows in
superficial burrows almost without nesting material and are forced
more often to endure extreme temperatures. This is reflected in
178
OPGAN THEBMOGENESIS
10-
5-^.
GOLDEN HAMSTER -80 GMS.
^^^^
I.I. I I L
WHITE MOUSE
24 GMS.
_l I L.
J I L
15-
10
5-
COMMON VOLE -18 GMS.
BANK VOLE - 18 GMS.
\^ -.. *'
:/M— k
♦^*-
\.
K,
J , \ 1 \ I L_
I . I ^ I I L
0 10 20 30 0 10 20 30
TEMPERATURE "C.
Figure 2. Working and resting oxygen consumption at different temperatures
in various mammals.
179
JANSKY
10
■
1
i\
#1 \
^'^.
T
/I \
/•
•"v.
^
V
^
^^^
/l "
5
>
i
r|
^ 1
1
» 1
1
» r
20
40
Figure 3. Maximal running speed of the common vole (x x) and the bank
vole (▲--▲) at various temperatiu-es. Ordinate: running speed in m/min.; Abscissa;
temperature in C. (Jansky, 1959b).
180
ORGAN THERMOGENESIS
their greater abilities to run at high and especially at low tempera-
tures.
Recently ithas been shown (Hart, 1962, in press) that warm- and
cold- acclimated rats behave differently with respect to substitution
of exercise for cold thermogenesis. Warm- acclimated rats, having
shivering thermogenesis only, substituted heat production from shi-
vering by heat production from exercise. Oxygen consumption during
work did not change with decreasing temperature and was identical
to the maximal oxygen consumption in rest at the lowest tempera-
tures. This is apparently due to the fact that exercise in cold may
reduce or eliminate shivering. This was surmised long ago and re-
cently demonstrated in pigeons durirjg flight (Hart, 1960). On the
other hand, in cold- acclimated animals, which can produce heat with-
out shivering (Sellers et al., 1954; Heroux et al., 1956; Cottle and
Carlson, 1956), the addition of exercise heat production to cold ther-
mogenesis is made possible (Figiore 4). The result is that working
oxygen consumption increase with decreasing temperature parallel
to resting values and the maximum heat production is greatly in-
creased.
However, at temperatures approaching the peak metabolic rate
for cold- acclimated rats, heat production during work did not in-
crease with loweringoftemperature. At these low temperatures, shi-
vering was clearly visible in the resting rats, and mechanical work
was substituted for shivering as in warm- acclimated rats (Hart, Jan-
sky, unpublished). The values followed closely the broken line shown
in Figure4. As shown for warm- acclimated animals, the resting me-
tabolism was, at very low temperatures, almost as great as the
values of working metabolism.
It seems clear, therefore, that the substitution relationship be-
tween working and resting heat production exists in these animals
only when shivering is replacedby gross physical activity. The addi-
tional relationship occurs over a certain range of temperatures in
these animals, when non-shivering thermogenesis plays thedomin-
ant role in maintaining body temperature.
All these data show that the values of maximal metabolism are
obtainable not only after simultaneous application of work and cold,
181
JANSKY
METABOLISM
-40 -30 -20 -10 0 10 20 30 40
AMBIENT TEMPERATURE, "C.
Figure 4. Working and resting oxygen consumption at various temperatures
in cold and warm adapted rats. (Hart 1962, in press)^
182
ORGAN THERMOGENESIS
but also in the resting state after exposure to low temperatures ap-
proaching the lethal level. Under the latter condition it is necessary
to measure the oxygenconsumptionfor a very short period after ex-
posure to cold, because of the substantial drop in body temperature
(Figure 4) . This period is about 20 minutes long for the rat (Depocas
et al., 1957).
Owing to the difficulties described above in measuring maximal
steady state metabolism, relatively few values have been published
for mammals (Ghevillard, 1935; Hart, 1950; Jansky, 1959a for the
white mouse; Hart and Heroux, 1955 for the lemming and rabbit;
Jansky, 1959b for the bank and common voles; Jansky 1959c for the
golden hamster; and most recently by Buskirk and Taylor, 1957, for
man). One can expect that rather larger species differences might
occur, owing to differences in body size, posture, hair insulation,
blood circulation, and air movement, which might be quite different
during maximal metabolism than during the resting state and could
have a different effect on the amount of heat dissipation.
When all published values of maximal steady state metabolism
are plotted against the log body weight of the animals (Figure 5) , it
was found that maximal steady state metabolism is equal to about
six times and basal rate, with a body weight exponent very close to
that found for basal metabolism. All the species examined have,
therefore, nearly the same capacity to increase energy metabolism
from the basal to the maximal steady state level. Species differences
in posture, insulation, and other factors that affect heat dissipation
have no apparent effect on this capacity to increase heat production.
Total Cytochrome- oxidase Activity
Since the rapid cooling of small animals at low temperatures
makes the measurement of maximal steady state metabolism quite
difficult, an additional method was sought for measuring the highest
metabolic capability of animals and tissues.
It can be assumed that the total oxidative activity of tissues can-
not be greater than that of the activity of the only terminal oxidative
enzyme, cytochrome oxidase. In other words, it is supposed that the
183
JANSKY
100,000
10,000
1000
- = MAXIMAL WORKING METABOLISM
• = TOTAL CYT-OX ACTIVITY
100
/ BMR.
MAX MET
100 1000 10,000
BODY WEIGHT , GMS.
100,000
Figure 5. Relationship of maximal steady state metabolism and total cyto-
chrome oxidase activity to body weight in various mammals.
184
ORGAN THERMOGENESIS
maximal oxidative activity of this enzyme corresponds to the highest
tissue oxygen consumption. It can also be assumed that cytochrome
oxidase does not occur in excess quantity in tissues, because cyto-
chrome oxidase activity readily becomes adapted to various condi-
tions (Tipton and Nixon, 1946; Hannon, 1960). For these reasons the
cytochrome oxidase activities of whole animals and their tissues
were examined to find whether the values were related to the maxi-
mal steady state oxygen consumption.
The method selected for use in these studies was the classic
manometric method of Schneider and Potter (1943), in which cyto-
chrome oxidase activity can be measured in terms of oxygen con-
sumption. The cytochrome oxidase activity was measured in a homo-
genate of the whole animal for direct comparison with the values of
maximal steady state metabolism. Before homogenation in distilled
water, the animals were depilated and after removal of their diges-
tive tract, they were ground in ameatgrinder. Oxygen consumption
of the homogenate was measured at 37 C .
The total cytochrome oxidase activity was determined in seven
species of rodents (wood mouse - Apodemus sylvaticus, bank vole -
Glethrionomys glareolus, common vole - Microtus arvalis, white
mouse, golden hamster, rat, guinea pig) in the range of body weight
from 17 to 700 gms. It was found (Figure 5) that the exponent of the
relationship between total cytochrome oxidase activity and body
weight was very similar to that found for basal and maximal meta-
bolism (Jansky, 1961).
By comparisonof the absolute values of oxygen consumption, ob-
tained in vitro, using cytochrome oxidase activity and those in vivo at
the level of maximal steady state metabolism, only small differences
were found.
In spite of close agreement between in vivo and in vitro values,
they are not considered to be identical. Both methods are completely
different, and we cannot expecttobeable to imitate the same condi-
tions in vitro as in living cells, where the concentration and com-
position of substrates, pH and various other factors can change dur-
ing the maximal performance of the organism. In addition there is
a possibility that certain organs such as kidney, brain, or gonads are
185
JANSKY
not performing at maximal capacity when the animal is engaged in
maximal steady state effort. This may explain the tendency for cyto-
chrome oxidase values to be higher than maximal working metabol-
ism in the various species.
It is, therefore, suggested that the terms "maximal steady state
metabolism," be used for values obtained in vivo and "total cyto-
chrome oxidase activity" be used for values obtained in vitro, which
represents the highest theoretical value of oxidative metabolism
(metabolic capacity).
Cytochrome Oxidase Activity in Body Organs
The values of total cytochrome oxidase activity are useful for
comparative purposes and seem to be especially suitable for esti-
mating the metabolic capacity of different body organs. At present,
we do not know of any other method for assessing maximal perform-
ance of body organs. The cytochrome oxidase method can provide
some information on the relative roles of different organs in the total
metabolic capacity of the whole animal.
The cytochrome oxidase activity was measured in 10 of the most
important organs (carcass, liver, skin, kidney, brain, lung, heart,
diaphragm, spleen, and gonads) in the golden hamster (Svoboda and
Jansky, 1959). Some other preliminary experiments were made on
the white mouse and on the rat.
In general, the highest cytochrome oxidase activity per mg of
dry substance was found in the heart, kidney and brain, the lowest in
the carcass and in the skin. The cytochrome oxidase activity per mg
dry substance in the same organs of various species seems to de-
crease in heavier animals.
The most important consideration for our purposes is the ratio
of cytochrome oxidase activity in whole organs to the total cyto-
chrome oxidase activity ofthe whole animal. The results on the gold-
en hamster show veryclearly that the muscles play the most impor-
tant role. At body temperature (37 G), they rep resent about 76% of
186
ORGAN THEPMOGENESIS
the theoretical total metabolic capacity (Figure 6). The role of other
organs is relatively small. The most important are skin (9%), liver
(5%), brain (3%), and gonads (3%). Similar observations were also
made on the rat.
Organ Thermogenesis in vivo
Owing to the large contribution of the muscles and the minor
contribution of visceral organs in the total cytochrome oxidase ac-
tivity of hamsters and rats, it is important to consider the relative
contribution of these organs in vivo to the maximal steady state me-
tabolism. At present only indirect estimation can be made on the
role of muscle in intact animals. In warm acclimated rats (Figure
4) the maximal steady state metabolism is approximately 270 Cal/
(hour x body weight ' ). The increase of metabolism from the basal
level (100 CaL/(hour x body weight * )) is about 170 Gal/(hour x
body weight * ), which is 63% of maximal metabolism (270 Cal/
hour) . Since shivering is the principal source of heat in these rats
exposed to cold, it can be assumed that the cold thermogenesis is
due to muscles. In addition to the cold thermogenesis, it has to be
estimated that the participation of muscles in the basal state a-
mounts to about 30% of the total metabolic rate (Field et al., 1939).
This would be approximately 10%of the maximal rate in these tests.
The total contribution of the muscles to the maximal metabolism
would therefore be 73% (63% + 10%).
In cold acclimated rats the quantitative estimation of the role of
the muscles is more complicated. In addition to shivering, the non-
shivering thermogenesis is developed (Sellers et al., 1954; Heroux
et al., 19 56; Cottle and Carlson, 19 56), which increases the maximal
metabolic rate to about 420 Cal/(hour x body weight) (Figure 4) . In
order to estimatethecontributionof muscles under these conditions,
the site of non-shivering tnermogenesis must first be ascertained.
The visceral organs have been considered as important sites of
non-shivering heat production for many years. Much of the evidence
has come from measurements of temperatures near the liver (Gray-
son andMendell956;Donhofferetal.,1957).ln cold acclimated rats,
the elevation of BMR and the elevation QO in vitro give support to
187
JANSKY
100%^
<
a.
<
o
o
_i
o
CD
<
I-
o
CD
O
cr
UJ
<
•4
SPLEEN
-0.1 %
LUNG
-0.6%
HEART
-0.8 7o
DIAPHRAGM
-1.3 %
KIDNEYS
- 1.6 7o
BRAIN
-3.0 %
GONADS
-3.1 7o
LIVER
SKIN
-4.7 7o
-9.1 7o
MUSCLES + BONE -75.67o
Figure 6. Contribution of various organs to the total metabolic capacity in the
golden hamster as measured by cytochrome oxidase activity.
188
ORGAN THERMOGENESIS
the increased thermogenesis of visceral organs (Weiss, 1954). How-
ever, direct evidence on the magnitude of the contribution is lacking.
On the other hand, evidence against the visceral organs as the
important site of heat production in non- shivering was provided by
Depocas (1958) who found, that the metabolic response to cold in
curarized cold acclimated rats was not reduced by functional evis-
ceration. Supporting evidence that the liver did not greatly contri-
bute to increased heat production in cold was provided by Kawahata
and Carlson (1959) in cold acclimated rats. Similar observations
have recently been obtained for the kidney ( Jansky and Hart, unpub-
lished). On the other hand, direct evidence for the participation of
muscle in cold thermogenesis was obtained by Jansky and Hart (un-
published) in the leg muscles of cold acclimated curarized rats
where elevation in oxygen consumption equal to that in the whole ani-
mal were found during exposure to cold.
While thermogenesis from visceral organs still cannot be ex-
cluded, it can be concluded that both shivering and non- shivering
thermogenesis are dependent to an important extent on the muscles.
The total increase in heat production of cold-apclimated rats from
the basal level (125 CaL/(hour x body weight ' )) is about 295 Gal
/(hour X body weight * ), which is 75% of the maximal rate (420
Gal/hour). If muscleaccountsfor the entire cold thermogenesis, this
would be equivalent to 77%of maximal metabolism, when the contri-
bution of muscle to the basal metabolism is also considered.
The calculations again agree closely with the large proportion
of muscle to the total cytochrome oxidase activity in hamsters and
rats and show that as an upper limit, muscle could contribute about
the same proportion to metabolism in both warm and cold acclimated
rats. However, it is clear that the absolute increase in maximal me-
tabolism of cold acclimated rats would require an increase in ab-
solute valuesof cytochrome oxidase activity in the organs concerned.
These observations, which are incomplete and permit only tentative
conclusions, will be extended by work now in progress on the cyto-
chrome oxidase activity of the muscles and other organs in warm
and cold acclimated rats.
189
JANSKY
SUMMARY
The measurement of maximal steady state metabolism is com-
plicated by the fact that both cold exposure and exercise may be re-
quired to elicit the maximal response and by the fact that the effect
of exercise and cold varies with environmental temperature, state
of acclimation, and other factors. In most small mammals studied,
the metabolic effect of exercise is added directly to the cold ther-
mogenesis, but in the bank vole and in warm acclimated rats, ex-
ercise substitutes for shivering and replaces cold thermogenesis.
In cold acclimated rats, the metabolic effect of exercise is added to
cold thermogenesis, except at the lowest test temperatures where
substitution is again observed. The varied responses of different
species and of cold- and warm- acclimated rats apparently depend
on the extent of participation of non- shivering thermogenesis, which
extends the range for activity and increases the maximal steady
state metabolism. Maximal steady state metabolism can be deter-
mined either by imposing exercise simultaneously with cold or by
exposing the subject to cold alone at very low temperatures.
The maximal steady state metabolism of different species was
equal to about six times the basal metabolism, and the exponent re-
lating log metabolism to log body weight was not obviously different
from that for basal metabolism (W * ) for the species tested. Basal
and maximal metabolism, therefore, give two parallel curves.
The total cytochrome oxidase activity was also measured in
homogenates of whole animals. It was found that the exponent of the
relationship between cytochrome oxidase activity and log of the
weight was very similar to that found for basal and maximal meta-
bolism. There was a close similarity between absolute values of
maximal metabolism, and the total cytochrome oxidase activity
provides a theoretical upper limit to the metabolic capability and is
useful for comparative purposes in various species and organs of
the same species.
The study of body organ cytochrome oxidase activity in the gold-
en hamster illustrates the importance of the muscles, which com-
prise about three fourths of the total cytochrome oxidase activity.
190
ORGAN THEBMOGENESIS
This fact agrees with observations on the site of thermogenesis in
living animals, where either shivering alone or shivering and non-
shivering thermogenesis together are responsible for maintaining
body temperature in cold environments.
♦Contribution from the Division of Applied Biology, National Research Council,
Ottawa, Canada, and Department of Comparative Physiology, Natural Science
faculty, Charles University, Prague, Czechoslovakia. Issued as N.R.C. No. 6679.
Postdoctoral Fellow, National Research Council, 1960-61.
191
JANSKY
LITERATURE CITED
1. Brody, S. 1945. Bioenergetics and growth. Reinhold Publishing
Corp. New York. p.915.
2. Buskirk, E. and H. L. Taylor. 1957. Maximal oxygen intake and
its relation to body composition with special reference to
chronic physical activity and obesity. J. Appl. Physiol. 11;
72-78.
3. Chevillard, L. 1935. Contributions a 1 'etude des echangesrespir-
atorires de la souris blanche adulte. II. Thermogenese et
Thermogenese et thermolysede la souris. Ann. physiol.phys-
icochim. biol. 11:485-532.
4. Cottle, W. H. and L . D. Carlson. 19 56 . Regulation of heat produc-
tion in cold adapted rats. Proc.Soc. Exp. Biol. Med., 92:845-
849.
5. Depocas, F., J.S.Hart, and O.Heroiix. 1957. Energy metabolism
of the white rat after acclimation to warm and cold environ-
ments. J. Appl. Physiol. 10:393-397.
6. Depocas, F. 1958. Chemical thermogenesis in the fiinctionally
eviscerated cold- acclimated rats. Can. J. Biochem. Physiol.
36:691-699.
7. Donhoffer, Sz., Gy. Szevgari, I. Varga-Nagy, and I. Jarai. 1957.
Uber die Lokalisation der erhbhten Warmeproduktionbeider
chemischen Warmeregulation. Pflugers Arch. 265:104-111.
8. Field, J., H. S. Belding, and A. W. Martin. 1939. An analysis of
the relation between basal metabolism and summated tissue
respiration in the rat. I. The post- pubertal albino rat. J. Cell,
and Comp. Physiol., 14:143-157.
9. Grayson, J. and D. Mendel. 1956. The distribution and regulation
of temperature in the rat. J. Physiol. 133:334-346.
192
ORGAN THEEMOGENESIS
10. Hannon, J. P. 1960. Effect of prolonged cold exposure on com-
ponents of the electron transport system. Am. J. Physiol. 198:
740-744.
11. Hart, J. S. 19 50. Interrelations of daily metabolic cycle, activity,
and environmental temperature of mice.Gan. J. Research, D,
28:297-307.
12. Hart, J. S. and O. Heroux. 1954. Effectof low temperature and
work on blood lactic acid in deer mice. Am. J. Physiol. 176:
452-454.
13. Hart, J. S. and O. Heroux. 19 55. Exercise and temperature re-
gulation in lemmings and rabbits. Can. J. Biochem. Physiol.
33:428-435.
14. Hart, J. S. 1960. The problem of equivalence of specific dyna-
mic action: Exercise thermogenesis and cold thermogenesis
in Cold Injury, Transactions of the 6th Conference, July, 1958.
Josiah Macy, Jr. Foundation, New York.
15. Hart, J.S. 1962. Physiological adjustments to cold in non-hiber-
nating homeotherms.Proc. of the 4th Symposium on Tempera-
ture. Am. Inst, of Physics, in press.
16. Heroux, O., J. S. Hart, and F. Depocas. 19 56. Metabolism and
muscle activity of anesthetized warm and cold acclimated rats
on exposure to cold. J. Appl. Physiol. 9:399-403.
17. Jansky, L. 1959a. Oxygen consumption in white mouse during
physical exercise. Physiol. Bohemoslov. 8:464-471.
18. Jansky, L. 1959b. Working oxygen consumption in two species
of wild rodents (Microtus arvalis, Clethrionomys glareolus) .
Physiol. Bohemoslov. 8:472-478.
19. Jansky, L. 1959c. Einfluss der Arbeit und der niedrigen Tem-
peraturen auf denSauerstoffverbrauchdes Goldhamsters. Ac-
ta Soc. Zool. Bohemoslov. 23:266-274.
193
JANSKY
20. Jansky, L. 1961. Total cytochrome oxidase activity and its rela-
tion to basal and maximal metabolism. Nature 189(4768) :921-
922.
21. Kawahata, A. and L. D. Carlson. 1959. Role of rat liver in non-
shivering thermogenesis. Proc. Soc. Expt. Biol. Med. 101:
303-306.
22. Kleiber, M. 1947. Body size and metabolic rate. Physiol. Rev.
27:511-541.
23. Lefevre, J. and A. Auguet. 1933. La thermoregulation du tra-
vail. Rapports de ses courbes avec celles du repos. Ann.
physiol. physicochim. biol. 9:1103-1121.
24. Lefevre, J. and A. Auguet. 1934. Les courbes thermogregula-
trices et les rendements de la machine vivante dans les
grandes puissances de travail. Ann. physiol. physicochim.
biol. 10:1116-1134.
25. Schneider, W. C. and V. R. Potter. 1943. The essay of animal
tissues for respiratory enzymes. II. Succinic dehydrogenase
and cytochromoxidase. J. Biol. Chem. 149:217.
26. Sellers, E. A., J. W.Scott, and N.Thomas. 1954. Electrical ac-
tivity of skeletal muscle ofnormal and acclimated rats on ex-
posure to cold. Am. J. Physiol. 177:372-376.
27. Sreter, F. A. and S.M. Friedman. 1958. Sodium, potassium and
lactic acid after muscular exercise in the rat. Can. J. Bio-
chem. Physiol. 36:1193.
28. Svoboda, L. and L. Jansky. 19 59. Sexual differences in the cyto-
chrome oxidase activity of different organs of the gold ham-
ster. Physiol. Bohemoslov. 8:552-557.
194
OBGAN THEBMOGENESIS
29. Tipton, S. R. and W. L. Nixon. 1946. The effect of thiouracil on
the succinoxidase and cytochrome oxidase of rat liver. En-
docrinology 39:300-306.
30. Weiss, A. K. 1954. Adaptation of rats to cold air and effects on
tissue oxygen (Consumptions. Am. J. Physiol. 177:201-206.
31. Wells, J. G., B. Balke, andD.D.van Fossan. 1957. Lactic acid
accumulation during work. A suggested standardization of
work classification. J. Appl. Physiol. 10:51.
195
JANSKY
DISCUSSION
HANNON: I was particularly interested in your cytochrome
oxidase measurements since we have assayed the activity of this
enzyme in the liver and muscle of warm and cold acclimatized
rats. As you are no doubt aware the manometric technique for
measuring cytochrome oxidase leaves a lot to be desired. Des-
pite this, however, we have used the same procedure as you have
and have found that cold acclimatization leads to a marked increase
in the activity of this enzyme in both liver and muscle tissue.
Besides this acclimatization effect, we were also most interested
in the fact that our studies showed the liver has about six times
more cytochrome oxidase than muscle. Thus, if this enzyme is
an index of maximum metabolic capability, as you suggest, the
liver would have six times greater metabolic capacity per gram
of tissue than muscle. And, to speculate a bit further, if we assume
that the level of cytochrome oxidase reflects the capacity of a
tissue to produce heat and if we take into account the fractions of
the total body mass represented by liver and muscle, then the
theoretical ratio of total muscle heat production to total liver heat
production would be about 2:1. It will be most interesting to see
whether or not this theoretical ratio will be verified by future exper-
iments where organ heat production is directly measured.
JANSKY: In our own recent experiments concerning the cyto-
chrome oxidase activity in various organs of cold acclimated rats we
have found a liver :muscle ratio of 2.5:1 for cytochrome oxidase acti-
vity. These values of organ cytochrome oxidase correspond to the
values of maximal metabolism, which can be measured in working
animals or animals exposed to extreme cold. At present it is prac-
tically impossible to measure organ heat production in moving ani-
mals or on animals in extreme cold. The body temperature of small
laboratory animals falls very rapidly under these same conditions.
HANNON: In your data on mice and rats I noticed a convergence
of the curves for work metabolism with the curves for metabolism
in the cold. In the golden hamster, on the other hand, such a conver-
gence was not apparent. If you had carried the temperature lower, do
you feel the same convergence might have occurred in the hamster?
196
ORGAN THERMOGENESIS
JANSKY: Yes, I think this does look like incomplete results
but I have good evidence that the metabolism in the golden hamster
will fall at lower temperatures. When 1 measured the highest run-
ning speed the values fell very rapidly at low temperatures; there-
fore I expect it will also happen in the white mouse, the common
vole, and the bank vole.
HANNON: Did you ever compare the absolute amounts of run-
ning, say over a period of a day, for animals living in a cold environ-
ment and animals living in a warm environment?
JANSKY: No, we measured activity only during the short- time
experiment. It was the forced activity or, better to say, running
at the highest level which could be obtained at a certain tempera-
ture. The animals were not adapted to definite conditions.
HANNON: We have conducted a few experiments on voluntary
running of rats living in both warm and cold environments and have
observed a tendency for cold to reduce such activity. This would
seem to agree with a prediction made some time ago by Dr. Hart
that running is an inefficient method for augmenting heat produc-
tion in the cold. I would like to ask Dr. Hart if he has ever con-
firmed this prediction experimentally.
HART: Yes, but I have not published it. I did some measure-
ments on rats a few years ago, and there seems to be a range of
decreasing temperatures over which running speed actually in-
creases in the cold, reaches a peak, and then falls off again. I
think Melvin Fregley has also done this type of work.
HANNON: At certain low temperatures they do increase their
running speed?
HART: The activity depends upon the temperature and on the
acclimation conditions. In cold acclimated rats it increases with
fall in temperature to about 5 G below which it declines as shown
in Figure 7.
197
JANSKY
+3
+ 2
+ 1
0
-I
-2
-3
30*C O
200
100
BODY TEMP CHANGE IN ACTIVITY
SPONTANEOUS ACTIVITY
-10
Figure 7. Upper panel: change in colonic temperature from initial resting state
in rats running at 140(f cm/min in a treadmill for 30 minutes at various tempera-
tures. Symbols are for groups of 8 rats acclimated for 4 to 8 weeks to 6 C, (•)
and to 30 C (0). The rats were exposed to each temperature for 10 min before start
of run. Lower panel: me£(h spontaneous wheel activity of 4 rats acclimated to 6 C
(•) and 8 rats acclimated to 30 (0) tested twice at each temperature for one hour
periods. Total range of variation shown by shaded areas. Same rats used in both
tests show lowering of spontaneous activity at both high and low temperatures,
especially those which cause hypotherma during forced exercise. Presented by
J. S. Hart.
198
ORGAN THEBMOGENESIS
FOLK: The temperature of the running wheel may be a fac-
tor here. If the feet are well protected, some species of animals
might make out all right, especially the white rat running on the
cold metal. The colder it gets, the more this factor might influence
the animal.
HANNON: How did you force your animals to work? We tried
this and had all sorts of problems.
JANSKY: All animals were running in a wheel made from
plastic. I attempted to get really maximal values of running and
to avoid having them change their position; they could not turn
back, for instance. In the axis of the wheel was a load, which
could touch and excite the animals forcing them to run.
HANNON: Did you have any trouble? Dr. Drury in our labora-
tory has done similar forced- exercise experiments with the rat
in a motor driven screen drum. Other people have tried to make
their animals run on a treadmill. We, as well as the individuals
to whom I have talked, have encountered a lot of foot and tail
injury.
JANSKY: It depends upon which animal we use for the experi-
ments. Some animals are better runners than others. The white
rat for example is not a good runner. Many small animals run
very nicely, since it is something like a natural movement for
them. The species we used really did not need too much force.
FOLK: We have had a great deal of difficulty forcing exer-
cise, and 1 did not quite understand how you got maximum run-
ning. You stimulated them, and I would like to hear more about
that.
JANSKY: We used the wheel, and as I said, the wheel was
narrow enough to prevent the animals from turning around. The
animals, of course, were not restrained. On the axis of the wheel
we suspended a load which was freely movable. This load was
located behind the animal and would touch him if he ran slower.
It was heavy enough to excite the animals. Another improvement
199
JANSKY
is a net to avoid gliding or riding the axle. Running speed was
controlled with a Variac to prevent the animals from being car-
ried by the wheel and we were thus able to obtain really maximal
values.
HART: Did you keep increasing the speed until they could
just maintain that position without being forced?
JANSKY: Yes, of course they sometimes stopped, but in
this case the load touched them and they started again.
JOHANSEN: When you are comparing metabolic rates in
these groups, that is, working and resting animals, it seems
to me there will have to be a different insulation in the two. How
would this reflect in your curves?
JANSKY: Comparing the values of maximal working meta-
bolism and those of resting metabolism, we can see, that at the
same environmental temperature the animals produce more heat
at the level of maximal metabolism than in the resting state with-
out a significant change in body temperature. This would suggest
a certain decrease in total body insulation. On the other hand
the values of maximal working metabolism in all species of ani-
mals that we studied form a definite exponent to the body weight.
This would mean that there are no changes in total body insula-
tion in working animals of different species.
KLEIBER: This change in insulation makes shivering ineffi-
cient because it increases the dissipation of heat.
HART: I am interested to know whether anyone has an opinion
on the method of total cyt-ox activity as a measure of the theoreti-
cal maximum metabolic capacity.
HANNON: Theoretically, at least, this enzyme should be a
good index of maximum metabolic capacity since most of the
oxidative processes are eventually channeled through it. The
manometric method of assaying it, however, is often open to
criticism since you are using ascorbic acid to reduce the cyto-
chrome c substrate. There is always a possibility that the ascorbic
200
ORGAN THERMOGENESIS
acid itself is being oxidized and at differential rates. A more
modern and perhaps more accurate method of assaying cyto-
chrome oxidase involves a spectrophotometric procedure where
the cytochrome c substrate is reduced with hydrogen gas and
palladium prior to its addition to the reaction system.
JANSKY: Of course there is a certain amount of autoxida-
tion of ascorbic acid in the manometric procedure, but we can
avoid it very easily by extrapolating to zero after measuring the
oxygen consumption in Warburg flasks containing various concen-
trations of homogenate. I would say the spectrophotometric method
is probably more convenient except that we cannot easily measure
the oxygen consumption.
201
TEMPERATURE REGULATION AND ADAPTATION *
TO GOLD GLIMATES
J. Sanford Hart
Studies conducted largely during the last 10 years have provided
us with a reasonably complete picture of the temperature regulation
of mammals in cold climates. It is clear that several types of ad-
justments to cold are theoretically possible, having been described
in previous reports byScholanderetal. (1950a) and Hart (1957). The
most economical is structural modification in which insulation of the
fur and tissues is increased to such an extent that very low ambient
temperatures can be tolerated without increased energy expenditure.
The most wasteful are metabolic modifications in which extremes of
low temperature that limit survival are extended only by increase in
metabolic rate. Behavioural adjustments (huddling, burrowing, etc.)
can modify costly metabolic requirements through avoidance of cold.
The metabolic studies conducted on mammals have in general
been limited to short term tests which do not provide an integrated
picture of 24-hour energetics such as that provided for small birds.
Nevertheless, within the limitation of the methodology it has been
shown that quite distinct adaptive processes are in part dependent on
differences in body size and also in part on broad differences be-
tween aquatic and non-aquatic animals. Itwillbethe purpose of this
review to describe the temperature regulation and adaptation to cli-
mate found in free living mammals. The term "acclimatization" will
be used to describe individual physiological modification by climate
in nature while the term adaptation will refer to differences between
groups brought about through evolution. Other aspects of tempera-
ture regulation and acclimation to cold under laboratory conditions
will not be considered in this review since they have been treated
elsewhere (Garlson, 1954; Burton, 1955; Hart, 1957, 1958, and 1962;
and recent symposia, 1955, 1957, and 1960).
♦Contribution from the Division of Applied Biology, NationalResearch Council,
Ottawa, Canada. Issued as N.R.C. No. 6580.
203
HART
Non- aquatic Fur Bearers
The large fur-bearing mammals have been investigated by
American and Russian investigators. The best known work on this
subject was published by Scholander et al. (1950a, b, and c), who
were the only workers to demonstrate the existence of true evolu-
tionary climatic adaptation. This demonstration was made by com-
paring arctic and tropical mammals with respect to metabolic rates
at different temperatures and with respect to pelage insulation. It
was found that the tropical mammals that were investigated were
very sensitive metabolically to lowering of ambienttemperatures, as
shown by an abrupt increase in oxygen consumption with lowering of
temperature. In contrast, the arctic mammals did not begin to in-
crease their metabolism until they experienced much lower tem-
peratures and some could virtually remain in a basal state at tem-
peratures down to -40 G and below. The results for the tropical
raccoon (Procyon cancrivorus or lotor), the small arctic lemming,
and the Eskimo dog pup (Canis familiaris) (Figure 1) illustrate these
distinctions. Using Scholander 's terminology, it was observed that
the critical temperature and the critical gradient for increase in ox-
ygen consumption was lower in arctic mammals. Since the slopes of
the curves were extrapolated to body temperature, the lower critical
temperatures were associated with a smaller increase in metabolism
for a given drop in temperature.
The distinction between arctic and tropical mammals was not
associated with differences in the resting metabolism or in body
temperature (Scholander, et al., 1950 b), but with differences in body
insulation. Arctic mammals were found to have greater pelage insu-
lation (Scholander, et al., 1950c) than tropical mammals (Figure 2).
Some of the northern mammals investigated by Russian work-
ers, for example Ol'nyanskaya and Slonim (1947) whose work is
shown in Figure 3, were also relatively insensitive to cold but there
was a very large individual variability within each species. The in-
terpretation given to the data by the authors did not distinguish be-
tween zones of physical and chemical regulation; hence no apparent
critical temperatures were noted. The rabbit (Lepus timidus) , which
showed an increase in oxygen consumption at temperatures below
20 G, differed from the Alaskan hare (Lepus americanus) studied
204
MAMMALIAN COLD ACCLIMATION
METABOLISM
BASAL MOO
l200
t«%
1^
^. ^•.'ty ••'*
ESKIMO DOG
-w -JO
20 30 10
•
1
•
iT
^
.
•
•
•^
•
•
•
/ARCTIC LEnninG
1 L I
t •
• • «
20 30
» •
•t <
TROPICAL RflCCOOM
■10 -30 -20 -10 0 10 30 30 MO
AIB. TEMPERATURE INCtR
Figure 1. Effect of environmental temperature on the metabolic rates in eskimo
dog, arctic lemming, and tropical raccoon, expressed in terms of basal metabolic
rate = 100. From Scholander et al 1950.
205
HABT
iniULflTION
C5 lOTTon
WflTTrDM2y37«
CAKlBOU
CAL/n'/I'iHBb'i'CCjR
DflLL SHtEP
WOLT
»/ GRIZZLY BtRR
POLAR BCftB,
ICE WftTflP,
Figure 2. Insulation in relation to winter fur thickness in a series of arctic
mammals. The insulation in tropical mammals is indicated by the shaded area.
From Scholander et al., 1950.
206
MAMMALIAN COLD ACCLIMATION
120
80 -
40 -
Q.
^ 120
o
o
80 -
VULPES
VULPES
LAGOPUS
VULPES
•^
4-5.7 KG
_-^
3.9 -5.3 KG
1
, 1,1,1,1
1 .
1.1,1,1
NYCTEREUTES
LEPUS
PROCYONOIDES
•
-^, TIMIDUS
—
6.4-6.8 KG
-
\. 2.1 -2.8 KG
K,
-t::>*
==^^A;
^'^'"^'^-^
'
^^^^W"
1
1 1 1 1 1 1 1 1
1 1
1 1 1 1 1 1 1
-20 -10
+ 10 +20 -20 -10
TEMPERATURE »C.
+ 10 +20
Figure 3. Effect of temperature on metabolism of some Siberian mammals.
Redrawn from Ol'nyanskaya and Slonim, 1947.
207
HABT
by Irving etal. (1955), in which metabolism did not increase until the
temperature fell below -10 G.
The regulation of body temperature by arctic mammals and
birds has been thoroughly investigated by Irving and Krog(19 55),
who showed that it depended both on thick fur or feathers over the
body and on peripheral cooling of the thinly covered legs and other
exposed parts. The temperature distribution on the body skin and ex-
tremities of various arctic mammals at different temperatures is
shown in Figure 4. Warm skin is dependent on a temperature drop
through the fur; this phenomena has been described for certain arctic
mammals by Griffin et al. (1953). An example of such a temperature
gradient measured by thermocouples placed in parallel at various
depths is shown in Figure 5.
In thinly fur-covered legs, tissues replace fur as insulators.
Heat exchangers are possibly located in the area of the base of the
limbs, which show a sharp temperature drop. Such heat exchangers
have been demonstrated in tropical sloths (Gholoepus hoffmanni and
Bradypus griseus) byScholander (19 57) and may occur widely in fur-
red mammals (Scholander, 1955). However, the presenceof a marked
temperature drop in a limb or appendage does not necessarily signi-
fy the presence of a heat exchanger.
The cooling of peripheral tissues, which suggests tolerance to
cold not shared by warm tissues, is one of the remarkable proper-
ties of homeotherms. The demonstration of functional differences
between cool and warm tissues is difficult, although suggestive evi-
dence has been found in the distribution of fats of lower melting
point associated with low temperature function. Irving, Schmidt-
Nielsen, and Abramsen (1957) have shown that the distribution of
low melting point fats in various animals is not related to the cli-
mate in which the animals live. Other adaptations to cooling in peri-
pheral tissues have been demonstrated by Chatfield et al. (1953) in
the ability of the leg nerve of the herring gull (Larus argentatus) to
conduct at lower temperatures in distal than in proximal parts of
the nerve, and by Heroux (1959) in a capability of the ears of rats to
recover from non-freezing cold injury (Rattus norwegicus) during
prolonged cold exposure. Nevertheless, the pronounced retardation
208
MAMMALIAN COLD ACCLIMATION
40
o
§
6
8o
<$>
o°
o
k^
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30
•
•
•
•
•
• •
•
••
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•
•
•
•
•
•
3
DATA FROM
to
a:
UJ
0.
•
•
• •
•
•
7CARIB0U
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9
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•
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•
•
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o loor
UJ
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CO
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p
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• •
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•
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•
. j» —
•40
.20 0 20
AIR TEMPERATURE'C
Figure 4. Combined presentation of temperature measurements in 37 indi-
viduals of 4 species of mammals adapted to arctic life. From Irving and Krog, 1955.
209
HABT
tips of hairs
10 20 30 40 50 60
Distance from skin (millimeters)
40
30
20
10
- 0
--I0
20
0
■30
■40
70
Figure 5. Temperature gradient through fur of a sled dog thoroughly accli-
matized to the cold. R and S are rectal and subcutaneous temperatures. Each
point is the average of readings 10 to 20 minutes after insertion of gradiometer
from Griffin et al., 1953.
210
MAMMALIAN COLD ACCLIMATION
of functional activity of cool tissues is one of the puzzling phenome-
na of homeotherms which must be active at all temperatures. Func-
tional retardation by cold, at least for growth processes, has recent-
ly been demonstrated by Heroux (1960), who showed that the mitotic
activity decreased about 10-fold for a 10 degree lowering of tem-
perature in the skin of the rat.
While large adult arctic mammals are apparently able to with-
stand the most severe cold with little or no elevation of metabolic
rate, such may not be true for infant animals of the same species.
Baby caribou (Rangifer arcticus) born during June in the far north
are exposed to cold, wind, and precipitation that may lead to mor-
tality (Hart et al., 1962c). These calves are extremely sensitive to
cold, as shown by the marked elevation in metabolism resulting
from exposure to the harsh environmental conditions (Figure 6) . In
contrast, a 9- month calf of the same litter did not show elevation of
metabolism at temperatures down to -50 C.
Seasonal changes in some northern mammals have been shown
by Irving, Krog, and Monson (1955) for the porcupine (Erethizon
dorsatum myops) and red fox(Vulpes vulpes alascensis),but not for
the smaller red squirrel (Tamiasciurus hudsonicus preblei). The
winter fox and porcupine had lower critical temperatures and would
require a much lower temperature than summer animals for the
same metabolic response. These comparisons made in a review by
Hart (1957) also showed a similar trend for the lemming (Dicros-
tonyx groenlandicus) when Alaskan (winter) and Ottawa (summer)
test animals wereconsidered.lt was also pointed out that no changes
in the slopes of temperature- metabolism curves were found for the
deer mouse (Peromyscus maniculatus gracilis). In this species,
winter animals were able to resist lower temperatures (Hart and
Heroux, 1953) mainly by metabolic compensation, although some in-
dication of a small increase in insulation of winter animals was ob-
served.
The seasonal changes in these mammals are in line with the
seasonal changes in pelage insulation observed by Hart (1956), who
demonstrated the obvious fact that smaller mammals with body
weights below about 100 gm, unlike the larger ones, fail to achieve
significant protection through increased fur thickness during the
211
HABT
01
X
<
(n
15
O 10
m
<
WIND , WET FUR
INFANT_^ V WIND, DRY FUF
CALVES
• \
• V
STILL , DRY FUR
-40 -30 -20 -10 0 10 20 30 40
TEMPERATURE "C.
Figure 6. Heat production as a function of environmental temperature in nine-
month calf (X) and infantcalves instill air with dry fur (•) , wind with dry fur (©) and
wind with wet fur (O). The shaded area and broken line indicate lethal level for pro-
longed exposure. From Hart 1962c, in press.
212
MAMMALIAN COLD ACCLIMATION
winter. Consequently they must rely for protection on nest building,
huddling, and other devices as shown by Sealander (1952), Pearson
(1960), and Barnett (1956). Microclimatic observations by Pruitt
(1957) in Alaska have shown that the environment of the boreal red
back voles (Glethrionomys rutilus) 3-9 inches below the moss sur-
face ranges for the most part between -5 and +2 C when the air
tempeature falls to -40 C and below. Nevertheless, temperatures
in this range are well below the thermoneutral range of most small
mammals as shown by Hart (19 53), Kalabukhov (1940), Morrison and
Ryser (1951), Morrison, Ryser, and Dawe (1959), Pearson (1960),
Smirnov (1958), and various other workers, suggesting that meta-
bolic compensation is necessary to maintain homeothermy under
these conditions. Evidently the protection afforded to Peromyscus
maniculatus during the winter in the Ottawa area is likewise insuf-
ficient to prevent cold exposure since metabolic acclimatization to
winter conditions was pronounced (Hart and Heroux, 1953). Unpub-
lished observations of Hart and Heroux have likewise shown season-
al metabolic acclimatization in wild dump rats, and similar obser-
vations have been made on short tailed shrews. Details of the sea-
sonal metabolic changes in rats reviewed by Hart (196 2b) are beyond
the scope of this review.
Semi- aquatic Fur Bearers
Certain fur bearing mammals such as beaver, otter, and musk-
rats are dependent on an aquatic environment for their food and
shelter, butspendonly a small portion of their total life in the water.
These mammals are protected from the cooling effect of the water
by a layer of air trapped in the fur. In general, very little is known
concerning temperature regulation in this group of mammals. How-
ever, observations of the author (Hart, 1962a) onmuskrats (Ondatra
zibethicus) in air and in water illustrate some of the problems in
the temperature regulation of a semi- aquatic mammal.
Muskrats tested in air at various temperatures for about 1 hour
showed an increased heatproductionattemperatures below a critical
level of approximately 10 C and a gradual lowering of body tem-
perature which became pronounced below -40 C (Figure 7). No
appreciable seasonal changes were observed.
213
HART
COLONIC TEMPERATURE "C
ro
OJ
ML. 0, CONSUMED PER KG.
1000 2000 3000
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i ' ! ' 1
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Figure 7. Oxygen consumption and body temperature in muskrats in response to!
air and water temperatures. Summer animals are indicated by (•) and winter by (O).
From Hart, 1962, in press).
214
MAMMALIAN COLD ACCLIMATION
Oxygen consumption and body temperatures of animals placed
in a small tank of water for about three fourths of an hour increased
progressively with lowering of water temperature below a critical
level of about 30 G. Colonic temperatures fell after the animals
were in water at all temperatures below about 20 C. During both
summer and winter, it was apparent that the heat production was in-
adequate to offset hypothermia for prolonged periods at winter tem-
peratures around 0 C. Skin temperatures measured under the fur
confirmed the presence of an air layer, because a gradient of ap-
proximately 7° C was maintained in the fur at a water temperature
of 0° G. Nevertheless, this air was insufficient to prevent general-
ized cooling. Since the animals were all healthy, muskrats in nature
may tolerate limited hypothermia during winter while under the ice
and may limit exposure to cold water to shorter excursions than the
test exposures in these experiments.
Bare Skinned and Aquatic Mammals
Metabolic studies have been carried outby Irving and coworkers
on swine in Alaska (19 56) and on seals of the Atlantic coast (1957,
1959). Swine and aquatic mammals willbe considered together in this
section because of similarities in problems of temperature regula-
tion associated with the presence of a minimal fur cover and an in-
sulating subcutaneous layer of fat or blubber.
Both the swine at various air temperatures (Figure 8) and the
harbor seals (Phoca vitulina) in air and in water (Figure 9) showed
marked temperature gradients through the tissues which were char-
acteristic of the insulating layers of fat and the different outside
cooling effects. The distributions of surface temperatures on the
body surfaces of swine and seals were also rather similar at com-
parable air temperatures, indicating similarity in physiological in-
sulation by cooling in these two animals. The critical temperatures
for increase in metabolic rate (about 0 C) were also comparable in
Alaska swine and harbor seals during the summer.
In water, the surface temperatures of harbor seals were, as
anticipated, only slightly greater than ambient, and the critical tem-
perature was elevated from approximately 0 Cto20 G (Figure 10).
215
HART
DEPTH ON GRADIENT
7o io ?0 60 80 100
Figure 8. Typical temperature gradients through superficial layers of the swine
in air at several temperatures from February to August. Because of seasonal
changes in depth of gradient, the scale of the abcissa is observed temperature in
tissues/body temperature in G x 100. Data from Irving, 1956.
216
MAMMALIAN COLD ACCLIMATION
0. 3dniva3dW3i anssii qnv wnia3w
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217
HABT
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A AIR \ oO WATER ^^
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TEMPERATURE 'C
Figure 10. Oxygen consumption of seals in the air (A) and in water (O) at
different temperatures during the summer. Body skin temperatures as a function
of temperature of the medium are also shown. Results from Hart and Irving, 1959.
218
MAMMALIAN COLD ACCLIMATION
This represents a difference of about twenty- fold in the cooling ef-
fect of air and water, but the total insulation (body + medium) in
water was about 50% of its value in air. It can be noted that the meta-
bolic response closely parallels the skin cooling in air and water.
The parallel between peripheral cooling and metabolic response
was also seen between different seals and was reflected in the indi-
vidual variability (Irving and Hart, 1957) (Figure 7). The smallest
seal, characterized as the "runt," had a very thin layer of blubber
and consequently was unable to maintain a surf ace temperature low-
er than 6 C to 8 G when in water at 0 C. The high heat flow re-
sulted in a high oxygen consumption at all temperatures. In other
harbor seals with a considerably deeper and less steep gradient
through the thicker blubber, there was a much lower surface tem-
perature and a maintenance of resting metabolism down to a criti-
cal level of about 10 C. However, a harp seal (Phoca groenlandica) ,
with a still deeper gradient and a lower surface temperature, was
able to compensate completely without elevationof metabolism even
in ice water. This represents the greatest cooling load experienced
by mammals in nature and the harp seal has the greatest physiologi-
cal insulation known for mammals.
Harbor seals tested in December at St. Andrews, N. B., and at
Woods Hole, Massachusetts, during the summer revealed seasonal
changes that were comparable to those found by Irving, Krog, and
Monson (1955) for the red fox and the porcupine. During the summer
there was a greater elevation of oxygen consumption in cold water
than during the winter and thecriticaltemperature was raised from
o o
about 11 C to 20 C in water. There was, therefore, a greater
physiological insulation in winter than in summer; this was associ-
ated with changes inperipheral tissues. No anatomical basis for this
change was noted. The nature of the seasonal alteration was such
that the differences were observed even at the same body skin tem-
perature (Figure 11). This puzzling phenomenon suggests that more
heat is lost in summer than in winter at the same body skin tempera-
ture. This could be accounted for by a greater evaporative heat loss
from the lungs or by a greater heat loss from the appendages,
neither of which were measured in this investigation.
219
HABT
40 -
10 -
"RUNT" ® "^
N»
X «
V
X
V
O ^
SUMMER v^ „„ ^>v
o ^
t ° ^^°°
WINTER'.^ ^V.0 o
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1 1 1 , 1 , 1 ,
10 20
TEMPERATURE °C
30
Figure 11. Oxygen consumption as a function of body skin temperature for seals
during wmter (A9) and summer (AO) in air (AA) and m water (#0). Results from
Hart and Irvmg, 1959.
220
MAMMALIAN COLD ACCLIMATION
While the temperature of the body skin was uniformly related
to the water temperature, temperatures of the appendages showed
striking fluctuations, suggesting independent control of heat loss,
which might be a basis for seasonal differences. The nature of the
fluctuations in temperature of the flippers was consistent with the
view that control of peripheral heat loss was affected by the pre-
sence of vascular heat exchangers, such as those described by Scho-
lander and Schevill (1955) for porpoises (Lagenorhynchus acutus and
Tursiops truncatus).
Comparison of Different Species
Metabolic response to cold versus skin temperature. It is diffi-
cult to compare the metabolic responses of species which live in
such differentmelia as air and water. One basis is to make the com-
parisons relative to the actual body skin temperature of the species
in question. This has the merit of relating the response to some as-
pect of the animals' own perception system to which it must be re-
sponding rather than to some physical aspect of the environment.
The use of skin temperature is disadvantageous because it is highly
variable and is known only for a few species. Skin temperatures
measured over the mid part of the body on the flank or back of a
series of animals are correlated with oxygen consumption in Figure
12, as originally shown by Hart (19 6 2b). The sources of the data are
indicated in the legend. Comparisons of the same species relative to
air temperature are also shown.
Clearly, the various species are distributed in a series with re-
spect to the sensitivity of the skin as a factor in the metabolic re-
sponse to cold. All the land mammals tested show increased heat
production at relatively high skin temperatures. Next in order is the
semi- aquatic muskrat, followed by the swine. The cooling of the
muskrat skin for the same metabolic response is not as great as that
for the harbor seal, especiallyduring the winter. The least sensitive
species was the harp seal, which showed no increase in metabolism
even in ice water. The range of responses indicates the very great
species differences that exist in toleration of peripheral cooling and
in temperature range of peripheral stimuli required to illicit that re-
sponse. It has also been shown for the harbor seal and for the leg
221
HABT
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222
MAMMALIAN COLD ACCLIMATION
nerve of the herring gull that these responses may be altered by ac-
climatization in the same species.
The comparisons in Figure 12 also illustrate the fact that the
metabolic sensitivity to cold may differ, depending on whether the
oxygen consumption is correlated with skin or with air temperature,
e. g., swine and muskrat. This is because the fur provides the insu-
lation for the muskratbut not for the swine. Similarly, the thick fur-
red arctic mammals with warm skin may be as sensitive to lowered
skin temperatures as the rat, caribou, and man, even though the most'
severe arctic conditions canbe withstood without elevation of resting
heat production (Scholanderetal., 1950a). Therefore, arctic and tro-
pical mammals may be quite similar with regard to the skin cooling
required for a given metabolic response.
Metabolic response to cold in relation to body size and insulation
of the fur. A summary of data published in the fourth Temperature
Symposium of the Americanlnstituteof Physics (Hart 196 2b)is illus-
trated in graphic form in Figure 13. The slope of the temperature-
metabolism curve below the critical level is given as the ratio of the
temperature drop to the increase in metabolism, which is dimension-
ally comparable to an insulation rather than a conductivity function.
This is done to facilitate comparison of slopes with fur insulation
(open circles) for the few species for which data are available.
It may be seen that the slope tends to increase with increase in
body weight, but that there is an enormous increase in species vari-
ability with increase in weight. This is because the small mammals
are all metabolically sensitivetocold while the large mammals may
be sensitive or insensitive. The least sensitive are the arctic mam-
mals with thick fur which give the three highest values for slope, e.
g., snow-shoe hare in winter, red fox, and white fox. The larger
mammals may also have little fur and lower values for slope, e. g.,
dog, harbor seal in summer, and Brahaman bull.
When slope is related to insulation of the fur (broken line), there
appears to be a much closer correlation. However, it is obvious that
the same correlation would notbe applicable for either bare-skinned
or aquatic mammals with subcutaneous fat and a thin fur cover. The
223
HAET
INSULATION "C/CAL/M^/HR.
0.5 1.0 1.5
.01 0.1 1.0 10
BODY WEIGHT KG.
100
1000
Figure 13. Overall body insulation (•) expressed as the slope of the tempera-
ture-metabolism curve below the thermoneutral range ( C/calA)ody weight 3/4 /hr)
in relation to body weight, and slope (O) as a function of pelage insulation (brokeni
line). Data are replotted from table given by Hart 1962b.
224
MAMMALIAN COLD ACCLIMATION
correlation may be applicable to most fur bearers, but information
at present is inadequate.
SUMMARY AND CONCLUSIONS
The temperature regulation and adaptation of mammals to cold
climates follows different patterns in large and small mammals, and
in fur-bearing compared to bare- skinned or aquatic mammals. The
large arctic mammals with thickfur have a capability for withstand-
ing the severest climatic conditions without elevation of heat produc-
tion. This is accomplished by considerable cooling of the peripheral
areas and appendages as well as by great insulation of the fur. The
combined effect of these insulators provides a variable response
graded precisely to the temperature of the environment in a way not
yet fully understood. Climatic adaptation to arctic and tropical en-
vironments as well as acclimatization to summer and winter en-
vironments appears to be related to alteration in insulation of the fur
rather than to changes in body temperature or in metabolic rate.
However, infant animals of arctic species may be very sensitive to
temperature.
In the mammals of small body weight, compensation for cold
through changes in insulation is not possible, and when protection is
inadequate, an elevation of heat production is necessary. Evidence
has been presented that small mammals such as mice and wild rats
show an increased cold resistance during the winter that is the re-
sult of the development of an increased metabolic capacity. It is
therefore apparent for the few species studied that cold exposure
and elevation of metabolism must have occurred during the winter
to account for the development of the observed seasonal acclimatiza-
tion.
The only fur-bearing semi- aquatic mammal studied (muskrat)
showed no evidence ofseasonal change even though exposure to water
at 0° C during the winter seems inescapable. The surprising feature
of the study was the degree of body cooling observed during short
term exposure to cold water and the failure of fur insulation and
225
HART
metabolism to compensate adequately for the observed cooling. It
was suggested that mild hypothermia might be tolerated by musk-
rats in nature.
In swine and in the true aquatic mammals with an insulating
layer of blubber, living tissues replace the fur as the effective insu-
lators, and there is pronounced cooling of peripheral tissues. In har-
bor seals exposed to ice water, there is a reduction of heat produc-
tion during the winter, signifying a seasonal change in insulation of
the living tissues. Arctic harp seals are superior to harbor seals
during the winter since they can tolerate ice water without lowering
body temperature or elevating heat production.
When the body skin temperature of various species are com-
pared, very large differences are found in the temperatures corres-
ponding to elevation of heat production. In the fur-bearing land mam-
mals studied, heat production increased with only slight skin cooling
whereas in aquatic mammals a pronounced skin cooling was necess-
ary. The swine and muskrat were intermediate. The distinction in
the metabolic response to cold between land mammals and aquatic
mammals is much more apparent with respect to skin temperature
than to air temperature.
The metabolic response to cold in different non- aquatic species
is related both to insulation of the fur and to body size. However,
while small mammals with thin fur are metabolically sensitive to
cold, large mammals may be sensitive or insensitive, depending on
the fur insulation. In aquatic mammals so far studied the fur insula-
tion was negligible and hence did not affect the metabolic response
to cold. Temperature regulation in aquatic mammals is effected
through physical regulation of heat loss in the general body surface
and particularly in the appendages.
226
MAMMALIAN COLD ACCLIMATION
LITERATURE CITED
o
1. Barnett, S. A. 1956. Endothermy and ectothermy in mice at -3
C. J. Exp. Biol. 33:124.
2. Burton, A. C. and O. G. Edholm. 1955. Man in a cold environ-
ment. Edward Arnold, London.
3. Carlson, L. D. 1954. Man in cold environment, a study in physi-
ology, Alaskan Air Command, Arctic Aeromedical Labora-
tory. U. S. Dept. Commerce, Office of Technical Services P.
B. report 111716, Washington.
4. Chatfield, P. O., C.P.Lyman, and L. Irving. 1953. Physiological
adaptation to cold of peripheral nerve in the leg of the herring
gull (Larus argentatus). Am. J. Physiol. 172:639.
5. Griffin, D. R., H. T. Hammel, H.M.Johnson, and K. S. Lawson.
19 53. The comparativephysiology of thermal insulation. Final
Rept. Contract 33 (038)-12764between US Air Force and Cor-
nell University.
6. Hart, J. S. 1953. Energy metabolism of the white footed mouse,
Peromyscus leucopus novaboracensis after acclimation at
various environmental temperatures. Can. J. Zool. 31:99.
7. Hart, J. S. 1956. Seasonal changes in insulation of the fur. Can.
J. Zool. 34:53.
8. Hart, J. S. 1958. Metabolic alterations during chronic exposure
to cold. Fed. Proc. 17:1045.
9 . Hart, J. S. 1957 . Climatic and temperature induced changes in the
energetics of homeotherms. Revue Can. de Biol. 18:133.
227
HART
10. Hart, J. S. 1962a. Seasonal changes in wild rats and muskrats.
Can. J. Zool., in press.
11. Hart, J. S. 1962b. Physiological adjustments to cold in non-
hibernating homeotherms. Proc. 4th Temp. Symposium. Am,
Inst. Physics, Columbus, Ohio, in press.
12. Hart, J. S. 1962c. The influence of climate on metabolic and
thermal responses of infant caribou. Can. J. Zool., in press.
13 . Hart, J, S. and O. Heroux. 19 53. A comparison of some-seasonal
and temperature- induced changes inPeromyscus: Cold resis-
tance, metabolism and pelage insulation. Can. J. Zool. 31:528.
14. Hart, J. S. and L. Irving. 1959. The energetics of harbor seals
in air and in water with special consideration of seasonal
changes. Can. J. Zool. 37:447.
15. Heroux, O. 1959. Histological evidence for cellular adaptation to
non-freezing cold injury. Can. J. Biochem. Physiol. 37:811.
16. Heroux, O. 1960. Mitotic rate in the epidermis of warm- and
cold- acclimated rats. Can. J. Biochem. Physiol. 38:135.
17. Irving, L. 1956. Physiological insulation of swine as bare-
skinned mammals. J. Appl. Physiol. 9:414.
18. Irvinj, L. and J. S. Hart. 1957. The metabolism and insulation
of seals as bare- skinned mammals in cold water. Can. J.
Zool. 35:497.
19. Irving, L. and J. Krog. 1955. Temperature of skin in the arctic
as a regulator of heat. J. Appl. Physiol. 7:355-364.
20. Irving, L., H. Krog, and M.M^nscn. 1955. The metabolism of
some Alaskan animals in winter and summer. Physiol. Zool.
28:173.
228
MAMMALIAN COLD ACCLIMATION
21. Irving, L., L. J. Peyton, and M.Monson. 19 56. Metabolism and
insulation of swine as bare-skinned mammals. J. Appl.
Physiol. 9:421.
22. Irving, L., K. Schmidt- Nielsen, and N. S. B. Abramsen. 1957.
On the melting point of animal fats in cold climates. Physiol.
Zool. 30:93.
23. Kalabukhov, N. 1.' 1940. Influence of temperature upon oxygen
consumption by wood- mouse (Apodemus silvaticus) and
yellow-necked mice (Apodemus flavicoUis). Compt. rend.
(Doklady) de I'acad. Sci. de I'URSS. N. S. 26:89.
24. Morrison, P. R. and F. A. Ryser. 19 51. Temperature and meta-
bolism in some Wisconsin mammals. Fed. Proc. 10, No. 1.
25. Morrison, P. R., F. A. Ryser, and A. R. Dawe. 1959. Studies on
the physiology of the masked shrew. Physiol. Zool. 32:256.
26. Ol'nyanskaya, R. D. and A. D.Slonim. 1947. On the adaptability
of organisms to very low temperatures of the environment.
Invest. Acad. Nauk. SSSR. Ser. Biol. 245.
27. Pearson, O. P. I960. The oxygen consumption and bioenergetics
of harvest mice. Physiol. Zool. 33:152.
28. Pruitt, W. O. 1957. Observations on the bioclimate of some
taiga mammals. Arctic 10:131.
29. Scholander, P. F. 19 55. Evolution of climatic adaptation in
homeotherms. Evolution 9:15.
30. Scholander, P. F. 1957. Counter current heat exchange and vas-
cular bundles of sloths. J. Appl. Physiol. 10:405.
31. Scholander, P. F., R. Hock, V. Walters, F. Johnson, and L.
Irving. 1950a. Heat regulation in some arctic and tropical
mammals and birds. Biol. Bull. 99:237.
229
HABT
32. Scholander, P. F., R. Hock, V. Walters, and L. Irving. 1950b.
Adaptation to cold in arctic and tropical mammals and birds
in relation to body temperature, insulation and basal meta-
bolic rate. Biol. Bull. 99:259.
33. Scholander, P. F., V. Walters, R. Hock, and L. Irving. 1950c.
Body insulation of some arctic and tropical mammals and
birds. Biol. Bull. 99:225.
34. Scholander, P. F. and W. E. Schevill. 1955. Countercurrent
vascular heat exchange in the fins of whales. J. Appl. Physiol.
8:279.
35. Sealander, J. A. 1952. The relationship of nest protection and
huddling to survival of Peromyscus at low temperature. Eco-
logy 33:63.
36. Smirnov, P. K. 1958. Characteristics of heat exchange in the
harvest mouse, Micromys minutus. Translation of Doklady
Acad. Nauk. SSSR in Doklady Biol. Sci. Section 117(4); 717.
37. Symposium sur I'acclimation au froid. 1957.Rev.Can.de Biol.
16:133.
38. Symposium in Centre Nationale de la Recherche Scientifique.
1955. Arch. Sci. Physiol. 9:C -C .
1 2^17
39. Symposium on cold acclimation. 1960. Fed. Proc. 19:1.
230
MAMMALIAN COLD ACCLIMATION
DISCUSSION
MORRISON: I have some data on related species living in
the same environment. These show differing thermal sensitivi-
ties that can be rather nicely correlated with their habits. I hope
this will be of interest because it represents work done with
Dr. F. A. Ryser in this laboratory some years ago.
These are simply measurements of the body temperature
against the ambient temperature. Figure 14 compares the two
common voles taken from the nearby Chena River in February
and March. Clethrionomys has excellent regulation. Microtus,
on the other hand, falls off badly at low ambient temperatures
both in regard to the summer temperature and the higher winter
temperature. This correlates with their habits since Microtus
stays strictly inside its burrow system when it is cold, whereas
Clethrionomys does come out and move around.
Figure 16 compares the two lemmings from the far north.
Dicrostonyx regulates well but Lemmus is not so effective.
Dicrostonyx is seen above the snow when it is very cold whereas
Lemmus carefully restricts himself to his subnivean micro-
climate. Incidentally, Dr. Hart showed a slide from Dr. Scholander
(Hart, Fig. 2) on insulation values in various northern mammals.
There the lemmings were grouped, but the two highest values
represented Dicrostonyx while the four lower points were for
Lemmus, which difference correlates with the physiology and
behavior.
HART : How long were the exposures of the Microtus?
MORRISON: These were caged animals living at these low
temperatures, so there were a number of hours of exposure, days
in some cases.
HART: Continuous exposure?
MORRISON: Yes.
231
HAET
-20 -iO
T^ IN °C
Figure 14. Body temperature in Clethrionomys and in Microtus as a function
of ambient temperature. Circles, winter trapped animals from Fairbanks; squares,
summer trapped animals.
232
42
40
38
IN
42
40 -
38"
MAMMALIAN COLD ACCLIMATION
T:
•7
LEPUS
TAMi/kSCIURUS
lit
H
::
p
-20
-10
iO
20
T^ IN "C
Figure 15. Body temperatures of the snowshoe hare and the red squirrel at var-
ious environmental temperatures. Symbols as in Figure 14.
233
HART
IRVING: They must be able to take quite a lot, because I
caught a live Dicrostonyx in March on one of the sand islands
off the coast east of Barrow. It was over a mile from shore; we
heard him scratching around during the night and he was still
alive in the morning. We then traveled about ten miles off-
shore on the ice and found one Dicrostonyx which had died out
there, but it was obviously not killed by, or transported by a
predator. I saw the tracks of several others around seven or
eight miles from the shore, which must take them quite a long
time at their rate of travel.
MORRISON: One of our group tracked a lemming a couple
of miles out on the ice off Barter Island. There was no indica-
tion of where it was going, but the tracks were in a straight line,
not as though it was searching or meandering.
HANNON; With respect to running ability we have observed
that the hamster, which is about the same size as the lemming,
can run six to eight miles a day — all of this distance being covered
entirely during the hours of darkness.
FOLK; The white rat can run 21 miles, so they are capable
of running distances, for example one ran 28 miles in 24 hours
and another ran 32 miles in 24 hours.
IRVING: But the lemmings were found under conditions where
even with their hardiness they were expending metabolic energy
at a very rapid rate for maintenance of body temperature.
JOHANSEN: I may perhaps comment on my work on the
muskrats. One project was concerned with the fact that the musk-
rat has a very dense fur and a naked tail, which suggested to me
that this tail might have a crucial importance as a heat exchanger;
and this turned out to be the case. The tail of the muskrat as it
was studied by temperature measurements and plethysmography
(where Charles Eagan gave expert help) showed that the tail blood
flow can change by a factor more than 400 within a very short
234
MAMMALIAN COLD ACCLIMATION
40
38
36
'5
IN
40
38 -
36
42 1
V
• • )• •
• •
• .••
i L
J I
i
0'Cf?OSTONYX
LEMMUS
-20 -10
iO
T^ IN °C
Figure 16. Body temperature in Dicrostonyx and in Lemmus as a function of
ambient temperature. Symbols as in Figure 14.
235
HART
40
38
36
°C 34
32
30
28
26
24
22
/'■' sj
■
\ RECTAL
TEMPERATURE
-
/
- ^
"
K ■--
S.'^-^X. .-• TAIL
\ \ ' TEMPERATURE
■
\
\
-
\
-
\
-
\
-
BLOOD
FLOW
-
if
■i
-
-
300
280
260
UJ
240 3
z
220 i
\
200 ^
in
180 ^
y-
160 o
(J
140 g
120 c
100 _
80
60 Q
o
40 3
m
- 20
4 6 8 10 12 14 16 18 20 22 24 26 28 30
TIME IN MINUTES
Figure 17. Changes in tail blood flow, rectal and tail temperatures during a
vasodilation of the muskrat tail. Note the tremendous increase in tail blood flow.
236
MAMMALIAN COLD ACCLIMATION
time (Fig. 18A). If the muskrat is overheated slightly either by
exercise or by being exposed to a high environmental tempera-
ture, his tail is "flushed" immediately. The skin temperatures
are practically as high as the body temperature.
I proceeded by trying to elucidate the mechanisms behind
these profound effects and the data acquired from doing nerve
blocks of the tail indicate that there exists such a thing as a
vasodilator innervation to the skin in the tail of the muskrat. If
1 nerve-blocked the tail, the animal became hyperthermic in a
very short time and in one instance an animal succumbed and
died of heat apoplexia when his tail was not intact (Fig 19 A).*
In the other project, I tried to assess the importance of the
air layer in the fur as an insulator. I compared two groups of
animals, one with the fir layer intact and one with the air depleted
by way of surface active materials, such as detergents. I anesthe-
tized the animals to standardize the condition and to avoid dif-
ferences in movement. I found that the intact muskrat had a volume
of about 800 cc, of which about 200 cc was air. In other words,
almost 25% of the volume of the muskrat is air. If these two groups
are subjected to water cooling or to air cooling, the temperature
drops five times as fast in the one depleted of the air.**
HANNON: There is one question I would like to ask Sandy.
In animals such as the muskrat and possibly wild rats living
outdoors continuously, do you feel it might be possible for these
animals to be continually cold-acclimatized, summer and winter?
In the muskrat, for example, in these northern areas, the water
is still quite cold in the summer. It may be that they get a level
*Johansen, K. 1962. Heat exchange through the muskrat tail. Evidence for vaso-
dilator nerves to the skin. Acta Physiologica Scandinav. (in press).
**Johansen, K. 1962. Buoyancy and insulation in the muskrat. J. Mammal, (in
press).
237
HART
_ ■ _ ^ ' — RECTAL
TEMPERATURE
\,
30
BODY 1 [~
HEATING 1
'cooling of TAIL
■
/V1
/
AMBIENT TEMP IB-20'C
■
/
TAIL NERVE
■•— BLOCKED — •
BODY HEATING
15
■
. / I
^ ^
TAIL
TEMPERATURE
30 40 50 60
TIME IN MINUTES
Figure 18. First portion of the figure demonstrates the course of rectal and
intracutaneous tail temperature during body heating and consequent vasodilation
in a normal undisturbed subject. Subsequently the tail is cooled down, and nerve
blocked. Body heating is reapplied but the tail vasodilation and the consequent heat
loss is prevented and a rapid increase in rectal temperature is seen.
238
MAMMALIAN COLD ACCLIMATION
of acclimatization and just maintain it. And that is why you cannot
see the difference between summer and winter.
HART: I always think of it as a matter of degree. The musk-
rat is probably to a certain extent acclimatized in the summer,
too, but you would think that they would be more so in the winter.
JOHANSEN: We did some measurements in the field here
and the temperatures in the pushups of the muskrats are rather
strikingly high during winter. They are from 5 C to 10 G above
freezing in the -40 C weather. We do not really know how much
time they spend in the cold water; this is what we should find out.
HANNON: You have essentially 0 C water in the winter time,
and maybe it will go as high as 15 C in the summer and maybe
a little higher. You still have a pretty big differential, but on the
other hand they may be a little more active in the summer time in
the water, so they get a longer exposure. ,
HART : It is possible.
IRVING; Dr. Fay has been making some measurements from
time to time in the New York Zoo on the temperature on the body
skin and flippers of walrus, both young and old. He has been able
to get some measurements of wild walrus around St. Lawrence
Island, too, and he finds a fair regularity in the relation between
the temperature of the skin of the body in air or water. As Hart
and I found in harbor seals, the flippers may be quite different
from the body and apparently fluctuate as if for fine adjustment
of temperatures. Fluctuations in the extremities are also subject
to non-thermal excitation, and in absence of obvious relation to
heat, are ascribed to plain nervousness.
PROSSER: In your summary slide, comparing the different
mammals, you suggested that there might be differences in the
sensory sensitivity.
HART; Do you mean sensitivity to skin temperature?
239
HART
PROSSER; Yes. Is it possible that there might be differences
in the endocrine response mechanism?
HART: You might have the same input and a different res-
ponse to the input.
PROSSER: Have you any evidence about the response of
either the thyroid or adrenal in these different series?
HART: Absolutely none.
PROSSER: It seems to me that endocrine response would be
an alternate explanation. Of course this could be explored.
EAGAN: However, this endocrine response could be mediated
only through the nervous system.
PROSSER: Yes, but the sensory input might be the same.
HART: Is there any way of assessing sensory input in animals?
I do not know of any.
PROSSER: It certainly would be worthwhile to try to record
the nerve impulses in response to a given cold stimulus.
KLEIBER: I do not think I would be accused of particularly
being in love with body surface or against the three- fourths power
of body weight. But when you express the specific insulation, I
wonder if it would not be wise, for internal consistency, to express
the metabolic rate per unit surface, whatever it might be. I mean
that you should use weight to the two- thirds power instead of the
three- fourths, because otherwise you might introduce a side effect
in this insulation which is actually not present.
HART: This is really a measure of metabolism, though.
KLEIBER: Yes, but the metabolism in this case is related to
heat exchange and the metabolism related to heat exchange is a
240
MAMMALIAN COLD ACCLIMATION
function of the surface or is related to surface area rather than
to metabolic size.
HART: It might not make too much difference because they
are rather close anyway.
KLEIBER; That is right, except when you go from one kilo-
gram to a thousand kilograms.
MORRISON: They are close, but there is a difference between
the two functions. In our measurements, taking the thermal con-
ductance from the slopes of the metabolism- ambient temperature
curves, a rather elegant relation describes some of the smaller
mammals (<500 g). Thus, conductance is equal to the square root
of the body weight if the weight is expressed in grams and the con-
ductance in ccO (gms x hr x G)
2
HART: If you express metabolism as a square root function
of body weight, it should then be independent of weight differences.
MORRISON: The exponent will change depending on whether
the expression is per gram or per animal. That would change the
exponent.
VIEREGK: In your figure comparing skin temperatures of
different species at different environmental temperatures, where
on the animal's body do you take the skin temperature? Do you have
any idea of how to get an average skin temperature for the surface?
HART: It was not an average at all. They were simply repre-
sentative temperatures taken over the trunk of the body.
VIERECK: But the fur is very thick in the back and thin in the
front. Where do you take the temperature?
HART: This is underneath the fur, and in the caribou they
were averages of several measurements taken on one side of the
fur. In the rat measurements were approximately at the same place.
241
HAET
VIERECK: Do you look for a place where the fur is thickest?
HART : Not necessarily.
FOLK: Possibly some experiments will be able to provide the
activity of the animal during oxygen consumption. Benedict has
stressed this so much. You find two groups of animals in your
series, at very cold temperatures where the metabolism is up high.
Some of the animals are quite restless and move around, while
others curl up and are quiet with high metabolic rates at these cold
temperatures.
HART; In those which I have observed, I find almost invariably
that they are huddled up and not moving at all. When the cold is such
that the metabolic rate is increased close to its maximum, then
these animals are seldom if ever moving in my experiments.
FOLK: Can you give examples of animals that were moving
under these circumstances? I think of the tropical raccoon. They
might be restless, which would account for part of the high
metabolism.
HART: Were there not some measurements by Erikson* on
ground squirrels which showed a definite correlation of meta-
bolic rate with activity in the cold? In these animals the activity
was greatest at the lowest temperatures which increased the oxygen
consumption further.
♦Erikson. H. 1956. Observations on the metabolism of arctic ground squirrels
(Citellus parryi) at different environmental temperatures. Acta. Physio l.Scandinav.
36:66-74.
242
TEMPERATURE RESPONSES AND ADAPTATIONS
IN DOMESTIC ANIMALS
Max KLeiber
The body temperature of homeotherms is nearly the same as
that of man, about 37 C. Consistent changes from the average do
occur, but they are not related to body size or to geographic dis-
tribution of the animal. Rat and elephant temperatures are about 1
C cooler than those of man; cow, sheep, and swine, about 1 C hot-
ter, rabbit and dog about 2 C* hotter; and the camel lets its body
o o
temperature vary from 34 C to36 C and seems not to mind a tem-
perature of 40 C if this is necessary for saving water.
Figure 1, somewhat schematized from data of Johnson, et al.
(1958) shows that below an environmental temperature of 80 F
(27 C) , cow and man regulate their body temperatures somewhat
more accurately than does the rabbit. Man is much more strict
in keeping cool in a hot environment than cow or rabbit. The cow's
body temperature rises when the environmental temperature is
higher than 80 F (27 C). This is also the case for cold adapted
rabbits, whereas rabbits adapted to a warm climate do not raise
their body temperatures before the air temperature exceeds 90 F
(32° G).
I am not aware of any biological theory which would explain
why in the evolution of homeotherms that 36 C to 40 C body tem-
perature has been so much more advantageous than other body tem-
peratures. For all conditions under which homeotherms live and for
all their sizes, this thermal level has been fixed by natural selec-
tion with a very small variation. It is fixed, however, and so is the
basal metabolic rate of homeotherms large and small, tropical and
arctic. It can be predicted with about 10% accuracy by the equation:
♦Rabbit's normal temperature is 39.6 C; its variation is generally not more
than 1.8° C. Robert C. Lee (1939).
243
KLEIBER
1 10
1
1
' /
^■|08
r
/
UJ
a:
Cold adapted^^ — ;
/
^106
-
/^ /
■~
<i
/ /
oc
/ /
^104
-
1^^
-
'S.
Rabbit
-^---"^^^
UJ
/
!lil02
Cow
/
■
h-
O
LXJIOO
-
~
a:
98
Man
1
1
1
40
110
60 80 100
ENVIRONMENTAL TEMPERATURE "F
Schematized from H.D.Johnson etoi, Mo. Res. Bui. 6^ p. 18, 1958
Figure 1. Rectal and environmentaltemperatures of man.cow, and rabbit (cold-
adapted and non-cold-adapted).
244
DOMESTIC MAMMAL ADAPTATIONS
3/4
B = 70 X W
where B = basal metabolic rate per day in kcal
W= body size in kg (Kleiber, 1947)
Scholander (1955) writes as follows:
The non- adaptability of the resting rate shows that the
heat production is notdetermined by the heat loss as one
might infer from the surface law of Rubner (1883) but
vice versa. Whatever the surface area happens to be, the
heat loss from it must be so regulated by various means
that it balances the heat production. In ahomeotherm one
might say that body temperature plays the first violin,
metabolic rate the second, and heat loss the third.
The major, or practically only, adaptation which occurred was
the adjustment of the thermal insulation to bring the third violin
into harmony with the first and second. This adaptation was accom-
plished in various ways, and it led to differences in the temperature
distribution of various animals.
Figure 2, also schematized from the data of Johnson et al.
(1958), shows the skin temperature as a function of the environ-
mental temperature. From 50 F to 90 F (10 C to 32 C) air
temperature the rabbit skin maintains an almost constant tem-
perature, whereas the temperature of the skin of cow and man
follows the environmental temperature.
This temperature distribution is the result of the high insulating
power of the rabbit fur and the fact that man lacks this insulation.
The main resistance against heat loss and therefore the greatest
temperature gradient in naked man is located in the subcutaneous
layer. The cow has a less efficient fur than the rabbit. The difference
between rectal temperature and skin temperature, which is an index
for the resistance of the subcutaneous layers to heat flow, is shown
in Figure 3.
As the environmental temperature rises, the skin temperature
of man and cow approaches the rectal temperature but does not reach
245
KLEIBER
60 80 100
ENVIRONMENTAL TEMPERATURE *F.
Schematized from H.D. Johnson etol, Mo. Res. Bui. £48 18, 1958
Figure 2. Skin and environmental temperatures of man, cow, and rabbit.
246
DOMESTIC MAMMAL ADAPTATIONS
.^J
1 ' 1 ' 1
LU"
\
or
-
xMon
^—
X
<t
\^
LU 0
__
\
\^
Q_
V \^
LU
-
Cow\ \
1—
N^ \
^ 4
—
\ \
:^
^^ \
CO
^^ \
to
_
^^ \^
3
^^ ^y
C
^^ ^k
'^ 2
1
—
\^\
<r
i—
o
LU
a:
0
Rabbit
5 10 20 30 40
ENVIRONMENTAL TEMPERATURE 'C.
Schematized from H.D. Johnson etol, Mo.Res>Bul.648 19 1958
Figure 3. Differences between rectal and skin temperatures in man, cow, and
rabbit at various environmental temperatures.
247
KLEIBEB
o o
it. When the air temperature rises from 30 C to 40 C, the man
and cow maintain an almost constant difference between skin and
body temperature. This is mainly the result of evaporative cooling.
The rabbit, however, lets his skin temperature almost reach the
level of the rectal temperature. Rabbits presumably rely mainly on
the evaporative cooling in the respiratory system (or possibly the
ear surfaces).
Richet (1889) shaved a rabbit and observed that in this condition
the rabbit regulated its body temperature at a lower level. This
effect is shown in Figure 4, drawn from data in Richet' s book on
animal heat.
Diurnal Changes of Body Temperature
Man changes his body temperature during a day in a cyclic
fashion, and Kleitman (1951) suggests that differences in this cycle
account for differences in the behavior of two types of people, the
early risers and the late risers. The late risers are grouchy be-
cause their body temperatures are low. They need to be warmed
up by a cup of hot coffee to reach a friendly disposition and a posi-
tive outlook on life, (See also Kleitman, et al, 1935).
Some domestic animals, such as the donkey and the camel,
start their days with a considerably lower body temperature than
that of man, and they do not have the benefit of a cup of coffee.
They may possibly be endowed with a higher basic level of social
grace than man and donotexpress their grouchy feelings as strong-
ly as some human beings do.
Figure 5 shows the diurnal temperature change of a Holstein
cow subjected to an environment simulating the Imperial VaUey
(Kibler and Brody, 1956). In man, a temperature of 108 F (42 C)
would be regarded as a very high fever and the cow's thermostatic
capability seems therefore not very impressive; yet comparison of
the cow's daily temperature fluctuations with those of the air tem-
perature under actual conditions in the Imperial Valley shows that
temperature changes in the body are a small part of those in the
248
DOMESTIC MAMMAL ADAPTATIONS
0.
UJ
o
UJ
4U.U
.8
V
NORMAL RABBIT _ q
/\
.6
N^
/^-cT \
V
/N
.4
:
V
1
.2
- A
b
p
i'
M
^^ ,'
>
39.0
-
SHAVED RABBIT
^d
\
.8
1
1 1 1 1 1 1
1
»
1 }
2 4 6 8
DAYS KEPT AT I2-I5°C
Figure 4. The effect of shaving on the body temperature of rabbits.
249
KLEIBER
ENVIRONMENTAL TEMPERATURE 'F. (Simulofinq Irrfperiol Volley)
65 60 70 90 100 110 90 80
9 12 15 If
HOUR OF DAY
(From H H, Kiblen and SBrody, Mo. Res. Bui. 601, 10, 19561.
Figure 5. The diurnal change in a cow's body temperature with changes in
environmental temperature.
250
DOMESTIC MAMMAL ADAPTATIONS
environment (Fig. 6). This is especially true in the relatively cool
months of May and June. When it gets extremely hot in July and
August, the fluctuations of body temperature become greater.
One may define the effectiveness of temperature regulation as
the quotient of the change in the environmental temperature and the
changes in the body temperature.
Figure 7 shows this calculation for the cow observed by Ittner
(1946) in the Imperial Valley.
As long as the maximum temperature of the environment stays
below 40 C, the change in the cow's body temperature is only about
one fortieth of the change in the environmental temperature, but when
the maximum temperature of the air reaches 44 G, as in July, the
cow's regulating efficiency drops to one half. Her temperature fluc-
tuation now becomes one twentieth of that of the environment. The
cow is better equipped to maintain her body temperature against a
cold than against a hot environment.
Some breeds of Asiatic cattle are better adapted to hot climates
than Western breeds. The Zebu cattle may thrive under conditions
under which Western cattle suffer. Brody and his coworkers have
investigated this difference and McDowell and his coworkers (1953)
have studied the inheritance of this adaptation. They crossed Jersey
cattle with Sendhi, a breed of Zebus, and exposed Jerseys and cross-
breeds to an environmental temperature of 10 5 F(40 C) for 6
hours. Figure 8 shows some of their results. The crossbreeds main-
tain a body temperature close to 102° F (39 C), whereas^the body
temperature of the Jersey cows rises to over 103 F (39 C). The
reaction of the Jerseys depends on the season. During the winter
months they are least able to cope with a 6 hour exposure to 10 5 F
(40° C), whereas during the summer months this exposure raises
their body temperatures to a level not much higher than that of the
crossbreeds.
251
KLEIBEP
45
40
35
.r30
25
20
15
10
I
i
^
Environmental
Max.
Min.
Cow's rectal
Max.
^XM Min.
MAY JUNE JULY AUG.
(Observations by Ittner, Imperial Valley, California, 1946)
Figure 6. Daily fluctuations of a cow's body temperature compared with those
of the environmental temperature.
252
DOMESTIC MAMMAL ADAPTATIONS
Month
Environment
Cow
(rect.)
Effectiveness
A Envir.
A Rect.
Min.
Max.
"C.
A Envir.
"C.
A Rect.
MAY
14
2-9
15
0,4
38
JUNE
23
40
17
0.4
42
JULY
27
44
17
0.9
19
AUGUST
28
42
14
0.9
16
Note: Total variation of rectal temperature 38.2 to 40 "C.
Based on observotirns by Ittner, Imperial Valley, Calif., 1946.
Figure 7. Daily temperature fluctuations and the effectiveness of a cow's
thermostat.
253
KLEIBER
(mean of G HI^S. at 105*F. Eb 34mrn H^ V. P. )
JERSEY HEIFEi^S JERSEY DR^Y COWS
SINDHI-JEf^SEY HE1FEK.5 SlNDHl-JEI^SEY Df^Y COWS
' 104
O
o
DC
zi03
UJ
_)
<
101
/y\
\
i /
1 /
-^
=r=
1 i ^
^- ; ^1
1
^' '
i 1 ^
1
1 1
i
1
j !
■ — ^ — ' — '■ 1 1 ;
1 1 I ! 1
JFMAMJJASOMD
MONTH
Journal of Animal Science, Vol. 12, No. 4, November, 1953
Figure 8. Seasonal effects on body temperature response to heat.
254
DOMESTIC MAMMAL ADAPTATIONS
REGULATION AGAINST COOLING
By cooling I mean a decrease in temperature and, to the best
of my knowledge, that is what Newton meant by cooling when he
formulated his law of cooling which is erroneously applied when one
means loss of heat rather than of temperature. Temperature reg-
ulation means prevention of cooling but not prevention of heat loss.
The classic example for adaptation to cold has been given by
Hoesslin (1888). He set out to test experimentally Rubner's theory
that the metabolic rate of homeo therms is proportional to their sur-
face area because their heat loss is proportional to their surface
area. Hoesslin argued if the metabolic rate is governed by the heat
requirement, then it should be directly proportional to the difference
between environmental temperature and body temperature. To test
this deduction, Hoesslin raised one dog at 32 C and a twin brother
o
of that dog in the refrigerator at 5 C. From his records of food
consumption and his estimate of body substance produced, Hoesslin
concluded that the dog raised at 5 C had a metabolic rate only 12%
above that of his brother raised at 32 C, The difference between
body temperature and environmental temperature of the cold dog was
about six times as great as the corresponding difference for the hot
dog.
Hoesslin concluded that heat requirement could not be the deter-
mining factor in the control of metabolic rate or the explanation for
the surface law. He observed that the cold dog's pelt weighed 3.6
times as much as that of the hot dog, indicating an adaptation of in-
sulation to environment. It may be that the adaptation was mainly on
the side of the hot dog, that his fur was abnormally light. We now
would accept Hoesslin's argument that the metabolic rate of his hot
dog was not determined by heat requirement, but we would maintain
that the metabolic rate of the cold dog presumably reflected a ther-
mostatic heat requirement. This assumption is justified by the rela-
tion of metabolic rates to body temperatures of various animals
255
KLEIBEP
obviously reflecting the insulating power of their body covering as
shown in Figure 9.
We simplify the situation by the scheme in Figure 10 . If the
dogs behaved strictly like ordinary thermostats, then the metabolic
rate of the hot dog would be on the line between the rate of the hot
dog and the rate zero reached when the environmental temperature
becomes equal to the body temperature. On the scale of our figure
the hot dog would produce about 16% of the "normal" rate marked
100. The hot dog, however, produces almost as much heat as his
cold brother and operates special devices to get rid of the excess
heat. Obviously, the metabolic rate of the hot dog cannot be explained
as a heat requirement. Rubner realized that, and he explained the
surface law of animal metabolism as heat requirement proportional
to surface area in a cold environment and as necessary cooling
power also proportional to surface area in a hot environment.
There is, however, a difference between the two dogs in their
immediate reaction to cold. If the hot dog were suddenly brought to
the cold living quarters of his brother, he would presumably shiver
and produce more heat than the cold-adapted litter mate. If he stayed
long enough in the wintery climate and if he had enough youthful
adaptability he would gradually grow a fur as thick as that of his
brother and quit shivering; then presumably the two dogs would have
the same metabolic rates. The rise in metabolic rate is known as
"chemical," or metabolic temperature regulation. By that term,
Rubner simply meant an increase in the rate of chemical processes,
whether or not connected with muscular movement such as shivering.
The idea of chemical temperature regulation as contrasted to reg-
ulation involving shivering is a later and not too useful complication.
The change in the insulation, in contrast to the change in metabolic
rate, is known as "physical" temperature regulation, and, if it in-
volves slow processes such aschangingone'sfur,it is classified as
"acclimatization."
Scholander reports that dogs truly acclimatized to the arctic
regions have a critical temperature as low as -40 C. This shows
that domestication has not led to a degeneration of the dog or at
least has left the dog the possibility of overcoming the softening
256
DOMESTIC MAMMAL ADAPTATIONS
0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 54 36 38 40 42
ENVIRONMENTAL TEMPERATURE "C.
Figure 9. Fasting katabolism in the hairless mouse, the rat, the dog, and the
rabbit at various environmental temperatures.
257
KLEIBER
2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40
Tc Tb
ENVIRONMENTAL TEMPERATURE
Figure 10. The rates of heat production in Hoesslin's "hot" and "cold" dogs at
various environmental temperatures.
258
DOMESTIC MAMMAL ADAPTATIONS
effect of civilization and becoming fit to follow "the call of the
wild," as Jack London would say.
Between the immediate response of shivering and the long
term acclimatization of growing a thicker fur, there is an intermed-
iary adaptation. For some time the dog brought from the hot to the
cold environment would presumably respond with "insulative cool-
ing." He would let the temperature, especially of the outer layers
of his body, drop. Scholander (1958) discovered this temporary an-
swer to cold exposure in the Australian aborigines. This adapt-
ation is especially advantageous in climates with great diurnal tem-
perature changes.
I remember Nansen's account of his polar expedition, especially
his description of Johansen's sleeping peacefully with his bare foot
stuck out from the tent into the subzero polar air. This observation
indicates that the Norwegian polar explorers may also have ac-
quired some ability to utilize insulative cooling.
Social Temperature Regulation
My account of adaptations to prevent a fall of body temperature
in a cold environment would not be complete without mentioning
social temperature regulation. Animals have learned to conserve
heat by "togetherness," also called "huddling." That this method is
effective has been shown in baby chicks, some of which were denied
fulfillment of their social instinct and were forced to burn up more
fuel to keep warm, while involimtarily practicing rugged individ-
ualism (Fig. 11).
REGULATION AGAINST OVERHEATING
An old method to get relief from too much heat is the use of a
fan. I am told that ladies used this instrument not only to increase
259
KLEIBER
200
80 -
CHICKS SEPARATED
10 15 20 25 30 35 40
ENVIRONMENTAL TEMPERATURE *C
(Proceed. Soc Exp Biol. Med ii, 158, 1933)
Figure 11. Social temperature regulation in chicks 20 days old.
260
DOMESTIC MAMMAL ADAPTATIONS
cooling but also to hide blushing and even to hide non-blushing.
Steers do not worry about blushing but they get relief against
overheating from fans, as shown on Figure 12, which was con-
structed from a table giving observations by Ittner, Bond, and
Kelly (1955), in the Imperial Valley of California. The fan could
keep the body temperature one degree lower than it would have
been without the fan. This type of relief, of course, is given the
animal by his keeper. The animal itself, however, also has methods
for preventing overheating. The first reaction of an animal ex-
posed to a high environmental temperature is to increase the
blood flow to the skin, which increases the heat flux from skin
to environment. This type of physical temperature regulation
is effective only when the skin temperature is higher than the
environmental temperature. When the air temperature and the
temperature of the objects toward which an animal radiates
are equal to, or higher than body temperature, more drastic
means of cooling have to be taken. The last resort is water
evaporation. Men and horses perspire. Dogs and cattle have
discovered a flaw in this method. When the surface is wet and
evaporative cooling takes place, there is not only the welcome
temperature difference for the flux of heat from the interior to
the surface , but also an increase in the flux from the hot environ-
ment to the animal surface. The animal therefore spends water
to cool its environment. To overcome that disadvantage, cattle
and dogs operate an internal evaporative cooler which leaves
the surface temperature higher and keeps the heat influx lower.
Dogs and cattle increase the evaporative cooling by panting.
Increased respiratory ventilation, however, involves the danger
of depleting the blood of CO , a condition known as acapnia which
causes unpleasant disturbances in the operation of the breathing
reflexes. The answer to this danger is shallow breathing, in-
creasing the ventilation rate in the upper parts of the respira-
tory system only, this provides the desirable increase in evapora-
tion, with little change of the CO washout from the alveoli.
Figure 13 shows the type of breathing in heat exposed cows
compared with that at a low (for the cow's taste comfortable)
temperature. A threefold increase in respiratory frequency pro-
duces a twofold increase in ventilation rate because the volume
for each breath is reduced. Cows do not start panting at a certain
261
KLEIBER
106
105
104
Q
O
CD
103
August 1 1, 1955 Imperial Valley -Air temp, at 2pm; 103 °F.
— I 1 1 1 1
WITHOUT FAN
10 II 12 13
TIME OF DAY
AIR TEMP.
— ^
14 15
Figure 12. The effect of a fan on a steer's body temperature.
262
DOMESTIC MAMMAL ADAPTATIONS
Environmental
7°C.
Temperature
32°C.
Breaths per minute
Respired air per minute, liters
Respired air per breath, liters
15.51 a 3
52 ± 3
3.4+0.2
46.013.8
05 ± 5
2.210.04
(Proceed. Soc. Exp. Biol. Med. 35,10-14, 1935).
Figure 13. Physical temperature regulation incows. The adaptation of breathing
at various environmental temperatures.
263
KLEIBEF
environmental temperature. As they get warmer, their breath rate
increases rather gradually, so that the relation between respiratory
frequency and the environmental temperature can well be expressed
by the Arrhenius equation.
Figure 14 shows the logarithm of respiratory frequency plotted
against the reciprocal of the environmental temperatiire in degrees
Kelvin.
The idea that cows do not perspire at all through their body
surface has been proven erroneous. Figure 15 summarizes the
results of Kibler and Brody (1952), which indicate that indeed
a great part of the heat given off by cows, especially in a hot
environment, is accounted for by surface evaporation, and the
evaporation in the respiratory system amounts to only one-
third of the total evaporation.
Kibler and Yeck (1959) later observed that the greater heat
tolerance of Brahman cattle compared with shorthorns is related
to a greater evaporative capacity and that in particular the ratio
of skin evaporation to respiratory evaporation is greater in the
heat tolerant Brahmans. The major advantage of the Brahmans,
however, in combating overheating, according to Kibler and
Brody (1954), is their relatively low metabolic rate, about 80
kcal/(m X hr) as compared with 150 kcal/(m x hr) in Jerseys
and Holsteins.
The Method of the Camel
The most ingenious system of keeping cool has been develop-
ed by the camel, also known as the ship of the desert. The U. S.
Navy has a perfectly good reason, therefore, for supporting re-
search on this animal by Knut and Bodil Schmidt- Nielsen, a
team of extraordinarily keen observers.
The camel apparently realizes the advantage of inside cooling as
opposed to surface cooling. It also is very much interested in the
most economic useof water and can hardly afford to have sweat drop
to the ground un evaporated, as it does in human athletes and in
264
DOMESTIC MAMMAL ADAPTATIONS
2.0
1.9
1.8
1.7
1.6
1.5
1.4
1.3
1.2
3.2
o
\
-o
Log./ = 10.549-2630 x 4^ _
<
>
m
nn ^ : \ I I^OK PflfiO* *
^v
1
X
^•■,
^1
\;
•
o
• ()
•
3.3
3.4
3.5
3.6
RECIPROCAL OF ENVIRONMENTAL TEMR °K,=t=xlO^
39°C
5°C
Proc. Soc. Exp. Biol. Med. ii : 1 1 (1935)
Figure 14. The Arrhenius equation for cow's respiratory frequency.
265
KLEIBEP
2o 4o 60
CHAMBER TEMPERATURE
Kibler a Brody
Mo. Research Bulletin 497 (1952)
Figure 15. Percentage of metabolic heat dissipated by surface vaporization.
266
DOMESTIC MAMMAL ADAPT ATIOI^
horses. Yet the camel apparently does notthink much of panting and,
having observed panting cows and dogs, I cannot blame the camel for
disliking that method. The ship of the desert solves the problem by
making the skin surface an inside surface insulated by an effective
fur. This leaves the outer surface of the hair hot and dry, minimiz-
ing the heat influx from the environment and reserves the entire
cooling effect of the evaporation for the benefit of the animal.
The Schmidt- Nielsens and theircoworkers (1957) demonstrated
the importance of the fur in water economy by clipping a camel's
hair. The result is shown in Figure 16 which is redrawn from Figure
1 inSchmidt-Nielsen's paper. Under given conditions, the furry cam-
el uses 2 liters of water per day per 100 kg body weight. Clipping of
the hair increases the water loss to 3.7 liters daily per 100 kg body
weight. *
Schmidt- Nielsen et al. also measured the water expenditure of
a donkey (presumably under the same conditions as the camel) , and
they state that the donkey wastes more water even than the clipped
camel. As a good Democrat I am bothered by this wastefulness of the
donkey and I think the accusation is unjustified. For a fair compari-
son ofwastefulness, the rates of evaporation should be expressed per
unit surface area instead of body weight, and when rates are ex-
pressed that way, the donkey is just as economical in the use of
water as the clipped camel. To demonstrate the fallacy of the com-
parison per unit body weight for this discussion, I have added the
probable rate of water loss of a 4000 kg elephant, and the result
shows that by Schmidt- Nielsen's comparison the elephant is much
more economical with water than even the furry camel. I must warn
my Republican colleagues not to get too excited about this result. It
is just a matter of body size, and the fact that elephants are bulkier
than donkeys has no political significance. I hasten to mention that
in fact my calculation is based on the strictly bipartisan assumption
that the evaporation rate per unit surf ace area is the same for don-
key and elephant.
Figure 17 shows the calculations which show the same
water loss for the camel and the donkey per unit surface area.
*Some water may be used for the excretion of metabolic products in urine, but
under the circumstances, evaporation presumably accounts for most of the water
used.
267
KLEIBEF
-o c _
O
O
H
~ T ~
7
a>
cu
a, e
6
o o
1 i
5
—
—
c:
o
CZl
4
—
£-_
~
-a
a>
>•
3
1
Water so
3
2
J
o.
>-<
ID
_\_
Elephant wastes less
water ttian a turry
1
-
<t
>-
<x
T
camei
_J
—1
UJ
LlJ
UJ
:^
n
S
S
z:
UJ
«=r
<r
o
1
n
(j>
C_3
Q
UJ
Data on camel and donkey from Sctimidt-Nielsen et al
Amer. J. Ptiysiol. 188 P 110. 1957. Elephant calculoted
with equal evaporation rate per m2 surface area as donkey
Figure 16. The effect of clipping and of body size on rate of water evaporation
per unit body weight in camel, donkey, and elephant.
268
DOMESTIC MAMMAL ADAPTATIONS
Camel | Donkey
Body weight 206 Kg_ j_8l Kg
Surface orea Wi'l 34.9 Kg^^^^J8.7 Kg^'^
Daily water used per 100 Kg (scnmidt-Nieisen i957*) 3.5 lit. _|__7.3 lit.
/• - onimal 7.2 "__|--5.9 '•
Kg^'' 0.206l| -0.206"
'Kg''* 0.133^-^-0.218"
*Amer. J. Physiol. 188, pgllO Fiq.7, 1957
Figure 17. Rate of water evaporation in the camel and the donkey.
269
KLEIBEB
The water loss per interspecific unit of body size is kg 3/4
(Kleiber, 1947). This interspecific unit is a unit of probable
metabolic rate and it shows thatthe donkey had a higher rate of wa-
ter loss than the clipped camel.
The comparison of rate of water loss between donkey and camel
leads not to one but to several different conclusions, and no one is
absolutely superior to the others. Assuming isometric composition
of the two animals, the conclusionbased on loss per unit body weight
indicates that the donkey loses a given percentage of its body water
twice as fast as the camel. For an estimate of the daily water re-
quirement of a caravan, it maybe of interest to know the water loss
per animal — 7.2 liters per camel, 5.9 liters per donkey. For a com-
parison of mechanisms of heattransfer it is noteworthy to know that
both camel and donkey lose daily 2.1 liters HO per m of surface
area. For comparisons of the rates of water loss with metabolic
rates, the loss per interspecific unit of metabolic body size is the
most useful.
Daily Heat Load and Body Size
In many regions, especially deserts, it is very hot during a
period of the day and cold during the night. Under those circum-
stances the larger animal has an advantage over the smaller one be-
cause heat load is proportional to body surface and heat capacity
proportional tobody weight. The rise in body temperature for a given
period of excessivetemperatureduringtheday is therefore inverse-
ly proportional to the cuberootof body weight. Figure 18 illustrates
this relation.
It is assumed that during a 6 hour period every day the influx of
heat exceeds the animal rate of heat loss so that during this 6 hour
hot period 2.5 kcal of heat are stored in the animal per dm of its
body surface. This would be a rate of influx of 250 kcal per m in 6
hours and would equal the basal metabolic rate which, according to
Rubner, is 1000 kcal per day per m .* What is the rise in body tem-
perature at the end of the 6 hour period resulting from this storage?
♦This is approximately correct for an animal of 100 kg body weight, whereas
smaller animals produce less, larger ones more heat per m per day.
270
DOMESTIC MAMMAL ADAPTATIONS
Surface
Cliange
Body Weight
Heat cop.
in Body Temp.
W
-- 12.5 X W-3
.o c Surfoce
" Heotcop.
Kg.
dm*
kcal / 'C.
•c.
1
12.5
31.4
10
5.81
14.5
00
2.70
6.7
1000
1.25
3.1
10000
0.58
1.4
Figure 18. Periodic heat }pad, body size, and body temperature for a periodic
heat storage of 2.5 kcal per dm . For a 6-hour period the pte of this storage would
be equal to the daily metabolic rate of one megacal per m (Rubner).
271
KLEIBEB
The,surface area in square decimeters may be estimated to be 10 x
W , where Wis the body weight in kg. The heat capacity of the ani-
mal may be estimated as kg water xO.4 x kg dry matter in the ani-
mal (Kleiber, 1961). Assuming a water content of 68%, the heat
capacity of the animal would therefore amount to 0.81 kcal/ C per
kg body weight. The ratio of surf ace a re a to heat capacity then would
amount to
2/3 .
or 12.5 W (second column in Figure 18)
0.81W ^ ^ '
' 2
The increase in body temperature from the storage of 2.5 kcal/dm
then amounts to 2.5 x 12.5 W~ . This rise would be 31.4 C for
an animal weighting 1 kg and 1.4 C for a 10 ton super elephant.
A large animal, therefore, may comfortably survive discontinuous
daily heat loads which are fatal for smaller animals. When, how-
ever, the heat load is continued, the advantage of size is lost.
Professor Regan at Davis noted that a cow can stand a good
deal of heat during the day when she cools off during the night,
whereas a constant rather moderately high temperature in an
air conditioned room may be fatal.
The camel can take advantage of cool nights by letting its
body temperature decrease to 34 C (see Schmidt- Nielsen). A
human being could hardly stand this, nor could he let his body
temperature rise to 41 C when water is short and the day hot.
Schmidt- Nielsen feels that this relatively large change in
body temperature should not be regarded as a failure regulation,
but rather as an adaptation which conserves water. It may be
more cautious to say that in this case the water economy at the
cost of an accurate temperature regulation proves advantageous
for survival.
The difference between controlled and run away increase
in body temperature, the latter resulting from positive feedback,
is clearly shown in a plot of pigs' body temperature against time
of exposure to various environmental temperatures, observed by
Robinson and Lee (1942).
272
DOMESTIC MAMMAL ADAPTATIONS
FROM:
4 5
EXPOSURE
ROOM TEMP IS SHOWN WITHIN THE GRAPH
K.ROBINSON AND D. H.K. LEE
PROC. ROY. SOC. QUEENSLAND 53 (9) 145 (1942)
Figure 19.
o o
A pig s body temperature in 75 F to 110 F air.
273
KLEIBEB
TEMPERATURE AND FOOD UTILIZATION
An animal that is producing flesh or other forms of animal
product invariably has a higl^er metabolic rate than a non-produc-
ing and especially a fasting animal would have. The difference in
heat production between the fed and the fasting animal is called
the "heat increment", or the calorigenic effect of food, or the
specific dynamic effect of food, an intriguing name considering
the fact that the effect is neither specific nor dynamic.
This calorigenic effect of food intake means a relief to the
animal in its fight against a cold environment and an extra burden
in the regulation against overheating.
The situation is illustrated in Figure 20. At a low environ-
mental temperature the metabolic rate, being determined by the heat
requirement, will be the same for fed and fasting animals. There is
thus no calorigenic effect of the food. At this low environmental tem-
perature the extra heat for thermostatic control is now less because
the minimum heat production of the fed animal is higher than that of
the fasting animal.and the calorigenic effect of the food helps to heat
the animal. The critical temperature of the fed animal (Tcf) for
that reason is lower than that of the fasting animal (Too). Between
these two temperatures the calorigenic effect of the food in-
creases from zero to C in proportion to the increase in environ-
mental temperature. Rubner called the description of this effect
his compensation theory. The calorigenic effect compensates for
the thermostatic rise in heat production of the fasting animal.
Above the critical temperature of the fasting animal, the
calorigenic effect of the food is independent of changes in environ-
mental temperature. The excess heat of the fed animal is greater
than that of the fasting animal. This means an extra burden in
the fight against overheating. If this burden becomes significant,
it affects the food intake. At a sufficiently high environmental
274
DOMESTIC MAMMAL ADAPTATIONS
uoipnpojd |D8H P ^\0U
00
0)
u
a
0)
^
o
bC
275
KLEIBEP
temperature , the animal may eat only enough for maintenance,
as illustrated in Figure 21 (Kleiber and Dougherty, 1934).
This temperature (T max) is the highest environmental
temperature for animal production. As the environmental tempera-
ture is decreased, the animal will eat more, and the net energy,
appearing in the animal product, N, will rise. Below the critical
temperature of the full fed animal, Tc , the heat production will
be determined by the thermostatic heat requirement. Since the
capacity for food intake is limited, whereas the heat requirement
continues to increase with decreasing environmental temperature,
less and less energy is available for production, and at the tempera-
ture, T . , the maximum food intake of the animal provides just
enough heat for maintaining the animal's body temperature. Below
this temperature the animal will eat all it can and yet starve to
death because it will have to burn up its own body substance in
addition to all the food it can eat in order to maintain its body
temperature. This situation may be less significant for practical
purposes than the lack of food in a cold environment which calls
for human action such as operation "Hay Lift". Between the low
temperature, at which the animal eats a lot but needs most of
the food for fuel for keeping warm, and a high temperature at
which it loses appetite to such an extent that it burns up all it
takes in for maintenance, there should be an optimal environ-
mental temperature at which the efficiency of animal production
is at a maximum. This is illustrated on the lower part of Figure 21.
An indication, though not too obvious, of such a temperature
optimum has been obtained in respiration trials with lactating
cows fed to capacity with alfalfa hay, beet pulp, and grain, and
kept alternately for weekly periods at 7 C, 18 C, and 30 C
(Kleiber, 1961). Total carbon and nitrogen balance was determined
over a three day period during each week.
The results are shown in Figure 22. The decline in food
intake at a high environmental temperature is most conspicuous.
The milk production was little affected, but the loss of body sub-
stance was greater at the low and at the high temperature, than
at 18 C where the net energy was at a maximum.
276
DOMESTIC MAMMAL ADAPTATIONS
Energy
Jntake
T min.
TC3 Tc2 Tc
Environmental temperature
T max.
J. Gen. Physiol. 17: 703 (193^^
Figure 21. Scheme of influence of environmentaltemperature on food utilization.
277
KLEIBER
10' 15' 20' 25'
Environmental temperature
30" c.
Figure 22. Food utilization of dairy cows at various environmental temperatures.
278
DOMESTIC MAMMAL ADAPTATIONS
Figure 23 shows a hydraulic model as an analog of animal
energy utilization in which the effect of cooling power is coordinated
with other effects such as stimulus for milk production and for
growth on the regulation of food intake. This was an early sugges-
tion (Kleiber, 1936) of the two great regulators of food intake, a
chemostatic principle now worked out especially convincingly by
J. Mayer (1953) and the thermostatic principle represented es-
pecially by Strominger and Brobeck (1953).
ENERGY IN:
0~®
.regulator of appetite
lAting capacity
ABSORPTION capacity
storage capacity
heat
f ^f/^'\ S ) n stimulus FOR GROWTH
*— MILK ENERGY
STIMULUS FOR MILK PRODUCTION
FASTING KATABOLISM REGULATOR
Figure 23. Scheme of energy- utilization.
279
KLEIBEE
SUMMARY
Domestication has not essentially changed the basic responses
of animals to challenges from cold or hot environments.
A reaction to cold exposure, common to man and other homeo-
therms, is an increase in metabolic rate called chemical tempera-
ture regulation. A more economical response, known as insulative
cooling, has been lost by civilized man, but operates in domestic
animals and ^^ustralian aborigines.
In order to adapt to continued cold exposure, animals increase
their insulation mainly by growing a thicker fur. Man has replaced
this adaptation by technical control of the microclimate.
Overheating is prevented mainly by evaporative cooling at the
body surface or in the respiratory system. Contrary to older be-
lief, cattle evaporate more water from the skin than by respira-
tion, even though respiratory frequency increases consistently
with increase in environmental temperature.
Evaporation from a wet body surface in a hot environment
is uneconomical because it allows an influx of heat from the
environment to the surface.
The camel's fur maintains its outer surface dry and hot,
minimizing the influx of heat to the skin which is kept cool by
evaporation. Clipping of the fur increases the camel's water
loss in a hot environment to a rate per unit area similar to
that of a donkey.
Excessive but time- limited daily heat loads producing heat
storage in the body can be endured better the larger the animal
because heat load is proportional to body surface area and heat
capacity is proportional to body weight. Increase in body tempera-
ture for given loads, therefore, is proportional to the reciprocal
of the cube root of body weight.
280
DOMESTIC MAMMAL ADAPTATIONS
Animal production increases metabolic rate and consequently
the problem of overheating. The breeds of cattle which are best
adapted to endure hot climates are usually low producers with
relatively low rates of heat production.
281
KLEIBER
LITERATURE CITED
1. Hoesslin, H. V. 1888. Ueber dieursachederscheinbscheinbaren
Abhangigkeit des Umsatzes von der Grosse der Korperober-
flache. Arch. Physiol. 11:323-379.
2. Ittner, N. R. 1946. A progress report on livestock investigations
in the Imperial Valley. College of Agr., Univ. of Calif., Davis.
Table 1, p. 3.
3. Ittner, N. R., T. E. Bond, and C. F. Kelly. 1955. Methods of in-
creasing beef production in hot climates. Cal. Exp. Sta. Bui.
761, Table 13.
4. Johnson, H. D., C. S. Cheng, and A. C. Ragsdale,1958. Compari-
son of the effect of environmental temperature on rabbits and
cattle. Missouri Res. Bui. 648:1-27.
5. Kibler, H. H. and S. Brody.1952. Relative efficiency of surface
evaporative, respiratory evaporative, and non- evaporative
cooling in relation to heat production in Jersey, Holstein,
Brown Swiss and Brahman cattle, 5 to 105 F. Missouri
Res. Bui. 497:19.
6. Kibler, H. H. 1954. Influence of radiation intensity on evapora-
tive cooling, heat production and cardiorespiratory activities
in Jersey, Holstein and Brahman cows. Missouri Res. Bui.
574:20.
7. Kibler, H. H. and S. Brody.1956. Influence of diurnal tempera-
ture cycles on heat production and cardio- respiratory
activities in Holstein and Jersey cows. Missouri Res. Bui.
601:10.
8. Kibler, H. H. and R. G. Yeck.1959. Vaporization rates and heat
tolerance in growing Shorthorn, Brahman, and Santa Ger-
trudis calves raised at constant 50 and 80 F temperatures.
Missouri Res. Bui. 701.
282
DOMESTIC MAMMAL ADAPTATIONS
9. KLeiber, M. 1947. Body size and metabolic rate. Physiol.
Rev. 27:538.
10 - Kleiber, M. 1936. Problems involved in breedingfor efficiency
of food utilization. Am. Soc. Animal Prod. Proc. p. 247-258.
11. Kleiber, M. 1961. The Fire of Life, and introduction to animal
energetics. Wiley and Sons, New York, p. 102.
12. Kleiber, M. and J. E . Dougherty. 1934. The influence of environ-
mental temperature on the utilization of food energy in baby
chicks. J. Gen. Physiol. 17:701-726.
13. Kleitman, N. 1951. When your temperature goes up. San
Francisco Chronicle "This Week", March, p. 18-19.
14. Kleitman, N. , S. Titelbaum and P. Feievson. 1935. Diurnal
variation in reaction time and its relation to body tempera-
ture. Am. J. Physiol. 113:82.
15. Lee, R. C. 1939. The rectal temperature of the normal rabbit.
Am. J. Physiol. 125:521-529.
16. McDowell, R, E., C. A. Matthews, D. H. K. Lee and M. H.
Fohrman. 1953. Repeatability of an experimental heat
tolerance test and the influence of season. J. Animal Sci.
12:757-776.
17. Mayer, J. 1953. Genetic, traumatic and environmental factors
in the etiology of obesity. Physiol. Rev. 33:472-508.
18. Richet, Gh. 1889. La Chaleur Animale. Felix Alcan, Paris,
p. 23.
19. Robinson, K. W. and D. H. K. Lee. 1942. Reaction of the
Pig to Hot Atmospheres, Proc. Roy. Soc. Queensland
53:145-158.
283
KLEIBER
20. Schmidt- Nielsen, K., B. Schmidt- Nielsen, S. A. Jarnum and
T. R. Houpt. 1957. Body temperature of the camel and its
relation to water economy. Am. J. Physiol. 188:103-122.
21. Scholander, P. F. 1955. Evolution of climatic adaptation
in homeotherms. Evolution 9:15-20.
22. Scholander, P. F. 1958. Studies on man exposed to cold.
Fed. Proc. 17:1054-1057.
23. Strominger, J. L. and J. R. Brobeck. 1953. A mechanism
of regulation of food intake. Yale J. Biol. Med. 25:383.
284
DOMESTIC MAMMAL ADAPTATIONS
DISCUSSION
EAGAN; There are three minor points I should like to make.
First, Figure 1 showed that the rectal temperature of the rabbit
decreased in response to a moderate decrease in environmental
temperature. I know that this has been shown by some people, for
instance by Carlson (1955) * but we have not seen this — not even in
rabbits that were exposed to -25 C. There is no change in rectal
temperature in mature animals exposed at-25 Cfor several hours
(Eagan, 1961).**
Secondly, Burton presented a theory on why the body tempera-
ture is regulated at about 37 G. This theory is presented in the
first chapter of Man in a Gold Environment (Burton and Edholm,
1955)*** to support the suggestion that the level of body tempera-
ture adopted by the hoineotherms has something to do with the
stability of temperature regulation. It is a matter of choosing a
temperature which favors economy in physiological function over
the widest range of environments.
KLEIBER: What is that theory?
EAGAN: I would refer the listeners to the original work cited
above. Briefly, the regulated body temperature is that one from
which a deviation will cause the change in heat production (Arrhen-
ius' law) to be balanced by the change in heat loss (Newton's law
of cooling), at the 25 C annual isotherm where homeothermic ani-
mals are believed to have originated.
*Carlson, L. D. 1955. Interrelationship of circulatory and metabolic factors,
pp 13-51 in Ferrer, M. Irene, Ed., Cold injury (Trans. Third Conf.). Josiah Macy,
Jr. Foundation, New York.
**Eagan, C. J. 1961. Reactive error in the measurement of rectal temperature
in the cold. AAL TN 59-20, USAF Arctic Aeromed. Lab., APO 731, Seattle, Wash.
***Burton, A. C. and O. G. Edholm. 1955. Man in a cold environment. Edward
Arnold (Publishers) Ltd., London.
285
KLEIBER
The thii-d point is that heat loss in the rabbit exposed to high
temperatures is certainly accomplished through panting. Ididsome
experiments wherein rabbits were exposed at 50 C (Eagan, 1961).*
In spite of vigorous panting by each animal, rectal temperature
rose steadily (after a transient slight decrease) and ear tempera-
ture ran between 1 C and 2 C higher than rectal temperature.
FOLK: Is there a histological difference in the skin of the
Brahman cattle and the American domestic breeds? Are there
sweat glands in any of the cattle?
KLEIBER: Apparently the histologists agree that there are
sweat glands in both breeds.
WEST: I was interested in the caloric intake of the cows; you
have quite a nice curve of caloric intake as temperature falls. Is
this something that they just do without any forcing or do they just
eat this much so they can produce milk or something?
KLEIBER: This was a theoretical, not an empirical curve. I
was attempting to figure out what we have to look for.
WEST: I see, because I was wondering how you were able to
get cows to do this. We are trying to do this with birds.
KLEIBER: It was just an arbitrary expression, thatthere must
be some limit where the temperature is too high for food intake,
and there must be some low temperature limit where the food intake
must be increased. I drew a curve against these two limits.
WEST: In other words, you think of it as a curve, not as a
straight line more or less paralleling the resting metabolism or
heat requirement?
KLEIBER; Well, it could be a straight line, perhaps, but I do
not see how.
*Eagan, C. J. 1961. Topical adaptation to cold in the rabbit ear. Fed. Proc.
20, No. 1, Part 1:210.
286
DOMESTIC MAMMAL ADAPTATIONS
WEST: It seems as though it were the same as maximal activity.
KLEIBER: The only reason I am not particularly happy with the
straight line is that usually these things do not stop all at once.
WEST; I was thinking of the work that Dr. Jansky showed, where
all the maximal rates were nearly parallel; this would be a similar
situation.
KLEIBER: It may be that within a certain range it might be
parallel with the other curve for resting metabolism, and then
smooth out.
JO HANSEN; I found it very peculiar that you could apply
"Arrhenius" so beautifully on the breathing rate of your cows. This
is very much different from what I found in the armadillo. They
increase their breathing rate suddenly; some marsupials do, too.
PROSSER: I would also question that Arrhenius plot, because
you are plotting the breathing rate against external temperature.
What does this mean-?One would think if you are going to extrapolate
to a chemically determined rhythm, you should do this against body
temperature instead of environmental temperature.
KLEIBER: Well, the body temperature remains essentially con-
stant; that is, within a small range.
PROSSER: In that case I am wondering what is the meaning of
the Arrhenius coefficient.
KLEIBER: Here you embarrass me, because the meaning is
completely unknown to me. It just happens to be so and the only
thing which I can deduce is that the breathing rate of the cow is not
the same function of environmental temperature as that of the
armadillo.
HANNON; This brings up a question that we have wondered
about for a long time. That is, why do small animals lose weight
when you first put them in the cold? Is it due to a lack of appetite,
287
KLEIBEB
to a lack of capacity in their G. I. tract for the extra food that is
needed, or is it due to some other factor? I would like to hear
Dr. Hart's opinion on this eventually, but from the data that Dr.
Vaughan and I have accumulated withdietsof a high caloric density,
it would seem that the capacity of the G. I. tract is not the limiting
factor. You can give them plenty of calories but they will still not
eat enough to gain weight at the same rate as their controls. Even-
tually, however, they will be able to increase their food consump-
tion, so that they can gain weight. It has been my feeling that the
reason it takes a while for the cold- exposed animal to acquire the
capacity to utilize more food and thus to gain weight is that he is
not initially able to metabolize food material at a fast enough rate
to supply all of his energy needs. Until he builds up an enzyme capa-
city to do this, his growth is going to lag behind the control animal.
HART: 1 would be very surprised if you could, by overfeeding
an animal, increase its capacity to oxidize the material. In other
words, the appetite would be regulated by internal mechanisms
adjusted to the oxidative capacity of the animals and by pushing food
in you are not going to change this.
HANNON: In our studies we compared the food consumption and
growth of rats that were maintained on a high carbohydrate diet
with rats that were maintained on a high fat diet. It was found that
the group subsisting on carbohydrate consumed much greater bulk
of food but the same number of calories as the group subsisting on
fat.
Apparently their ability to utilize the calories was the limiting
factor, not the ability to get calories into the digestive system.
HART; Did the carbohydrate or the fat diet have any particular
advantage?
HANNON; Not as far as we could see.
KLEIBER: Yes, I think the limiting capacity is not the capacity
of the volume. Adolph showed this when he diluted diets with clay
and other kinds of inert matter. His rats took in and digested as
288
DOMESTIC MAMMAL ADAPTATIONS
much energy with the bulky diet as with the other. This is in line
with Jean Mayer's* idea of the regulation of the food intake, which
is a hemostatic principle. It may have been slightly premature to
suggest in my scheme of 1926** that these two regulators of food
intake, namely the hemostatic principle (which is affected by con-
centrations of material in the blood stream) and the thermostatic
principle, proposed by Brobeck according to which food intake is
affected by the possibility of getting rid of heat.***
EAGAN; Limitation in oxidative capacity is not the only factor,
for in rabbits which are moved to a cold (5 C) environment, food
intake will oftenbeless than normal for the first week or so, where-
as a 50% to 100% increase would be required if body weight were to
be maintained. It can hardly be thought that oxidative capacity is
reduced when the animal is moved into the cold. An explanation
must be sought for its change in behavior — a failure to eat suffi-
ciently even though food is continuously available. This must repre-
sent an effect of cold stress upon the organism as a whole.
HANNON: I think this is possible in some animals, anyway. I
do not think it appears in rats.
VAUGHAN: Rats will increase their food intake within a couple
of days after you put them in the cold — the delay is probably par-
tially due to the shock of putting them into the cold environment,
but it is also probably due to just moving them into different sur-
roundings. If they are accustomed to a certain diet, we have found,
especially with synthetic diets, that they will increase their food
intake very rapidly in the cold within a few days, e. g., up to 50%
over their normal rate of intake.
*Mayer, J. 1953. Genetic traumatic and environmental factors in the etiology
of obesity. Physiol. Rev. 33:472-508.
**Kleiber, M. 1926. Problems involved in breeding for efficiency of food utiliza-
tion. Amer. Soc. Animal Prod. Proceed, pp 249.
***Kleiber, M. 1961. The Fire of Life. An Introduction to Animal Energetics. New
York, Wiley and Sons, Inc. pp 282 ff.
***Brobeck, J. R. 1946. Regulation of Energy Exchange. Howell's Textbook of
Physiology. (J. F. Fulton, ed.) Philadelphia, Saunders.
289
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