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COMPARATIVE PHYSIOLOGY

OF TEMPERATURE REGULATION

PART 3

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Editors

JOHN P. HANNON
ELEANOR VIERECK

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ARgTIC AEROMEDICAL LABORATORY

FORT WAINWRIGHT

ALASKA

1962

COMPARATIVE PHYSIOLOGY
OF TEMPERATURE REGULATION

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PART 3

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Editors

JOHN P. HANNON
ELEANOR VIERECK

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ARPTIC AEROMEDICi^J^ LABORATORY

FORT WAINWRIGHT

ALASKA

1962

RESPONSES AND ADAPTATIONS OF WILD BIRDS
TO ENVIRONMENTAL TEMPERATURE

George C. West

Birds maintain relatively constant bcxiy temperatur^Sv in gen-
eral several decrees higher than those of mammals, in spite of
external temperatures that range for some species to above 40 C
and for others as low as -60 G. The ability to maintain a constant
temperature in the face of such thermal extremes is dependent
upon the proper coordination and regulation of the mechanisms for
heat production and heat loss. A complete understanding of these
mechanisms would enable one to obtain a more thorough picture of
how birds adapt to their ever changing environments in nature.

The basic principles of thermal exchange inhomeothermshave "
been well reviewed by Hart (1957) and more recently by King and
Farner (1961), who have shown that birds behave essentially as
heat machines, varying heat gain and heat loss to maintain a con-
stant temperature under all thermal conditions in which they are
capable of surviving.

This review will attempt to summarize some of the recent work
on the responses of wild birds to temperature, with particular em-
phasis on the effect of environmental temperature below body tem-
perature and the bioenergetic adaptations of birds to temperature
under natural conditions.

Body Temperature

A large number of deep body temperatures have been recorded
for adult birds in almost every order (Baldwin and Kendeigh, 1932;
Bartholomew and Dawson, 1954; Bartholomew and Gade, 19 57; Daw-
son, 1954; Earner, 1956; Farner etal., 19 56; Irving and Krog, 1954,

♦Contribution, in part, from the Division of Applied Biology, National Research!
Council, Ottawa, Canada. Issued as N.R.C. No. 6629.

291

WEST

1955, 1956; Steen and Enger, 1957; Udvardy, 19 53, 1955; Wetmore,
1921; and others). The variety of methods used, however, prohibits
legitimate comparison in most cases, e.g.: (1) use of a thermo-
couple or mercury thermometer inserted into the cloaca or proven-
triculus of a bird held in the hand, (2) use of a thermometer in the
cloaca or proventriculus immediately after shooting, (3) use of
thermocouples inserted temporarily in the cloaca, (4) use of indwel-
ling thermocouples implanted with the junction under the skin or in
the pectoral muscles. The last method will give the most satisfac-
tory results for comparative purposes, especially when tempera-
tiires are recorded continuously in the dark at night (for diurnal
species) while the bird is at a thermoneutral temperature (near 30
G) and in a post- absorptive condition (King and Farner, 1961). Deep
body temperatures obtained under these conditions average about
40.3 C for passerines and 39.5 C for non-passerines.

The core temperatures of birds are relatively constant,, and
fluctuations in temperature are minimized. The shell, consisting of
the skin, feathers, scales, subcutaneous fat, and tissue, including
some skeletal muscle, acts as an insulating layer whose rate of
thermal conductance can be increased when deep body temper atures
rise and decreased when deep body temperatures fall. The distal
unfeathered portions of the leg and foot are most important for
rapid dissipation of heat (Bartholomew and Dawson, 19 58), while the
subcutaneous fat and feathers are important for the prevention of
heat loss.

Gore temperatures of adult diurnal birds increase with gross
activity during the day and drop when the bird is at rest during the
night. At high and constant ambient temperatures, diurnal fluctua-
tions in body temperature are less pronounced, being about 1 C to
3 C (Bartholomew and Dawson, 1954; Dawson, 1954), while at low
ambient temperatures, body temperatures may drop 3 C to 4 C
at night below the normal daytime value (Fig. 1) .

Temporary hypothermia has been recorded for adult birds in
the Gaprimulgiformes, Apodiformes and Goliiformes (Bartholomew,
Howell, and Gade, 1957) and possibly in two families of the Passeri-
formes, the Hirundinidae (McAtee, 1947) and the Paridae (Steen,

292

BIRD ADAPTATIONS

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Figure 1. Body temperatures of eight Evening Grosbeaks recorded by indwelling
thermocouples at a constant temperature of 30 C (0). a constant temperature of
-15 C (■), and outdoors during January at -6.8 C (•).

293

WEST

19 58). It has been observed that nocturnal h3qDothermia in the cold,
such as that recorded by Steen, in small passerines is c^ten due to
the birds' inability to adapt to caging and experimental conditions
on the first night of capture. Most birds whose body temperatures
dropped more than 4 C the first night of capture lost weight or
ultimately did not survive (Fig. 2) .

Temporary hypothermia is common among the young of most
altricial species since they are essentially poikilothermic when
hatched and develop homeothermy during the nestling period (Bald-
win and Kendeigh, 1932). Body temperatures of these young, there-
fore, are subject to considerable variation independent of activity
or time of day since they are dependent for warmth on the brooding
of their parents.

Heat Regulation

Physical Mechanisms. Physical thermoregulation involves al-
teration in the physical aspects of the shell, increased use of the
respiratory surfaces as an avenue of heat loss, and changes in be-
havior pattern. As the temperature falls below thermoneutrality,
birds gradually increase their total insulation until it reaches a
maximum level, which is then maintained. According to classical
theory, this increase in insulation occurs before an increase in
heat production is required (Fig. 3)(Scholander et al., 1950a; Hart,
1957; King and Farner, 1961). Insulation in the cold involves vaso-
constriction of peripheral vessels, increase in the insulating ability
of the plumage, and behavioral adaptations such as huddling, sitting
on legs and feet, 'TDalling up" by putting the head under the wing,
burrowing, or roosting in cavities (Kendeigh, 1961a). It is evident

that the plumage is the major insulator, since temperatures recorded

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under the skin are within 0.5 C to 1.0 C of the core temperature

(Steen and Enger, 1957; West and Hart, unpublished), and thermo-
couples placed on the skin under the feathers are also within 1 C
to 2 C of the core temperature (Dawson and Tordoff, 1959).

Direct measurements of the insulating ability of the plumage
are difficult to make (Scholander et al., 1950b), but calculations of

294

BIRD ADAPTATIONS

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Figure 3. Classical picture of partition of chemical and physical thermoregula-
tion, showing the thermoneutral zone (ABB'), the critical temperature (B, B'), and
metabolism slopes (BCD, B'C'D') that extrapolate to body temperature (T). (Hart,
1957).

296

BIRD ADAPTATIONS

insulating ability have been made for several species of birds at
thermoneutrality and at a few lower temperatures (Hart, 1957;
Misch, 1960; Wallgren, 19 54; West, unpublished). Investigations on
the Evening Grosbeak (Hesperiphona vespertina) and calculations
based on data in the literature indicate that the total insulation
(Body T - Air T/(kcal x bird x hour)) increases gradually as tem-
perature falls (Fig. 4). It can be readily observed that the insulation
increase is almost linear for some species (Tree Sparrow, Spizella
arborea) , but a curve for most. The highest temperature at which
insulation reaches its maximum is 0 C in both the Cardinal (Rich-
mondena cardinalis) and the Evening Grosbeaks studied by Dawson
and Tordoff (1959), while many species continue increasing their
insulation to the lowest test temperature (House Sparrow, Passer
domesticus, and Variable Seedeater, Sporophila aurita).

Conservation of heat at cold temperatures by peripheral blood
flow control and vascular heat exchange in non- insulated portions of
the body has been demonstrated in the Glaucous- winged Gull (Larus
glaucescens) (Irving and Krog, 1955) and in many other species
(Bartholomew and Dawson, 1954; Bartholomew and Cade, 1957;
Scholander, 1955).

At air temperatures approaching body temperature, insulation
is decreased to its minimum, and mechanisms for dissipation of
heat are invoked. These include increase in peripheral blood flow
to the legs and feet, increased ventilation, evaporation from the
respiratory surfaces, and panting. Some birds are able to increase
the temperatures of their legs and feet and still maintain a favorable
gradient for heat loss even attemperatures above body temperature
(Bartholomew and Dawson, 1958). Birds living in hot regions have
evolved behavior patterns enabling them to avoid the heat of day.

Metabolic mechanisms. Thermogenesis in reponse to cold
occurs chiefly by increased physical activity such as exercise, in-
creased muscle tone, and shivering. The heat produced by the spec-
ific dynamic action of digestion and assimilation may help to main-
tain body temperature, but evidence for this is lacking in wild birds
(King and Earner, 1961). Non-shivering thermogenesis has been

297

WEST

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Figure 4. Insulation indices calculated by the formula:

Body T C - Air T G
kcalA)ird/hour

Average indices of birds held at constant temperature (•,A); and of birds under
natural fluctuating conditions (0,A). TS=Tree Sparrow (West, 1960), GB=Evening
Grosbeak (West and Hart, unpublished). Thedashed lines are values calculated from
the literature: J=Slate-colored Junco (Seibert, 1949); YB=Yellow Bunting (Wallgren,
1954); VSE=Variable Seedeater (Cox, 1961; C=Cardinal (Dawson, 1958); HS=House
Sparrow (Kendeigh, 1949); BJ=Blue Jay (Misch, 1960); GB=EveningGrosbeak (Dawson
and Tordoff, 1959).

298

BIRD ADAPTATIONS

described for the white rat (Cottle and Carlson, 1956), but the few
experiments done by Hart (in press) indicate that curarized pigeons
(Columba livia) are not able to increase their metabolism in the
cold.

Recent work by Steen and Enger (19 57) on pigeons and by West
(unpublished) on Evening Grosbeaks and Common Redpolls indicate
that shivering is the major source of heat production by birds in the
cold. Experiments on the Evening Grosbeak show that these birds
shiver all night out-of-doors at all temperatures below thermoneut-
rality in both summer and winter. The intensity of shivering in-
creases as the ambient temperature falls (Fig. 5) .

Since shivering in particular and metabolic thermoregulation
in general are achieved by an increase in energy expenditure, it
is pertinent to review some of the recent work on energy exchange
in wild birds.

Indirect calorimetric measurements of heat production can be
made either by recording the respiratory exchange of oxygen and
carbon dioxide or by recording food consumption and excrement
production. Although the first method has been widely used by most
workers, it is limited in that metabolic rates are sampled over rel-
atively short periods of time. Both "open circuit" and "closed
circuit" apparati have been employed, the latter being further re-
stricted because the ambient temperature must remain constant.
Energy balance studies such as those used by Kendeigh (1949),
Seibert (1949), Davis (19 55), King and Earner (1956), West (1960),
and Cox (1961) for wild birds yield an average metabolic level over
a period of several days. However, this method is not able to dis-
tinguish between metabolic levels at different times of the day.

Automatic recording oxygen and carbon dioxide analyzers have
been successfully used to record oxygen consumption and carbon
dioxide production simultaneously for 2 to 3 days at a time on wild
birds. The birds live in small cages and are supplied with food and
drink ad libitum. Daytime and nighttime values can easily be obtained
by examining selected portions of the record (Fig. 6). Another ad-
vantage of this system is that the birds are not disturbed once the

299

WEST

-10 0 10 20

TEMPERATURE °C

Figure 5. Shivering of summer acclimatized Common Redpolls recorded in
microvolts during short term exposure at each temperature. Each point repre-
sents averages of four birds.

300

BIRD ADAPTATIONS

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WEST

experiment is under way. We have observed that metabolic rates
remain elevated for about 1 hour after the birds have been placed
in a darkened metabolism chamber (West and Hart, unpublished).

Previous thermal history affects the metabolism of an animal at
any given test temperature. In order to test the effect of ambient
temperature on mot£.oolism, it has been customary to follow one of
two methods: (1) Biids are acclimated to a single constant tempera-
ture of season and then metabolism values are obtained at a series of
test temperatures (Scholander et al., 1950a; Wallgren, 1954; Irving
et al., 1955; Steen, 1957; Dawson, 1958; Dawson and Tordoff, 1959;
Misch, 1960; Hart, in press; West and Hart, unpublished; and others).
(2) Birds are acclimated and their metabolism measured at a single
temperature; the temperature is changed and the birds are accli-
mated and run again, etc. (Kendeigh, 1949, Seibert, 1949; Davis,
1955; Rautenberg, 1957; West, 1960; Cox, 1961; and others).

Many workers have assumed that a linear regression line fitted
to the metabolism values at a series of temperatures must extra-
polate to body temperature according to Newton's law of cooling
(Scholander et al., 1950a; Steen, 1957; and others). This interpret-
ation results in a distinct thermoneutral zone and a critical tempera-
ture which divides physical from chemical thermoregulation. Most
of the results on small birds obtained by these workers can be equal-
ly well interpreted as either a straight line drawn through all points,
thus eliminating the critical temperature and thermoneutral zone
completely (Fig. 7) or as a curve, which also eliminates the defini-
tion of a single critical temperature. The latter interpretation has
been suggested by Dawson (1958) for his data on the Cardinal (Fig.
8), and by Dawson and Tordoff (19 59) for the Evening Grosbeak.

The slopes obtained by workers measuring metabolism over
24 hour periods are in general much flatter than those obtained in
short-term tests on non- acclimated birds. They show no thermo-
neutral zone, no critical temperature; and the temperature vs. meta-
bolism slope does not extrapolate to body temperature (Fig. 9).
Studies in progress on the Evening Grosbeak indicate that the flat
slopes may be explained by marked differences in diurnal and noc-
turnal metabolism and levels of motor activity that change with

302

BIBD ADAPTATIONS

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303

WEST

CARDINAL

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Figure 8. Oxygen consumption of Cardinals at various temperatures. Modified
from Dawson (1958). (Courtesy of University of Chicago Press, copyright holder).

304

BIRD ADAPTATIONS

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ambient temperature (West and Hart, unpublished).

It seems reasonable from the available data that most small
wild birds have a curvilinear relationship of metabolism to tem-
perature (Fig. 10). The data in Figure 4 indicate that most birds
increase their insulation gradually from high to low temperatures,
rapidly at first, then leveling off as maximum insulation is achieved.
Heat production, however, increases slowly at first, but then pro-
ceeds faster as metabolic mechanisms become the only method of
maintaining homeothermy at the lower temperatures. The slope of
the curve at the lower temperatures extrapolates to body tempera-
ture according to Newton's law of cooling. However, the upper por-
tion of the temperature- metabolism curve extrapolates beyond body
temperature since both insulative and metabolic mechanisms are
operating simultaneously. Therefore, a prolonged thermoneutral
zone and a definite critical temperature probably do not exist for
wild birds.

Acclimation and Acclimatization

Gelineo (1955) acclimated birds to three constant tempera-
tures and then obtained metabolism values at a series of test
temperatures for each acclimation group. In most cases the cold
acclimated birds had a higher metabolism slope and thermo-
neutral metabolism than the warm acclimated birds (Fig. 11). Sim-
ilar results have been obtained by Miller (1939) for House Spar-
rows, Dontcheff and Kayser (1934) and Steen (19 57) for the Pigeon,
and Wallgren (1954) for the Ortolan (Emberiza hortulana) and
Yellow Bunting (Emberiza citrinella) .

Contrary to the results obtained with temperature conditioned
birds, most species acclimatized to summer and winter seasons do
not show differences in their standard metabolisms or in their
temperature metabolism slopes (Kendeigh, 1949, and Davis, 1955,
for the House Sparrow (Fig. 12); Wallgren, 19 54, for the Yellow
Bunting; Irving et al., 19 55, for the Black Brant (Branta nigricans);
Rautenberg, 1957, for the House Sparrow and Brambling (Fririgilla
montifrir.gilla) ; Dawson, 19 58, for the Cardinal; Hart, in press,
for the Pigeon, House Sparrow, Evening Grosbeak, and Starling

306

BIRD ADAPTATIONS

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TEMPERATURE

Figure 10. Overlap of insulative (dashed line) and metabolic (solid line)
adjustments for thermoregulation in small wild birds. After insulation reaches
its maximum, increases in metabolism carry the bird to its lower limit of tolerance
(Lj). This slope extrapolates to body temperature (BT) according to Newton's
law of cooling. Above body temperature, metabolism increases, and insulation
reaches its minimum as the upper limit of tolerance is reached (L ).

307

WEST

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TEMPERATURE

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Figure 11. Temperature- metabolism curves of birds acclimated to warm (•)
and cold (O). Gelineo's data replotted by Hart (1957).

308

BIRD ADAPTATIONS

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TEMPERATURE •C

Figure 12. Metabolized energy of winter (O) and summer {•) acclimatized
House (English) Sparrows. Davis' data replotted by Hart (1957).

309

WEST

(Sturnus vulgaris). The reason for the difference in metabolic
response between laboratory acclimated and seasonal acclimatized
birds may be that the temperature conditioning process is sup-
pressed by variable ambient temperatures (King and Farner, 1961).

The ability of birds to tolerate low temperature extremes is one

of the best indications of seasonal metabolic acclimatization. The

work of Kendeigh (1949), Seibert (1949), and Davis (19 55) clearly

shows that the House Sparrow can extend its low temperature tol-

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erance limit from 0 C in the summer to -31 C in the winter (Fig.

12). In contrast, the Tree Sparrow does not change its lower limit
of tolerance and survives to -28 C in both summer and winter
(West, 1960). The ability to tolerate low temperatures depends pri-
marily on the length of time that the birds can maintain their max-
imum metabolic rates. By subjecting seasonally acclimatized birds
to a single low temperature. Hart (in press) shows that winter ac-
climatized Evening Grosbeaks, Starlings, and Pigeons can maintain
their maximum metabolic rates for longer periods of time than
summer acclimatized birds.

In addition to increased metabolic capacity during the winter,
there may be a seasonal shift in insulation since Kendeigh (1934)
showed a 29% increase in plumage weights of winter over summer
House Sparrows, and West (1960) an increase of 25% of winter over
summer plumage weights of Tree Sparrows.

Many species of birds exhibit annual cyclic thyroid activity
while others do not (Wilson and Farner, 1960). Wilson and Farner
show a direct correlation between thyroid activity and ambient tem-
perature in the Gambel's White-crowned Sparrow (Zonotrichialeu-
cophrys gambelii). These birds experienced an annual temperature
cycle of at least 20 C (0 C to 20 C) in eastern Washington. Sim-
ultaneously, Oakeson and Lilley (1960) studied the same race of
White-crowned Sparrow both on its wintering ground in California
and on its breeding ground in Alaska and in contrast, found no annual
change in thyroid activity. Wilson and Farner explain this difference
by showing that the amplitude of the cycle of temperature that Oak-
eson and Lilley's birds experienced was probably about 5 C, 15 G
less annual variation than their own birds received.

310

BIRD ADAPTATIONS

This brings out an interesting correlation between thyroid
activity and metabolic acclimatization in migrant and non- migrant
species. From the data cited above and from those of Miller (1939),
it may be observed thatpermanentresident species have pronounced
thyroid cycles and therefore greater degrees of metabolic acclim-
atization because they experience pronounced annual fluctuations in
temperature, while migrants, such as the Tree Sparrow or the
White- crowned Sparrow studied by Oakeson and Lilley do not have
cyclic changes in thyroid activity and therefore little change in meta-
bolic acclimatization because they experience similar temperature
conditions in both winter and summer.

Ecological Implications

The physical and metabolic thermoregulatory mechanisms
possessed by a species enables it to adapt to a specific set of en-
vironmental conditions, i.e., its distribution is limited by these
mechanisms. The habitation of any area is determined in part by
the ability of a species to acquire not only enough existence energy,
but also sufficient productive energy (Kendeigh, 1949) for carrying
on energy demanding activities such as molting, reproduction, and
migration. In addition to these physiological limits, morphological
and behavioral adaptations impose further restrictions on, the actual
distribution of a species. Although thermoregulatory adaptations to
specific environments are covered elsewhere in this symposium,
it is important to discuss some of the energy requirements for exis-
tence and other activities under natural conditions.

The energy intake of all small wild birds yet studied increases
in the winter. The added energy intake is used for existence, which
includes maintenance of homeothermy and body weight, acquiring
food and drink, the SDA of digestion and assimilation (Kendeigh,
1949), and the deposition of body fat. The added fat may be an emer-
gency measure against severe winter weather or an aid in total
insulation. Permanent resident species of temperate regions, such as
the House Sparrow, maintain favorable energy conditions throughout
the year by increasing their ability to metabolize energy in the cold
(see above). Permanent residents of tropical regions, such as the

311

WEST

Variable Seedeater, Yellow-bellied Seedeater (Sporophila nigricol-
lis), Blue-black Grassquit, (Volatinia jacarina), and Green-backed
Sparrow (Arremonops conirostris) , need vary their energy intake
for existence only slightly, with minor changes in temperature and
photoperiod throughout the year (Cox, 1960).

Migrant species, however, must adjust to the climatic conditions
of two localities. Arctic and temperate breeding birds attain more
nearly uniform environmental temperatures by migrating to southern
latitudes in the winter. Therefore, the lack of metabolic acclimat-
ization in the Tree Sparrow (see above) maybe a result of spending
the whole year in a relatively constant climate.

In contrast to permanent resident species, migrant birds must
increase their energy intake for migratory flights in the spring and
fall (Famer, 1955; Rautenberg, 1957; Kendeigh et al., 1960). The
added energy intake is used for the deposition of migratory fat, and
in caged birds, for motor activity at night (Zugunruhe). When fat
stores are completed and weather conditions are satisfactory, actual
flight, utilizing the stored fat, occurs. The pattern of added energy
intake for fat deposition alternated with migratory flights is repeated
until the final destination is reached (Wolfson, 1954). The added cost
of fat deposition and spring nocturnal unrest increases the daily
energy intake of White-crowned Sparrows by 30% to 50% (King and
Farner, 1956) and the intake of Tree Sparrows by 21% to 22% (West,
1960; Kendeigh et al., I960).

Following migration, reproductive activities are initiated. The
amount of energy required to produce a clutch of eggs is undoubtedly
considerable although it has not been experimentally determined for
wild birds (Kendeigh, 1941). The added cost of incubation of eggs by
the female Tree Sparrow has been calculated to add about 22% to its
existence energy requirementperday (West, 1960). Kendeigh (196 lb)
shows that incubating House Wrens (Troglodytes aedon) also require
23% more energy while incubating.

Most small passerines have a complete post nuptial molt in
the fall. The growth of new feathers requires energy. Metabolic
rates of the Chaffinch (Fringilla coelebs) (Koch and deBont, 1944)

312

BIRD ADAPTATIONS

Yellow Buntings and Ortolans (Wallgren, 1954) increased 10% to
26% during molting. The increases, however, are variable, and it
appears that the greatest energy cost occurs during growth of
the large flight feathers of the wing and tail (Koch and deBont,
1944). It is doubtful that' the gradual loss and replacement of fea-
thers causes a measureable lowering of body insulation in most
passerines, and any metabolic increase, therefore, is due to the pro-
duction of new feathers (King and Famer, 1961).

Davis (1955) did not find an increase in metabolized energy of
House Sparrows during molting, although his data exhibited greater
variability at this time. King and Famer (1961) have pointed out that
the added daily cost of producing new feathers is so small that it
might not be detected infood consumption experiments. West (1960),
however, found a 27% increase in metabolized energy of molting
Tree Sparrows for over one week. This may have been during the
time of flight feather regeneration and an average value over several
weeks might be lower.

When the values for fatdeposition, migration, reproduction, and
molting are added to the daily existence level, the total energy ex-
penditure of a single species canbe traced throughout the year (Fig.
13). The added cost of living a free existence as opposed to a caged
existence may be greater in the winter than in the summer due to
the difficulty of finding food. The uniform spacing of energy demand-
ing activities is such that the average daily intake of energy is
about the same throughout the year.

A species must be confined to localities where it can secure
enough energy not only for existence, but also for all its essential
activities. Therefore, climate, and particularly temperature, plays
a major role in controlling distribution by excluding species from
regions which impose energy requirements exceeding metabolic
capabilities.

313

WEST

JAN FEB MAR APR MAY JUN JUL AUG SEP OCT NOV DEC

Figure 13. Total energy requirements of Tree Sparrows throughout the year.
The lowest curve is thatof existence energy to which the energy required by various
activities has been added (West, 1960).

314

BIRD ADAPTATIONS
SUMMARY

Birds maintain relatively constant body temperatures by reg-
ulating mechanisms for heat production and heat loss over a wide
range of environmental temperatures.

The variable insulative ability of the plumage is the chief
mechanism for prevention of heat loss. As temperature falls, in-
sulation gradually increases until it reaches a maximum. At the
same time, peripheral circulation decreases and heat is retained
in the core of the body. Simultaneous with the increase in insulation,
shivering increases as the ambient temperature drops. After the
insulation reaches its maximum, metabolic mechanisms alone main-
tain homeothermy until the lower limit of temperature tolerance is
reached. In most small passerines, the total effect of combined in-
sulation and shivering responses to temperature results in a curvi-
linear relationship of metabolism to temperature, with no prolonged
thermoneutral zone indicated.

Birds acclimated to low constant temperatures in the laboratory
generally have higher metabolic rates at any temperature than those
acclimated to warm temperatures. Birds acclimatized to different
seasons, however, show little change in metabolic response at ther-
moneutral temperatures. Seasonal changes in thermoregulatory
mechanisms involve an increased ability to produce heat by increas-
ing the metabolic rate in the cold of winter for extended periods of
time and possibly an increase in the amount of plumage insulation.

Existence energy requirements of small wild birds living in
temperate regions are increased in the winter. Permanent residents
may have a more pronounced seasonal difference in their ability
to tolerate low temperatures than migrant species since they en-
counter greater extremes of temperature.

The added daily cost of nocturnal unrest and of depositing mi-
gratory fat differs slightly among migrant birds according to the
length of time spent in premigratory preparation and in the average

315

WEST

length of each migratory flight. The average daily intake of small
birds probably remains relatively constant throughout the year,
since energy demanding activities such as existence in winter cold,
deposition of fat, migration, reproduction, and molting are uni-
formly spaced. The distribution of a species is therefore limited
to locations where the climate permits fulfillment of all essential
energy demanding activities.

316

BIPD ADAPTATIONS

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of the American Kestrel. Falco sparvarius. Wilson Bull. 69:
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3. Bartholomew, G. A. and W. R. Dawson. 1954. Body temperature

and water requirements of the Mourning Dove, Zenaidura
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in California and Gambel's <^uail. Auk 7 5:150-156.

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6. Cottle, W. H. and L. D. Carlson. 1956. Regulation of heat pro-

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7. Cox, G. W. 1961. The relation of energy requirements of tropical

finches to distribution and migration. Ecology 42:253-266.

8. Davis, E. A., Jr. 1955. Seasonal changes in the energy balance

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317

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10. Dawson, W. R. 1958. Relation of oxygen consumption and eva-

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11. Dawson, W. R. and H. B. Tordoff. 1959. Relation of oxygen

consumption to temperature in the Evening Grosbeak. Con-
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12. Dontcheff, L. and C. Kayser. 1934. Le rythme saisonnier de

metabolisme de base chez le pigeon en fonction de la tem-
perature moyenne de milieu. Ann. physiol. physicochim.
biol. 10:285-300.

13. Farner, D. S. 1955. The annual stimulus for migration: exper-

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14. Farner, D. S. 1956. Body temperatvire of the Fairy Prion

(Pachyptila turtur) in flight and at rest. J. Appl. Physiol.

8:546-548.

15. Farner, D. S., N. Chivers, and T. Riney. 1956. The body tem-

perature of North Island Kiwis. Emu 56:199-206.

16. Gelineo, S. 1955. Temperature d'adaptation et production de

chaleur chez les oiseaux de petite taille. Arch. sci. physiol.
9:225-243.

17. Hart, J. S. 1957. Climatic and temperature induced changes in

the energetics of homeotherms. Rev. can. biol. 16:133-174.

18. Irving, L. and J. Krog. 1954. Body temperatures of arctic and

subarctic birds and mammals. J. Appl. Physiol. 6:667-680.

19. Irving, L. and J. Krog. 1955. Skin temperature in the arctic as a

regulator of heat. J. Appl. Physiol. 7:354-363.

20. lining, L. and J. Krog. 1956. Temperature during the develop-

ment of birds in arctic nests. Physiol. Zool. 29:195-205.

318

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21. Irving L., H. Krog, and M. Monson. 1955. The metabolism of

some Alaskan animals in winter and summer. Physiol.
Zool. 28:173-185.

22. Kendeigh, S. C. 1934. The role of environment in the life of

birds. Ecol. Monographs 4:299-417.

23. Kendeigh, S. C. 1941. Length of day and energy requirements

for gonad development and egg- laying in birds. Ecology 22:
237-248.

24. Kendeigh, S. G. 1949. Effect of temperature and season on the

energy resources of the English Sparrow. Auk 66:113-127.

25. Kendeigh, S. G. 1961a. Energy conserved by birds roosting

in cavaties. Wilson Bull. 78:140-147.

26. Kendeigh, S. G. 1961b. The energy cost of incubation. MS.

27. Kendeigh, S. C., G. G. West, and G. W. Gox. 1960. Annual

stimulus for spring migration in birds. Animal Behaviour

8:180-185.

28. King, J. R. and D. S.Famer. 19 56 . Bioenergetic basis of light-

induced fat deposition in the White-crowned Sparrow. Proc.
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29. King, J. R. and J. S.Famer. 1961. Energy metabolism, thermo-

regulation and body temperature, p. 215-288. In Marshall's
Biology and Gomparative Physiology of Birds.

30. Koch, H. J. and A. F. deBont. 1944. Influence de la mue sur

I'intensite de metabolisme chez le pinson, Frinsilla coelebs
coelebs. L. Ann. Soc. zool. Belg. 75:81-86.

31. McAtee. W. L. 1947. Torpidity in birds. Am. Midland Natur-

alist 38:191-206.

319

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32. Miller, D. S. 1939. A study of the physiology of the sparrow

thyroid. J. Exp. Zool. 80:259-281.

33. Misch, M. S. 1960. Heat regulation in the Northern Blue Jay,

Cyanocitta cristata bromia Oberholser. Physiol. Zool. 33:
252-259.

34. Oakeson, B. B. and B. R. Lilley. 1960. Annual cycle of thyroid

histology in the races of White-crowned Sparrow. Anat.Rec.
136:41-57.

35. Rautenberg, W. 1957. Vergleichende Untersuchungen uber den

Energie haushalt des Bergfinken (FringillamontifringillaL.)
und des Haussperlings (Passer domesticus L. ) , J. Omithol.
98:36-64.

36. Scholander, P. F. 1955. Evolution of climatic adaptations in

homeotherms. Evolution 9:15-26.

37. Scholander, P. F., R. Hoch, V.Walters, F.Johnson, and L. Irv-

ing. 19 50a. Heat regulation in some arctic and tropical mam-
mals and birds. Biol. Bull. 99:237-258.

38. Scholander, P. F., V. Walters, R. Hoch, and L. Irving. 1950b.

Body insulation of some arctic and tropical mammals and
birds. Biol. Bull. 99:225-236.

39. Seibert, H. C. 1949. Difference between migrant and non-mig-

rant birds in food and water intake at various temperatures
and photoperiods . Auk 66:128-153.

40 . Steen , J. 19 57 . Food intake and oxygen consumption in pigeons at

low temperatures. Acta Physiol. Scand. 39:22-26.

41. Steen, J. 1958. Climatic adaptation in some small northern

birds. Ecology 39:625-629.

42. Steen, J. and P. S. Enger. 1957. Muscular heat production in

pigeons during exposure to cold. Am J.Physiol. 191:157-158.

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43. Udvardy, M. D. F. 1953. Contribution to the knowledge of body

temperature in birds. Zool. Bidvag. Uppsala 30:25-42.

44. Udvardy, M. D. F. 19 55. Body temperature of parids in the arc-

tic winter. Ornis Fennica. 32;10 1-107.

45. Wallgren, H. 1954. Energy metabolism of two species of the

genus Emberiza as correlated with distribution and migration.
Acta Zool. Fennica 84:1-110.

46. West, G. G. 1958. Seasonal variation in the energy balance of

' the tree sparrow in relation to migration. Ph. D. Thesis,
Univ. of Illinois, Urbana.

47. West, G. C. 1960. Seasonal variation in the energy balance of

the tree sparrow in relation to migration. Auk 77:306-329.

48. Wetmore, A. 1921. A study of the body temperature of birds.

Smithsonian Misc. Coll. 72(12) :51pp.

49. Wilson, A. C. and D. S. Famer. 1960. The annual cycle of

thyroid activity in White-crowned sparrows of eastern Wash-
ington. Condor. 62:414-425

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434.

321

WEST
DISCUSSION

JO HANSEN: I am very impressed with all the facts that are
available on birds now. I think this surpasses what we know about
mammals, particularly with regard to ecological factors involved
in temperature regulation. I was particularly pleased to hear your
doubts as to whether we really can consider the critical tempera-
ture as a fixed point, and also whether insulation is gradually
mobilized during the period of active increase in metabolism. As
I pointed out in my paper, I think this applies also to the more
primitive mammals.

WEST; And I think also to the small mammals.

JOHANSEN; Definitely. I had another question, and that is,
how does this ten-fold difference in electrical activity correspond
with the actual metabolic difference between the two? Could you
comment on that?

WEST; We do not have the metabolism of the rats worked out
in calories. Also no simultaneous measurements of metabolism
and shivering have been done at a series of temperatures for
mammals.

JOHANSEN; I was wondering whether you could correspond
metabolism with electrical activity.

WEST: I have done it for birds but not for mammals. In birds
there is a linear relationship between electrical activity and meta-
bolism. The slope varies with the size of the bird. So far we have
plotted data for three species and the smallest, the common red-
poll, increases its electrical activity much faster than it does

its metabolism. The larger birds do not increase their shivering

o
as fast and there is about a 45 slope for birds of about 100 grams.

HART: It is much higher for birds than it is for mammals.

322

BIRD ADAPTATIONS

HAKT: No, not ten times. For example, the pigeon has about
the same weight as the rat, and it has about five times the electrical
activity. We do not know enough about different species of birds,
but this is the trend. It seems there is a much greater electrical
activity in birds.

WEST: I think this will work out better when we put it on a power
spectrum basis rather than a simple muscle potential.

HANNON: It would seem,if youhad agood measure of shivering
activity, you should be able to have a 45 relationship between meta-
bolic change and shivering change or muscle activity change.

WEST; Yes, muscle is the source of total heat production and
I believe that if the results are standardized on a body surface basis
the lines would be close together.

HANNON; Because your peak microvolts went up considerably
faster than your metabolism did.

HART: Yes, that went up about ten times.

HANNON; For 100% increase in metabolism, there is a con-
siderably greater increase in peak microvolts as a measure of
your shivering.

WEST; I agree, for the smaller species.

PROSSER; After all, what you are concerned v/i this the energy
produced by the chemical reactions in the muscle. Might not a deli-
cate vibration detector or something for measuring movement be
as effective? Have you tried any of these spring gadgets?

IRVING: Ballistic cardiograph?

PROSSER: Yes, like a ballistic cardiograph.

WEST: We have not tried any, no.

323

WEST

ADAMS: I would suggest that there must be a constant differ-
ence in the relationship between the shivering index as you have it
and the oxygen consumption, since you do have a straight line
relationship. And if this is true, then perhaps we have a frequency
recording artifact all the way along the scale, not just at one peak.

WEST: The frequency of shivering is very low at the higher
temperatures and we do record that faithfully, because it only goes
up to around 200 cycles per second or so, but our recent analysis
shows that intense shivering goes as high as 700 c.p.s.

PROSSER; Of course you have to sacrifice the bird, but just
as a check it might be useful to do phosphocreatine breakdown. I
would like to ask one question about the fact that you find no differ-
ence in the slope or in the shivering response with the seasons,
but do find that the winter birds can maintain their metabolism
longer under cold stress. Now, this suggests that acclimatization
may be an endocrine phenomenon. Have you any information about
the state of the adrenal cortex?

WEST: Not about the adrenal cortex, but a little on the thyroid.
But Wilson and Earner, and Oaksen and Lillie have found that the
thyroids of permanent resident birds that were held in one spot
increased in the winter time because the temperature fluctuated
greatly, which corresponds to the permanent resident metabolic
acclimatization. But birds studied on their wintering ground in
California and on their summer ground in Alaska, showed no differ-
ence in thyroid, 'Taecause" they experienced a temperature fluctua-
tion both summer and winter of 5 G, whereas those maintained

o
in Washington had a temperature fluctuation of 20 C. This may be

a tie-up there, although this is very tenuous, and there are results
in thyroid activity going in the other direction for some species.
I do not know anything about the adrenal.

IRVING: I look at migratory birds from the wrong end. I mean
from the unconventional end of being on the arctic ground where
the birds arrive after migration, instead of in the temperate places
from which they are preparing to start. It has always been

324

BIRD ADAPTATIONS

interesting for me to see this migratory fat still preserved by birds
at the time of their arrival on the nesting ground, and then diminish-
ing markedly during the period of courtship of the male and some-
where along during the incubating period of the female. So I am not
sure that it is strictly and seasonally a migratory fat, although it
may beusefulforthebird topackhis California fat up to Alaska. But
certainly the moment when migratory fat is utilized is, like the fat
of the bull fur seal, during the actual breeding period.

WEST: Are you speaking of shore birds primarily?

IRVING: It is pretty general among the birds arriving in arctic
Alaska breeding grounds. There are some 40 species for which I
have sufficient records to be indicative including all families and
sizes.

WEST: Do you think possibly a sandpiper or plover who may
fly non-stop over a great distance could retain a large proportion
of his fat when he reaches the breeding ground?

IRVING: They do have considerable fat when they arrive so far
as I can compareweights with those of similar birds when they were
ready to depart from the wintering grounds. They may be a little
less fat, but they are still very fat birds.

WEST: The question then arises how they get enough energy to
fly that distance unless they stop enroute to keep augmenting their
fat stores, which we know to be the case in passerines.

IRVING: I realize these are net results, but the situation of the
observer can change one's point of view. You mentioned the energy
requisite for reproduction. The other day I was looking at the eggs
of Least Sandpipers, which, like all sandpipers, are quite large. We
weighed these and the four eggs weighed 25 grams. They were laid
on four successive days and the female bird which produced them
weighed 21 grams; I suggest that you might start introduction of
Least Sandpiper blood into white leghorns because the sandpiper
equals her weight in egg production in four days, instead of the two
months necessary for the good white leghorn to equal her weight of
egg production.

325

WEST

FOLK: I have two points to make; one is, we are equally sur-
prised to find a large quantity of fat in hibernating ground squirrels
after 4 months of hibernation. Not all animals, but some are very
conspicuously fat in spite of the fact that they awaken periodically.
This matches Dr. Irving's observations on birds. The second ques-
tion is a technical one. In measuring the oxygen consumption of the
evening grosbeaks you described a 3-day run with a hood on the
cage. Do you continue a photo-period during this period?

WEST: Yes.

FOLK; And what is the photo- period?

WEST: Ten hours of light. We use a lucite cover with a loose
polyvinyl plastic cylinder taped to it that slides down over the
cylindrical cage and is sealed to the sides of the cage with electrical
tape. An outlet is provided at the top where air is pumped out into
the oxygen analyzer. An inlet is provided at the base of the cage.
These cages are identical with the cages we use for acclimation or
for housing the birds, and so we just have to drop the hood over
them. I think there is a lot to this psychological business. They do
not have to adjust to a new cage.

IRVING: I have seen calculations on fat and tried to make some
myself to indicate that a gram of fat will transport a 20 gram bird
quite a long distance; the several grams that they have is adequate
for quite a considerable extra expenditure of metabolic energy, but
how about the requirement for water? I have not seen reference to
any visible reserve for water.

WEST: You mean birds migrating over the ocean?

IRVING: Yes. I wonder how they hold out.

WEST: You do not think they get enough metabolic water?

IRVING: I do not know. Can you calculate the water require-
ments and relate them to stores?

WEST: I have not done so.

326

BIPD ADAPTATIONS

IRVING: Rough calculations which I have tried to make and
which I do not trust suggest that water may be much more criti-
cal than the fat.

WEST: You are thinking, of course, of birds that are flying
over the ocean.

IRVING: Yes.

WEST: And I am always thinking of sparrows that hop, skip,
and jump 100 miles a flight and then come down.

IRVING: This flight is nothing to them; it takes an hour or two.

WEST: Yes, they do about 30 miles an hour, roughly. How long
does it take for an Arctic Tern or Golden Plover to go its distance
non-stop? Do they not go very fast?

IRVING: The travel of the plover from Alaska to Hawaii and
from New Foundland or Nova Scotia to South America is a couple
thousand miles non-stop.

WEST: How many hours, forty- eight hours?

IRVING: It is in the order of a couple of days rather than so
many hours.

WEST: I think they could probably make it all right with respect
to water requirements.

PROSSER: Are you sure they never put down?

IRVING: It has not been observed and it is inconceivable that
they could derive any benefit from it except to sit out the time.
They are not swimming birds. They could not feed there.

HART: Gould they drink the sea water and excrete the salt?

327

WEST

MORRISON: I would like to return to the matter of the applica-
bility of these simple relations between metabolism and ambient
temperature, which was first raised by Dr. Johansen's talk. I do
not think that we should speak as though this relation is discredited
and not applicable in these animals. We must remember that these
represent limits which any animal will follow more or less closely.
They are limits of minimum metabolism and of minimum thermal
conductance and as such are excellent descriptive terms. Now, the
great deviation of your birds from the limiting curve is very inter-
esting as representing a physiological inefficiency since this extra
metabolism need not be expended if the bird were using the maxi-
mum potential of its insulation. It would be useful to describe the
bird both in terms of its limiting conductance, and also in terms of
its deviation from that limit. Perhaps this might be in terms of the
temperature range over which it deviates and the ratio of the meas-
ured and the basal metabolism at the critical temperature.

WEST: I agree to that, but with these birds there is such great
deviation we should not force our data to fit the classical theory,
just because it is a classical theory.

JOHANSEN: Critical temperature as a term is only meaning-
ful when we know that the core temperature stays constant up to
this point.

MORRISON: I am not sure that the critical temperature has
been strictly defined in terms of these refinements.

PROSSER: Why does a bird molt? It seems to me a most
wasteful thing. What is the advantage of getting rid of an old set
of feathers to grow a new set?

WEST: They wear out.

PROSSER: Are new feathers really better insulators?

WEST: They probably are. I do not know, but they wear out.
From the behavioral standpoint, they have to grow their new colors
again for the fall and spring. We know that the total weight changes,

328

BIRD ADAPTATIONS

but we do not see any evidence in any of our curves that there is
any effective increased insulation.

HANNON: This goes on in most animals, does it not? We grow
more skin continuously.

IRVING: If you look at the plumage of birds from tropic or
arctic locations, you have a hard time convincing yourself by that
examination that one is arctic and one is tropic. Among the jays
you might think that there is a little thinner body plumage on the
tropical than on the arctic form, but the quantity of feathers does
not seem to vary very much with the climate where the specimen
originated. Of course feathers are not for insulation alone; they
serve an aerodynamic function in which the dimensions of a bird
that would be affected by increasing its feathers would quite des-
troy its aerodynamic qualities, although a mammal can carry fur
ten times as long if he does not trip over it.

PITELKA; Your question, Dr. Prosser, is aggravated by a
circumstance which is not yet well documented in the literature,
which is that some tropical species, if they are not breeding, are
molting. Dr. Irving a moment ago mentioned tropical jays; I have
some data shortly to be published for a 50-gram species of tropical
jay. The breeding season is March through June or July and other-
wise the population as a whole is molting, starting its molt in late
May and continuing into February, so that in effect the birds are
either breeding or molting. And when we get situations like this,
contrasting with tree sparrows or longspurs which molt in a very
short time, then the whole business of budgeting of energy and
the advantage of the molt is so delicately adjusted as it is, becomes
more interesting and intriguing.

I would like to comment on a couple of other things about plum-
age which are relevant to Dr. West's remarks about insulative
problems and also relevant to something Dr. Irving said a moment
ago. There is one kind ofdifference between high latitude and tropi-
cal birds which, to the best of my knowledge, has gone unnoticed in
the literature, and which as you will see, must obviously bear a
great deal on the capacities of birds thatdeal with low temperatures

329

WEST

and also bear a great deal on the rates at which they can or do
adjust to lowering temperatures. We talk about feather tracts,
and apteria, but I invite you to trap a Snow Bunting in late May
and rip all its contour feathers off. In other words, rip the feathers
off the pterylae, that is, the feather tracts. What will you have
left? You will have a body which is covered with a dense down
which covers the apteria.

I have prepared finches from high latitudes and low latitudes,
and there is a striking trend. The lower latitude finches are
genuinely naked on their apteria, but the high latitude ones which
I have examined, the Golden Crowned Sparrow, the Lapland Long-
spur, and the Snow Bunding, are not. This must be a relevant con-
sideration to those interspecific differences on Dr. West's graphs
which seem puzzling.

Another little detail which is perhaps a little more esoteric
is this; in larger passerines like the Steller's Jay, there is a
highly modified, stiff, hair- like feather, which is distributed
over the body. What is this for?Iam not sure that I have an answer
to what it is for, and I have not said anything about this in print
because there is such a depressingly large European literature
on plumage that I have not gone through it yet to see if somebody
has said something on the matter. But these stiff, hair-like feathers,
distributed over the body on a large passerine which has a very lax
and dense plumage, could increase the efficiency of spacing of the
plumage when the bird expands it and contracts it; and the presence
or absence of these hair- like feathers must be another little detail
that has to be plugged into these considerations of why Dr. West's
curves deviate as they do.

WEST: What is the distribution of those?Are these filoplumes?

PITELKA; Yes, filoplumes. They are regularly distributed
among the contour feathers.

WEST: How about on the smaller birds, sparrows?

330

BIRD ADAPTATIONS

PITELICA: I do not think they are present. I am not sure about
that. I have not looked for them, actually. If they are there at all,
they are certainly not easily noticed.

HUDSON: I would like toadd toDr. Johansen's, Dr. Morrison's,
and Dr. West's remarks with respect to the lower critical tempera-
ture. In our laboratory we have had a number of cases in which we
have been unable to get nice extrapolations of the metabolic rate to
the appropriate body temperature, and in some cases we get extra-
polated body temperatures as high as 44 C and 45 C. At the same
time, using the same techniques and animals from similar areas, we
are also able to successfully extrapolate, so that we are reasonably
certain that it is notour technique, but have the feeling that possibly
there was some change in conductance going on even below the lower
critical temperature.

PROSSER: May I ask just one more question about the computed
insulation curve? If similar curves are constructed for mammals,
what would be the shape and the value of the index that Dr. West
presented?

HART; In lemmings, during activity there is a large variation,
but during rest in mice at least, the variation of insulation v/ith tem-
perature was similar to the hypothetical insulation curve for birds
except that it conforms more closely to the critical temperature.
In other words, the curve becomes flat at higher temperatures. If
body temperature is constant and the correlation between metabolism
and temperature extrapolates to zero at a value higher than body
temperature, then insulation would increase wath fall in temperature
in a manner comparable to that seen in birds.

HUDSON; And these are also animals which have, from general
appearance, reasonably good coats, have metabolic rates that are
approximately what you would expect from their body size, but also
have lower critical temperatures that are extremely high, that is
above 30 C. So that on the basis of general judgment you would
expect the animal to have the capacity to continue his regulation by
physical means through much lower temperatures than he does.

331

WEST

IRVING: It is so hard to figure on some of these things in
examining the metabolism of the Brant in summer and winter.
The Brant is a big bird weighing a kilogram and a half, and with
feathers so thick that when you grasp hold of him you cannot feel
through the underlying bird or meat, and yet its metabolic rate
begins to increase at just about freezing temperature. It is a bird
with the thickest insulating feather cover that you can find, and yet
he does not use it for insulation. Of course the Brant, like the
other water fowl, follow the open water throughout the year and
perhaps they do not need any more insulation, but that does not
give any physical explanation. In fact, the explanation is probably
physiological rather than a matter of simple feather thickness.

MORRISON: As far as changing body temperature goes, of
course this relation is related to difference between body tempera-
ture and ambient temperature.

IRVING: Are you not working in a limited range of animal size
where the measurements are difficult? Perhaps life itself is diffi-
cult for animals of these very small dimensions and they have to
resort to metabolic subterfuges which are legitimate for them but
illegitimate from our point of view. They are difficult to examine
because you are looking at the 10 to 100 gram or so size range.
Perhaps some clarification would come if you went to larger birds;
I think your only representative above 100 grams was the pigeon,
was it not?

WEST: Yes, I was concerned with the small wild birds, most
of the passerine group.

PROSSER: Are you saying that this temperature- metabolism
curve rises continuously as you go to lower temperatures, and
that you have no thermo-neutral zone or critical temperature for
smaller birds, while in a larger bird there is a critical temperature?

WEST: Yes.

332

BIED ADAPTATIONS

IRVING: I do not say that these deviations from what we expect
to be the rule, or what we would like to hope would be a rule, are
incorrect. I am sure they are correct, but they may represent the
deviations of birds on account of size, as small mammals deviate.

333

RACIAL VARIATIONS IN HUMAN RESPONSE TO
LOW TEMPERATURE

Frederick A. Milan

The investigations of racial variations in thermoregulation have
been based on the premise that races of mankind inhabiting regions
characterized by seasonal ordiurnal periods of low temperature are
biologically adapted* to life in these environments. It has been
assumed that thermoregulation in a race living in regions of low
temperature may function differently from that of a race in a warmer
climate. These studies of racial variation in physiologic function are
attempting to accomplish the task recommended for biologists by
Prosser (1959). This task is to assess critically the functional adap-
tive features (includingbehavior) that can describe the unique fitness
of a species to its environment.

According to the inferentialevidenceof archaeology and paleon-
tology, Homo sapiens evolved in tropical Africa and Eurasia, and his
original geographical distribution resembled that of the present day
Old World non-human primates. Earlyhominidspresumably lived in
a thermally neutral environment. It has also been clearly shown by
finds in Tanganyika that prehominids had already acquired tools and
fire before Homo sapiens evolved as a species (Washburn, 1959).

It is obvious that man erects a cultural screen of dwellings,
clothing, living techniques, and behavioral adjustments between him-
self and his environment. Except at high altitudes (as on the Bolivian
altiplano, for example) where little can be done about low oxygen
tension by preliterate peoples, man's cultural screen effectively
ameliorates environmental stress and is an essential part of his
external temperature regulation. This cultural carapace must be
considered in enumerating human groups chronically exposed to low
temperatures.

*A biological adaptation is "...an aspect of the organism that promotes its gen-
eral welfare, or the welfare of the species to which it belongs in the environment
it usually inhabits" (Simpson et al., 1957).

335

MILAN

Experimental data are available which describe some aspect of
thermoregulation in peoples as various as Eskimos, Arctic Athapas-
cans, South American Indians (the Alacaluf), Norwegian Lapps, Aus-
tralian aborigines, African Bushmen, American Negroes, European
Norwegians, and a host of North American White controls. In this
paper these data will be reviewed and the results of my own experi-
ment which was designed to further investigate thermoregulation
and to compare tissue insulation in Anaktuvuk Eskimos , Athapascans ,
and Caucasian soldiers will be presented.

A HISTORICAL REVIEW AND LITERATURE SURVEY

The Eskimo

Possibly because of their geographical location, the earliest
studies were undertaken on the Eskimos. The Eskimos are a geneti-
cally, linguistically, and culturally homogeneous population living
along the coasts of Greenland, Northern North America, and a small
area of Siberia. It is apparent that they have been in the Arctic for a
considerable length of time. The Denbigh Flint Complex of Norton
Sound, presently the oldest cultural assemblage on the Alaskan side
of the Bering Strait, has been dated at between 2500 and 3000 B.C.
Eskimo type cultures have succeeded one another in this area from
about 500 B. C. to the present (Giddings, 1960). Material from the
bottom layers of a midden at Nikolski, Umnak Island, in the Aleu-
tians has been dated ataboutSOOO B.C. (Laughlin and Marsh, 1951).

A folk migration of expert arctic travelers, carriers of the
Thule culture, wandered from the Bering Strait 6,000 miles to
Greenland about 1,000 years ago and caused the present linguistic,
racial, and cultural homogeneity over this vast area (Collins, 1954).
The Thule people replaced the earlier arrivals, the Dorset people,
who had been in the eastern Canadian Arctic and Greenland since
about 675 B. C, (Larsen and Meldgaard, 1958). The fiist European-

336

HUMAN RACIAL PESPONSES

Eskimo contact occurred in 988 A. D. when Eric the Red encountered
the Greenlanders.

The main characteristics of the climate of the high Arctic are
year-round aridity, low temperatures and high winds with drifting
snow in winter and cool temperatures and a high incidence of fog in
summer. It has been clearly recognized by physiologists that the
success of the Eskimo in exploiting his environment is due to the
fact that he carries his private microclimate about with him. Never-
theless, it is difficult to understand how one could live in the Arctic
and not suffer occasional cold exposure, and therefore many phys-
iological investigations have been designed to elucidate the more
subtle differences in thermoregulation.

Basal metabolism. August and Marie Krogh(1913) reported that
the Greenland Eskimos were utilizing more than 300 gm of protein
in their diets per day and later suggested to Hygaard (1941) that the
elevated heat production (+13% of the DuBois Standard) of 22 Ang-
magssalik Eskimos of East Greenland may have been due to dietary
factors. An elevated basal metabolic rate has been reported by al-
most all investigators of the Eskimo. Rodahl (1952), who has re-
viewed the early literature, measured surface areas, and measured
the BMR's of 73 healthy Eskimos, concludes that apprehension and
the high protein diet are the reasons for the high BMR. MacHattie
et al. (1960), however, on the basis of the 24 hour metabolic studies
of the night fuel energy fractions in Anaktuvuk Pass Eskimos, con-
sider factors (unknown at present) other than the SDA of protein to
be involved.

It is puzzling to many that the SDA of protein has such long last-
ing post prandialeffects on Eskimo metabolism. Keetonet al. (1946),
however, fed experimental diets high in either protein or carbohy-
drate to 12 male conscientious objectors for 5.5 months and reported
an 18% to 19% increase in metabolism (6 hours after the last meal)
due to the SDA of protein. And Hicks et al. (1934) reported the SDA
of raw meat ingested by Australian aboriginals to be 80% after five
hours.

337

MILAN

Brown et al. (1953) measured BMR's in nine males and seven
females at Southampton Island and reported them to be between 124%
and 130% of normal. They described their subjects as clinically
hypermetabolic but not hyperthyroid in the sense of thyrotoxic. The
suggestions of others that the elevated BMR might be due to anemia,
polycythemia, racial characteristics, unidentified disease, or the
high protein diet were discussed. They have concluded that the high
metabolic rate was not entirely the result of a high protein diet, but
that the diet is merely another manifestation of the effects of the
environment and the food available.

Thyroid metabolism. Gottschalk et al.(1952) measured the pro-
tein bound iodine in seven U. S. soldiers attending an arctic indoc-
trination course at Fort Churchill, seven male Eskimos from South-
ampton Island, and seven Eskimos from Chesterfield Inlet in winter.
There was no change in the soldiers' basal metabolic rate or PBI
due to their arctic sojourn. The Eskimos had significantly higher
values in PBI (4.2 to9.0 microgram percent) than enthyroid patients
in U. S. hospitals.

131
Rodahl et al. (1956, 1957) administered tracer doses of I to

84 Alaskan coastal and inland Eskimos, 17 Athapascan Indians of Ft.

Yukon and Arctic Village, and 19 white controls to assess the role of

thyroid in man during cold exposure. Except for the inland natives,

there was no s^nificant difference in thyroid uptake or urinary

elimination of I or in PBI and no seasonal difference in PBI.

There was no significant difference between natives and whites in

PBI. The Anaktuvuk Eskimos and the Arctic Village Indians had high

and rapid uptakes of I which were related to the low iodine in

their diets and to the hig,h incidence of endemic goiter. A reduction

rsi

in the rateof uptakeof I occurred following supplementation daily
for 3 months of 0.6 mg postassium iodide.

Blood volumes. Brown et al. (1953) measured blood volumes by
dilution of Evans Blue dye and hematocrits in 22 male Eskimos at
Southampton Island. They reported blood volumes to be 124% to 142%

338

HUMAN RACIAL RESPONSES

above normal (normal is 100%). The increase was noted in both the
plasma and in the total red blood cell volume.

Response to extremity cooling. Pecora (1948) studied the

"pressor response" in 23 male Eskimos of Nome and Fairbanks

using a sphygmomanometer and compared the results with those of

similar experiments conducted on 44 Caucasian soldier controls.

o
An arm was immersed in unstirred water with a temperature of 4 C

o
to 5 C. The Eskimo group had a higher basal blood pressure, but

the increase due to the cold immersion was less than in the control

group. In addition, the Eskimos reported less subjective pain.

Brown et al. (1952), by venous occlusion plethysmography,

measured hand blood flow in 22 male Southampton Island Eskimos

and 37 Queens University medical students in room air and in water

o o

baths ranging between 5 C and 45 G. The hand blood flow of the

Eskimos was nearly twice as great as that of the Caucasians in room
air of 20 C. Values were; Eskimos, 8.6 cc/lOO cc tissue/min; con-
trols, 4.7 cc/lOO cc tissue/min. The Eskimo hand flow was greater
at any given water bath temperature.

Brown et al. (1953), by venous occlusion plethysmography,
determined forearm blood flow and measured the temperatures of
forearm skin, subcutaneous tissue, muscle, and rectumsof29 male
Southampton Island Eskimos who were not all racially pure and 37
male Kingston Ontario medical students. In a 45 C water bath, the
blood flow was similar in both groups. Below 45 C the Eskimo
group had a greater blood flow. In water baths below 38 C the
Eskimo forearm muscle temperature was lower as a result of a
greater venous return and consequent cooling of arterial blood.
In the 5 C bath, the Eskimo forearm flow was 3.8 cc/lOO cc tis-
sue/ min in contrast to 1.5 cc/lOO cc tissue/ min in the medical
students.

Page et al. (1953) investigated hand blood flow, subcutaneous
temperatures, muscle temperatures, and rectal temperatures in
Southampton Island Eskimos and a control group of medical students
during heating and cooling of the legs in water baths. During heat-
ing at 42.5 C forearm muscle temperature and blood flow was

339

MILAN

greater in the control group. During cooling of the legs at 10 C the
Eskimos showed little change in blood flow in contrast to the con-
trols who showed a pronounced fall.

Eisner (1960) measured limb blood flow in six Anaktuvuk
Eskimo males and athletic and non-athletic Caucasians. Limb blood
flow was somewhat elevated at rest in the Eskimos.

Meehan (1955) measured the temperature at the base of the nail
of the right index fingers of hands immersed for 30 minutes in stir-
red ice water in 52 Alaskan natives (14 from Barter Island, 24 from
Fort Yukon, and 14 from Gambell), 38 American Negroes, and 168
Caucasians. During the last 25 minutes, the Alaskan natives main-
tained the highest mean finger temperatures. Only 5% of the Alaskan
natives, in contrastto 21% of the Caucasians and 62% of the Negroes,
had mean finger temperatures of 0 C during the last 25 minutes.

Pain sensation. Meehan et al. (1954) investigated the "warm"

pain threshold in 26 Athapascan Indians, 37 AnaktuvukPass Eskimos,

and 28 white controls. A 3- second thermal stimulation on the back of

o o

the hand was used. The threshold was about 43.1 C to 43.7 C, and

there was no significant difference between the groups.

Differential sweat rates. Rodahl et al. (19 57) investigated the
comparative sweat rates of six male Anaktuvuk Pass Eskimos and
five male Caucasian controls exposed nude for 3 hours to several
ambient temperatures during exercise (15 minutes at 3.5 mph on
an 8.6% grade) and during a 3 hour walk wearing standard clothing
at -23 C. They found that at all ambient temperatures the resting
metabolic rate for the Eskimos exceeded that of the Caucasian group
by over 30%. The average skin temperature of the Eskimo tended to
be higher at all environmental temperatures below 35 C. The
Eskimo skin, particularly of the forehead and back, had a greater
concentration of active sweat glands at 33 C environmental tem-
perature. During the treadmill exercise the group differences were
not significant, although the Eskimo group had to dissipate 21% more
heat to maintain the same body temperature. According to nude

340

HUMAN FACIAL BESPONSES

weight loss, the Eskimos' sweat rate was twice as great during
the 3 hour walk at -23 G. The elevated metabolism of the Eskimo
required that they increase total body heat loss to maintain thermal
equilibrium, and the sweating mechanism accounted for the dissipa-
tion of 91% of the excess heat. Respiratory heat loss (Eskimo 5.1
Cal/m /hr; White 3.4 Gal/m /hr) was constantly greater in the
Eskimos because of a higher minute volume.

Kawahata et al. (1961) counted active sweat glands during maxi-
mal sweating at an ambient temperature of about 41 G in Gauca-
sians, Negroes, and eightfemale and two male Eskimos of Anaktuvuk
Pass, Alaska. The rank order in total number of sweat glands be-
ginning with the lowest number was Caucasian females, Caucasian
males, Eskimo females, Negro males, Eskimo males. The rank
order in number of sweat glands per cm of body surface area was
Caucasian females, Eskimo females, Caucasian males, Eskimo
males, Negro males.

Response to whole body cooling. Adams et al. (1958) exposed 6
Anaktuvuk Eskimo males, seven American Negroes and seven
Caucasian soldier controls nude for 120 minutes to an air tempera-
ture of 17 C. The Eskimos had a higher metabolic rate in the con-
trol period (Eskimo 50, White 40, Negro 38 Gal/m /hr). The average
rise in metabolism due to shiveringwas similar in the Eskimos and
soldier controls (22 Cal/m /hr). The Eskimo group had higher core
and shell temperatures during cooling and shivered, as did white
controls, when the average skin temperature reached 29.5 C.

Tissue conductance. Covino (1960, 1961) studied thermal regula-
tion in five Pt. Barrow Eskimos and five controls (including one

o o

American Negro) immersed in a bath calorimeter at 35 C and 33

C. The Eskimos produced more heat and lost more body heat dur-
ing the immersion periods and their rectal temperatures fell to
lower levels. There was no difference in digital blood flow. The
greater tissue conductance was related to the significantly smaller
percentage of body fat in these Eskimos.

341

MILAN

Adipose tissue. Govino (1960, 1961) and Eisner (1960) report
that the body fat content of all Eskimos is characteristically low.

Eskimo summary. Possibly owing to dietary factors (Rodahl,
1952), Eskimos have a 20% to 30% higher basal metabolism than
Caucasians when S. A. (Brown et al., 1953; MacHattie et al., 1960)
or lean body mass (Govino, 1960) is used as a reference standard;
and this difference is maintained during shivering (Adams et al.,
1958) and exercise (Rodahl et al., 1957). At high ambient tempera-
tures or during a hard walk in the cold, sweating accounts for most
of the dissipation of the excess heat (Rodahl et al., 1957). In addi-
tion, a higher minute volume results in a greater respiratory heat
loss (Rodahl et al., 1957). During a whole body cold stress, the
"critical temperature," which causes a rise in metabolism by
shivering, is the same in Eskimos and Caucasians (Adams et al.,
1958). When either legs or hands are cooled in water, blood flow
is greater in the hands and forearms of Eskimos (Brown et al.,
1952; Brown et al., 1953; Page et al., 1953; Meehan, 1955). The
threshold for "heat" pain is the same (Meehan, 1954) but there are
suggestions of a difference for "cold" pain. Tissue conductance in
cold water immersions is greater because of a significantly smaller
percentage of body fat and a higher heat production (Govino, 1960,
1961; Eisner, 1960). The Eskimo has a higher metabolic heat pro-
duction which requires a greater potency of heatdissipation mechan-
isms. According to Hardy (1961) it is body temperature which is
regulated by the hypothalamus, not the energy flux through the
organism.

Athapascan Indians

The antiquity of the northern Athapascan tribes is presently
unknown. The exigencies of a nomadic existence in a subarctic
environment imposed certain arbitrary population controls; few
permanent camps were established, and artifactual remains are
sparse. They presently inhabit interior Alaska and Canada, where
a continental type climate results in seasonal extremes in tempera-
ture. According to Sapir (1936), Newman (1954), and Kraus et al.

342

HUMAN RACIAL RESPONSES

(1956) language affinities between the Apaches and the Northern
Athapascans indicate that the former migrated southward 400 to
600 years ago.

Response to whole body cooling. Meehan (1955) measured
metabolic rates, and surface and rectal temperatures of nine male
Fort Yukon natives and Caucasian controls clad in a light under-
wear suit and exposed for 90 minutes to an air temperature of
6 G to 7 C. Initial resting metabolic rates and respiratory quo-
tients were close to basal values and were the same in both groups.
In the cold room, the natives shivered more and had a significantly
higher metabolic rate increase (142±22%) after 90 minutes than
did the Caucasian controls (77±11%). The hands and feet of the
natives were significantly warmer and the Caucasians incurred a
greater total heat debt.

Irving et al. (1960) measured the sleeping metabolism, rectal
temperatures, and skin temperatures of eleven male Old Crow
Indians and seven Caucasian controls. These parameters were
measured during 7 hours of warm sleep and 7 hours at 0 C with
about 1 clo insulation. Initially, the Indian basal metabolism was
approximately 14% higher than Benedicts' standards. By using
"lean weight" as a reference, the two groups did not differ in meta-
bolism. During the cold exposure the average elevation of meta-
bolism in the Indian subjects was 29% and in the Caucasians 32%.
During the warm nights the Indians and controls were awake 12%
and 13% of the time respectively. During the cold nights the
Indians were awake 49% and the Caucasians 69% of the time. Dur-
ing both warm and cold nights the Indians lost more heat from
body storage. However, the skin temperatures of the Indians and
Caucasians did not differ significantly, and no evidence was found
of adaptation in metabolic rate of thermal reactions.

Eisner et al. (i960) , in order to investigate seasonal differences
in the Old Crow population, restudied eight male Indians in the
spring. Metabolism, skin temperatures, and rectal temperatures
were measured during sleep at 0 C to 3 C with 1 clo insulation.
Basal oxygen consumption of four natives was approximately 10%

343

MILAN

above DuBois standards. Metabolism increased 30% during the night;
and skin and rectal temperatures declined as in the previous study.
It was concluded that meager evidence for general metabolic and
thermal adaptation was found by methods which revealed important
differences in naked Australians and warmly dressed Lapps.

Response of extremities to cooling. Eisner etal. (1960) studied

the transfer of heat via the circulation of blood to the hands of Old

Crow Indian males. In the first experiment nine Indians and eight

Caucasian controls immersed their right hands in 5 C water for 30

o
minutes after a control period of 30 minutes in 30 C water. These

experiments were done with the subjects clothed in a warm room and
unclothed in a warm room. The Indian hands transferred a signifi-
cantly greater amount of heat to the water in both the warm and cold
environments. In a second experiment, six Indians and five controls
immersed the right hands in ice water. The Indian group had a more
rapid rewarming and suffered less pain.

Meehan (1955), quoted earlier, reported warmer finger tem-
peratures in ice water in Fort Yukon natives as compared to those
of Caucasian controls.

Physical fitness. Anderson et al. (1960) investigated the physi-
cal fitness of eleven male Indians from Old Crow. Respiratory gas
exchange and heart rate during steady state exercise were meas-
ured. The response of extra ventilation to a standard exercise load
was also determined. The results showed that the Indians occupied
an intermediate position between young sedentary Norwegians and
Norwegian athletes in their fitness for work.

Athapascan Indian summary. Basal metabolic rates are the
same in Athapascans as in Caucasians when compared to "lean
weight" (Irving etal., 19 60), but 14% higher than Benedict's standard,
and 10% above DuBois standard values (Eisner et al,, 1960).

Indians showed no difference in metabolic and thermal reactions
when compared to Caucasian controls that were exposed to low

344

HUMAN FACIAL RESPONSES

temperatures during sleep in the fall (Irving et al., 1960) and the
spring (Eisner et al., 1960).

Indians, even when in negative heatbalance, have warmer hands
in cold water than Caucasian controls (Eisner et al.,1960) and
warmer fingers in ice water (Meehan, 19 55).

Physically the Indians are lean (Irving et al., 1960) and occupy
an intermediate position between young sedentary Norwegians and
Norwegian Olympic athletes in their fitness for work (Anderson et
al., 1960).

The Lapps

Lappland, which has no political existence, consists of the for-
ested highlands of northern Sweden, tundra- cove red areas of north-
ern Finland, Norway's coastalprovinceofTroms and Finnmark, and
much of the Russian Kola Peninsula. The Lapps presently number
about 35,000. They have national allegiance to the country where they
are domiciled and share this country, with a larger population of
Finns, Norwegians, Swedes, and Russians with whom they have been
interbreeding for centuries. Historical accounts seem to indicate that
the Lapps were originally hunters who in about 1500 A. D. became
reindeer domesticators , having learned this art from the Samoyedie
peoples to the east. According to a number of blood surveys, the
Lapps have apparently reached their present genetical constitution
through long isolation as a relatively small population. Norwegian
Lapps have in recent centuries received a larger genetical contri-
bution from the outside than have the Swedish Lapps.

Russian Lappland, Finnish Lappland, and the part of Swedish
Lappland situated above the Arctic Circle en joy aboutthe same tem-
peratures as the southern half of the Labrador peninsula because of
the amelioratingeffectofthewarm water of the Gulf Stream upon the
climate (Milan, 1960, from published sources).

The information on the physiology of the Lapps is restricted to
that obtained from studies of reindeer nomads and villagers from
Kautokeino in northern Norway.

345

MILAN

Critical temperature. Scholander et al. (1957) determined the
"critical temperature," i. e. the lowesttemperature at which a rest-
ing metabolic rate maintained a constant body temperature, in nine
male migratory Lapps from Kautokeino and three male Norwegian
controls. The nude subjects bicycle on an ergometer wheel in a
temperature regulated room. Rectal temperatures and oxygen con-
sumption were monitored. The intersect of resting values of oxygen
consumption and values in the cold occurred at approximately 27 C,
and this was taken as the critical temperature. The subjects per-
ceived a fall inrectaltemperature as smallas 0.2 C. Critical tem-
peratures were the same in both groups.

By measuring skin temperature under the clothing of Lapps out-
of-doors, it was determined that they live within a warm micro-
climate.

Response to whole body cooling. Lange Andersen et al. (1960)
measured skin and rectal temperatures and metabolism in 14 male
Lapps from Kautokeino and five male Norwegian controls during 8
hour exposure to 0 C while sleeping nude with about 1 clo insula-
tion. The Lappish subjects consisted of five settled villagers and nine
reindeer nomads. During the cold exposure, most of the reindeer
nomads slept well with no obvious shivering. The controls slept
poorly and suffered from surface cooling, especially in the legs and
feet. The nomads and controls had similar skin temperatures, but
the nomads lost more heat from the body core because of a lower
metabolic heat production. The Lapp villagers were intermediate
between the controls and nomads in their responses.

Response to extremity cooling. Krog et al. (I960) measured
hand blood flow in a venous occlusion plethysmograph at various
temperatures and hand heat loss and finger temperatures in 0 C
stirred ice water. The subjects were 13 male Kautokeino Lapps,
10-12 Lofoten Island fishermen, 6-11 Gothenburg medical students,
and 4 authors. Maximum hand blood flow at 40 C was similar in
all subjects. Hand blood flow at 10 C and 20 C was the same in

346

HUMAN FACIAL RESPONSES

all subjects. The blood flow values reported in this study are con-
siderably higher than those reported by Brown et al. (1952); these
authors suggest that Brown kept his subjects cooler, and their hand
flows were influenced by vasoconstrictor fiber activity. During im-
mersion in 0 G water the temperatures of the cold habituated sub-
jects (Lapps and fishermen) were similar to those of the controls.
There was, however, an earlier onset of vasodilation in the Lapps
and fishermen. Although the cold habituated subjects experienced
less pain and discomfort, two Lapps and three fishermen fainted
during the experiment. The results of the study did not support the
hypothesis that cold habituated individuals possess a purely local
vascular adaptation resulting in a greater blood flow through the
hands .

Lapp summary. Kautokeino Lapps, when compared with Nor-
wegian controls, slept well with no obvious shivering during a night
exposed to an air temperature of 0 C and lost more heat from the
core because of a lower metabolic heat production (Lange Andersen
et al., 1960). Paradoxically, the criticaltemperature is the same for
Lapps and Norwegian controls (Scholander et al., 1957). Hand blood
flows at various temperatures and finger temperatures inO C water
are the same for cold habituated nomadic Lapps, Lofoten Island fish-
ermen, and controls, but the former two groups vasodilated earlier
and reported less pain when vasoconstricted.

The Indians of Southern Chile

The aboriginal inhabitants of the islands in and around the
Straits of Magellan in southern Chile and Argentina became famous
for their cold hardiness through the writings of Charles Darwin, who
visited this region in the H. M. S. Beagle. The Fuegian tribes con-
sisted of the Chono, Haush, Ona, Vaghan, and Alacaluf, Only the
physiology of the Alacalufs has been investigated.

The Alacalufs formerly inhabited the islands from the Gulf of
Penas as far south as the northwest part of Isla Grande on Tierra
del Fuego. This habitat is an isolated and densely vegetated region

347

MILAN

with 120 inches of precipitation, which falls as snow in winter. It
has been estimated that the Alacalufs numbered between 3500 and
4000 in 1850. Presently there are about 50 Alacalufs who are settled
on Wellington Island (Bird, 1946; Cooper, 1946).

Response to whole body exposure. Hammel etal. (i960) studied
nine male Alacalufs exposed for 8 hours during the night to an air

0 0

temperature of 2 G to 4 C and six male Alacalufs during sleep
while comfortably warm. Oxygen consumption and skin and rectal
temperatures were measured. No controls were used. Atthe begin-
ning of the night the metabolic rate was about 60% above the basal
values for a standard white European of the same weight, height, and
age. In similar circumstances a white would be no more than 20%
above basal values (Hammel et al., 1959). The average metabolism
during the cold nights was indistinguishable from that during the
warm nights, except for occasional bursts of shivering, and meta-
bolism gradually decreased over the 8 hour period. The Alacalufs
resembled the Indians of Old Grow in their metabolic responses,
which were nearly twice as great as those measured in the Aus-
tralian aborigines during a similar exposure. Rectal temperatures

were about the same as those measured in European controls, while

o o

skin temperatures were about 1 C lower. Thefeet were about 2 C

to 3 G warmer. Measurements of tissue conductance in the Alaca-

hifs showed complete vasodilation in these subjects when sleeping

warm. During the cold nights, tissue conductance was halved, but it

was still 30% higher than in the Australian aborigines.

Responses to extremity cooling. Eisner in Hammeletal. (1960)

measured the heat output of the feet and hands of Alacaluf Indians

and three white controls in cold water. The hands and feet, after an

o o o

initial immersion in 30 G water, were placed in 5 G and 10 C

water, respectively. The range ofheat output in these subjects over-
lapped that of white controls. Whereas the Alacaluf men and women
reported no pain, the controls experienced intense pain in the feet
during the immersion.

348

HUMAN RACIAL EESPONSES

Alacaluf summary. The Alacalufs studied in the field have an
elevated basal metabolism, and during an 8 hour moderate cold
exposure their metabolism is virtually indistinguishable from that
measured while warm (Hammel et al., 1960). During cooling of the
feet and hands, heat loss was similar to that of white controls but
pain sensation, reported as intense in the controls, was absent.

The Australian Aborigines

The land connection between Australia and the mainland of Asia
was submerged during the late Pleistocene. Australia thenbecame a
refuge area for archaic forms of plants, animals, and men. It has
been estimated that the continent has been inhabited for about 15,000
to 20,000 years, and its human population has been described as tri-
hybrid in origin, representing an amalgamation of archaic Cauca-
soids, Veddoids, and Australoids (Birdsell, 1950). This human popu-
lation lived in virtual isolation until the first European settlement
was established in Botany Bay in 1787. Atthe time of first European
contact, the aborigines numbered about 250,000 in some 500 tribes,
and they were naked (Elkin, 1954). In 1956 there were an estimated
60,000 aborigines in the population at large (Smythe et al., 1956).

Winter night temperatures in Central Australia fall to freezing
or below, and the night sky radiation temperature is about 20 C
lower. The aborigines who formerly slept naked on the ground be-
tween small fires were chronically exposed to cold.

Sir Stanton Hicks et al., (1931, 1933, 1934, 1938a, 1938b) and
Goldby et al. (1938) initiated the pioneer studies of temperature
regulation in the aborigines. Morrison(1957), while studyingmarsu-
pials in Central Australia, measured aboriginalbody temperatures.
Scholander et al. (1958) and Hammel et al. (1959) have used more
precise methods in extending and confirming the early data.

Observations during sleep in the natural state. Hicks et al.
(1934) measured oxygen consumption and skin temperatures in
sleeping male natives in Central Australia. They found that the meta-
bolism of the natives was not elevated by the cold of early morning

349

MILAN

and that skin temperatures were low. They postulated a more effec-
tive vasomotor control than that of civilized individuals. After the
ingestion of raw meat, the SDA of protein resulted in an 80% rise in
metabolism after 5 hours. The RQ was measured as 0.7 in fasting
subjects and moved toward unity after a meal.

Morrison (1957) used a StoU-Hardy radiometer to measure skin
temperatures in sleeping aborigines at Haast's Bluff in Central
Australia. He concluded that the aborigines had a lower sensitivity
to cold, which allowed them to sleep despite low body temperatures.

Scholander et al. (19 58) studied the Pitjandjara tribe which in-
habits the deserts of Central Australia. Two natives and two Euro-
pean controls slept naked "proper bush style," lying on the ground
between two fires in winter. Neither Australians nor Europeans ele-
vated their oxygen consumption, although the Europeans were uncom-
fortable and did not sleep well. The natives stoked their fires three
to ten times while the Europeans stoked eleven to fourteen times.
The natives tolerated a lower average skin temperature.

In a second experiment four Europeans and six natives slept

naked in a bag of 1.9 clo insulation on a canvas cot under a thin

^ o o

radiation shield. Night temperatures were between 5 C and 0 C.

The metabolism of the natives fell below basal values during the
night, whereas the Europeans elevated their metabolism by bursts
of shivering. The natives slept, while the European controls were
kept awake by cold feet, although the natives had lower skin tempera-
tures. It was concluded that the natives had adapted both their tech-
nology and physiology to withstand chronic cold exposure.

Hammel et al. (1959) returned to study the Central Australian
natives in summer to see if the differences reported by Scholander
et al. (1958) were seasonal. In addition, natives from the tropical
north coast with a history of little cold exposure were studied. Eight
male Pitjandjara, nine male tropical natives, and seven male Euro-
pean controls were exposed during sleep in a 1.7 clo bag in a refrig-
erated meat van for 8 hours at 5 C. The metabolism of the Pitjand-
jaras was lower than that of the European controls. The tropical
natives were intermediate in metabolic response. The Pitjandjaras

350

HUMAN RACIAL PESPONSES

allowed greater cooling of the core and shell, their thermal conduc-
tance was significantly less, and their average skin temperatures
were considerably lower. The low tissue conductance in the tropical
natives resulted in skin temperatures which were intermediate be-
tween those of the Europeans and Pitjandjaras. The rectal tempera-
tures were the same in the tropical natives and European controls.
It was concluded thatthe Australian aboriginals had an inborn ability
to tolerate greater body cooling without recourse to metabolic com-
pensation and that this tolerance could be increased by prolonged
exposure to cold.

Australian summary. Australian aborigines lying naked on the
ground find low skin and rectal temperatures compatible with sleep
(Hicks et al., 1934 and Morrison, 1957). Central Australian abori-
gines, when contrasted with European controls in a moderately cold
sleeping environment, do not elevate their heat production despite
low skin and rectal temperatures either in winter (Scholander et al.,
1958) or summer (Hammel et al., 1959).

The American Negroes

American Negroes were transported as slaves from the old
empires of Ghana, Melle, and Songhay in West Africa. The Negro-
American population is by no means pure, and it is considered a
race in the process of formation by several recent authors (Goon
et al., 1950).

Responses to whole body cooling. Rennie et al. (1957) exposed
eight male Caucasian soldiers and eight male American Negro
soldiers for 90 minutes to -12 C in summer and winter. Subjects
were clothed except for hands and fingers. The Caucasians had a
higher heat production, and the increase in metabolism was delayed
in the Negroes. After 70 minutes the Negro rectal temperature was
significantly lower. Although the average skin temperature was the
same, the Negro hands and feet were colder.

351

MILAN

Adams et al. (1958) contrasted the metabolic and thermal res-
ponses of six male Eskimos, seven male Negro soldiers, and seven
male Caucasian soldier controls exposed nude for 120 minutes to
17 C. While the Eskimos and Caucasians shivered at a mean skin
temperature of 29.5 C, the Negroes did not shiver until their skin
temperatures reached 28 C. Skin temperatures were the same in
the Negro and control groups, but the metabolic response was
greater in the latter.

lampietro et al. (1959) matched 16 male American Negro sol-
diers with 17 male Caucasian soldiers for percentage fat, height,
weight, etc. and exposed them nude for 2 hours to 10 C. Metabolic
responses were the same. Although the difference between groups
in average skin temperatures approached significance after 100
minutes (Negroes were 0.8 C lower), other temperatures were the
same.

Response to extremity cooling. Meehan (19 55) measured tem-
peratures of index fingers immersed for 30 minutes in stirred ice
water in 52 Alaska natives, 38 American Negroes, and 168 Cauca-
sians and reportedthat Negroes maintained the lowest temperatures,
lampietro et al. (19,59) measured temperatures of fingers in ice
water in 16 male Negro soldiers and 17 male Caucasian soldiers.
The white subjects had higher finger temperatures, and the "hurting"
reaction was more pronounced.

Negro summary. The metabolic and thermal responses of

American Negroes were reported tobedifferent from those of white

controls during a standardized cold stress of -12 C while clothed

o
(Rennie et al., 1957) and 17 C while nude (Adams et al., 1958) but

the same when nude at 10 C (lampietro et al., 1959). The fingers

of Negroes immersed in ice water are cooler than those of white

controls (Meehan, 1955; lampietro et al., 1959).

The Bushmen

Presently the Bushmen number approximately 55,000. They

352

HUMAN RACIAL BESPONSES

occupy a small fraction of their former territory and are found in
South West Africa, Bechuanaland Protectorate, Angola, Rhodesia,
and the Republic of South Africa. They are hunters and gatherers,
lighter in color than their Bantu neighbors, and speak a Click lan-
guage. In physical appearance they are short of stature (4 feet 9
inches to 5 feet 4 inches) and have a number of anatomical infantile
features (Tobias, 1961).

The Bushmen were formerlydistributedover much of southwest
Africa but are presently confined to the high plateau of the Kalahari
Desert at altitudes between 3000 and 5000 feet. Here the winter night
climate is sufficiently cold to be stressful for a habitually naked
people.

Response to whole body cooling. Wyndham etal. (1958) measured

the skin and oral temperatures of two male Bushmen and two white

South Africans sitting nudefor two and one half hours. Ambient tem-

o o

peratures ranged between 10 C and 15 G. The oral temperatures

of the Bushmen were lower. The skin temperature of one bushmen

sleeping naked under his cloak next to a fire was measured for 8

hours. Ambient temperatures ranged between 12 C and 13 C. Air

temperatures under the cloak were about 26 C, and temperatures

on the trunk were about 35 G. It was concluded that the Bushmen

have made an intellectual rather than a physiological adaptation to

diurnal temperature changes.

Ward et al. (1960) measured the metabolism and skin and rectal
temperatures in eight male Bushmen and five male European con-
trols exposed naked to the Kalahari Desert night environment. Night
temperatures ranged between 22 C and 2.7 C. A radiation shield
was interposed between the subjects and the night sky. A thermo-
couple on a plastic holder manipulated by an observer was utilized
to obtain skin temperatures. Face masks and a Douglas Bag were
used to sample metabolism intermittently. The metabolic response
in the Bushmen was higher than in the controls, but the percentage
increase related to skin temperature was the same for the controls,
Bushmen, and Norwegians (Ward et al. , 196Q. Rectal temperatures
were similar. The Bushmen's skin temperatures were lower because

353

MILAN

of less body fat. It was concluded that the Bushmen had not adjusted
physiologically to the climate, but that they created a local climate
around them, using the meager available materials.

Bushmen summary. While sleeping on the desert in his native
environment, the Bushman utilizes an artificial microclimate to
avoid cold exposure. Limited tests of skin and oral temperature
decline in response to cold stress revealed no difference between
Bushmen and controls (Wyndham et al., 1960). Bushmen subjected
to moderate cold stress while sleeping nude for short periods have
similar metabolic and thermal responses to those of controls (Ward
et al., 1960).

ARTIFICIAL ACCLIMATIZATION OF MAN TO COLD

The results of experiments undertaken to artificially acclima-
tize man to cola or to study the effects of chronic cold exposure
upon soldiers or arctic and antarctic sojourners, which complement
the findings of cold adaptation in chronically cold exposed natives,
will be briefly reviewed. Extensive and recent reviews of the litera-
ture on the effects of cold on man are those of Burton et al. (1955) ,
Carlson (1954), Carlson et al. (1959) and Hardy (1960).

Scholander et al. (1958) exposed eight inadequately clad male
Norwegian students to low ambient temperatures in the mountains of
Norway for six weeks in September and October. Metabolism and
skin and rectal temperatures were measured at night while the sub-
jects slept with 2 clo of insulation at an air temperature of 3 C.
Their responses to the cold stress while sleeping were contrasted
with thoseof 12 male controls. The acclimatized men had higher skin
temperatures, especially in the feet, and they were able to sleep.
They shivered in their sleep, whereas the controls did not sleep at
all. A slight but transient elevation of basal metabolic rates and a

354

HUMAN RACIAL BESPONSES

2 G to 3 C lowering of the critical temperature occurred in the
acclimatized.

Le Blanc (1956) found a significantly decreased oxygen consump-
tion in cold acclimatized soldiers as compared with that of nonaccli-
matized controls when both were exposed to a series of standard
acute cold stresses. He suggested that acclimatization is associated
with a lowering of the body thermostat to more economical levels.

Milan et al. (1961) studied antarctic sojourners who spent a
year at Little America V. The metabolic rates and the thermal res-
ponses of eight subjects (who served as their own controls), exposed
nude to 17 G air temperature were measured over the year. Mean
body and average skin and foot temperatures increased significantly
over the year, whilethere was a decrease in heat production to meet
the same thermal demands since shivering diminished.

Davis et al. (1961) exposed six male white subjects nude to
13.5 G air temperature in a cold room 8 hours each day for 31 days
(except Sunday) in September and October. At the end of this period,
metabolism remained between 35% and 75% above basal values, but
shivering decreased. Skin temperatures were unchanged.

In a similar experiment, Davis et al. (1961) exposed ten male

white subjects to 11.8 G for 31 days in March. At the end of this

o o

period, rectal temperatures had decreased (37.2 Cto36.7 G) , skin

temperatures were unchanged, and although metabolism was un-
changed, shivering decreased. These authors suggest thattheseare
indications of non-shivering thermogenesis.

Adams et al. (1958) and Heberling et al. (1961) have demon-
strated that elevated skin temperature during cold stress may be a
result of an increase in physical fitness.

Trends

Although it is difficult at first glance to generalize about these
experiments investigating acclimatization and adaptation, there are
certain trends which are apparent:

355

MILAN

(1) An increased ability to draw upon body heat stores.

(2) Vascular changes in the hands and feet in order to maintain
warmer extremities.

(3) A diminution of shivering, a moderate cold stress possibly
related to what Eisner (1960) has termed "habituation."

(4) A transient elevation of the BMR, resulting from an ability
to shiver while sleeping.

Native peoples investigated are either naked or thinly clad
exposed to moderatecold — the Australians, Bushmen, and Alacalufs,
or heavily clothed exposed to extreme cold — Lapps, Eskimos, and
Arctic Athapascans.

These cold adapted peoples show:

(1) A form of insulative cooling with a decreased tissue con-
ductance.

(2) A metabolic sparing with the ability to draw upon body heat
stores.

(3) An elevated basal metabolic rate.

(4) A decreased perception of cold sensation.

(5) An increased peripheral blood flow.

This then brings us to a recent study done in collaboration
with Drs. Hannon and Evonuk.

356

HUMAN RACIAL RESPONSES

A COMPARATIVE STUDY OF THERMOREGULATION
IN ESKIMOS, INDIANS, AND U. S. SOLDIERS

Subjects

The subjects for these experiments were six American white
soldiers, six Alaskan Eskimos, and six Athapascan Indians. Their
physical characteristics are presented in Table I.

Cold Exposure

The soldiers had been in Alaskaless than ten days, had arrived
from training camps in the southern states and, except subject 1,
were all born in the Southern U. S. Their previous cold exposure
was very negligible.

The Eskimos came from the isolated village of Anaktuvuk Pass
in the Brooks Range and earned their livelihood by hunting and trap-
ping land animals. They pursue a relatively vigorous existence in a
cold climate.

The Indians came from the village of Tetlin, Alaska, on the
Upper Tanana River. This is a region of climatic extremes and the
lowest winter temperature in North America has been reported
from this general area. Aboriginally these people were nomadic
hunters; presently they are engaged in trapping and wood cutting,
receive governmental subsidies, and are not as active in the cold
as formerly.

Methods

These experiments were conducted in November, December, and
January. Four and five days after they had arrived at the laboratory
and had been subsisting on a hospital cafeteria diet, duplicate meas-
urements of basal metabolic rates were made on the Eskimos and

357

MILAN

Total

Wt.

Ht.

S.^. S
m

klnfold

Lean Body Wt.

Sub]

Age

Adiposity

Fat

Soldiers

65.8

177.8

1.82

50.7

75.4

179.0

1.93

58.9

77.3

183.0

2.00

60.3

64.3

176.0

1.79

50.8

78.4

178.8

1.96

61.2

93.2

180.4

2.15
Indians

172

55.0

52.7

169.4

1.59

45.9

55.1

168.3

1.62

44.7

65.0

174.0

1.79

55.3

10 JO

171.4

1.82

56.8

70.9

175.2

1J86

54.6

79.3

171.5

1.92
Eskimos

55.5

55.9

159.0

1.56

7.5

48.7

62.1

166.5

1.68

9.9

52.2

61.9

161.0

1.65

6.8

53.9

64.1

164.9

1.70

3.1

60.9

68.7

172.6

1.82

5.5

62.5

64.3

175.2

1.78

6.8

57.2

Table I. Physical Characteristics of Subjects.

358

HUMAN RACIAL BESPONSES

Indians. The subjects were in a basal state, and the measurements
were made on the subjects in their ownbeds immediately after they
had been awakened.

The subjects exhaled through a rubber mouth piece, a one way
plastic valve, and a short length of nibber hose into the portable
MuUer-Franz respirometer described by Lehman (1953), and
Montoge et al. (1958). Aliquot samples of expired air, which were
about 0.3% of the total volume, were passed through Alcoa Alumina
desiccant in a 50 cc glass syringe into a Model C Beckman Oxygen
Analyzer. Expired air volumes at BTPS were reduced to STPD.
Heat production was calculated from the following expression by the
method proposed by Weir (1949):

kcal/hr/m =

V^ X (1.046 - 0.05% O E) X 60
2 E ' 2 '

S. A.

where:

V = minute volume of expired air
E

%0 E = % oxygen in expired air

2
S. A. = surface area in m

Bath calorimeter. The thermoregulated recirculating water bath

calorimeter constructed and previously described by Carlson (1961)

was utilized. It was similar to that used by Burton (1936). The bath

contained 396 liters of water, and its temperature could be regulated

within ±0.1 C. The bath was installed in a room where the room air

o
temperature could be controlled within ±1.0 C. Water temperatures

o o o

selected were 35 C, 33 C and 30.5 G, and room temperatures

o
were maintained about 14 G lower to insure a constant rate of heat

loss. Water and room temperatures were allowed to stabilize for 12
hours. The average amount of electrical energy required to main-
tain the water temperature in the calorimeter was measured at 6

359

MILAN

minute intervals. The factor 0.86 was used to convert watts to
kcal/hr (Handbook of Chemistry and Physics).

The subject reclined in the bath with all except his face im-
mersed in water. The subject's total heat loss was determined with
a correction applied equal to the caloric equivalent of the water
displaced by the subject. Total immersion time was one hour. Al-
though heat production did not equal heat loss during this hour and
true steady state conditions were not achieved, rates of change were
constant during the last 30 minutes, and these data were used. This
period is what Burton (1939) has termed a "dynamic steady state."

Heat production. Heat production was continuously monitored by
the respirometer-oxygen analyzer combination utilized to measure
basal metabolic rates.

Rectal temperature. An indwelling catheter type thermistor was
inserted 10 cm into the rectum and secured to the buttock by water-
proof tape. Temperature^ were measured on a Yellow Springs
Instrument Go. Telethermometer and recorded on the strip chart
of an Esterline Angus Recorder.

Calculation. The Laws of Heat Transfer by Thermal Conduction
have been summarized by Hardy (1949) and are analogous to Ohm's
Law for electrical circuits. The fundamental equation for heat con-
duction in the steady state is:

H = KA(T - T ) X t, gm cal

where:

Hp. = quantity of heat conducted

K = thermal conductivity, a constant

A = area of conducting surfaces
360

HUMAN RACIAL RESPONSES
T and T = temperatures of the warm and cool surfaces

t = time

d = thickness of the conductor

It follows that tissue insulation may be determined from the
equation:

K. =

(^r - T^

i H

where;

o , / 2 /
K = tissue insulation C/kcal/m /hr
1

T = average rectal temperature

T = water temperature
w

2
H = heat loss (kcal/m /hr) measured over 30 minutes

For these calculations it is assumed that skin temperature is
equal to water temperature and that regional gradients over the
body have been obliterated. Although this assumption disregards
the temperature of the boundary layer between the skin- water inter-
face, the assumption has precedents (Carlson et al., 1958; Govino,
1960).

Determination of Body Fat

The skin fold calipers described by Best (1953) were used to
measure the thickness of ten double folds of skin and subcutaneous
fat at the sites recommended by Allen et al. (1956). Percentage of
adiposity was determined from the total skinfold thickness minus 40
mm (the thickness of ten double folds of skin) according to Allen's
formula. Percentage of adiposity was multiplied by 0.62 which
corrected for water in adipose tissue (Brozek et al., 19 54).

361

MILAN

Statistical Treatment

These data were analyzed in a single classification analysis of
variance.

RESULTS

Basal metabolic rates. Average basal metabolic rates and
standard deviations were 47.6 ± 4.41 and 45.4 ± 4.91 kcal/m /hr
for the Eskimos and 42.7 ± 1.70 and 42.2 ±3.92 kcal/m /hr for
the Indians. The basal metabolic rates of the soldiers were not
measured. Lewis et al. (1961) have reported a mean value of
37.4 ± 3.66 kcal/m /hr for 349 measurements on 29 British men
with an average age of 29 years. This figure is close to the average
metabolism of the soldiers in the 35 Cbath. Each hour the Eskimos
produced about 8 to 10 kcal and the Indians about 5 kcal more than
the soldiers when surface area was used as the metabolic reference
standard.

Calorimetric studies. A summary of the data showing the
manner in which the three groups are similar or differ, and the
level of significance attached to these differences is shown in
Table 2. It is of more than passing interest that although there
were no differences in the fall of rectal temperatures, the Eskimo
group, in general, produced and lost the greatest amount of heat
in the water baths at all temperatures.

The relation between an index of "effective thermal conduct-
ivity" and the physiological temperature gradient across which the
energy is transferred is shown graphically for all subjects in
Figure 1. The relation between tissue insulation, actually the recip-
rocal of conductivity, and the temperature gradient is shown in
Figure 2.

362

HUMAN RACIAL EESPONSES

35° C BATH

SOLDIERS INDIANS ESKIMOS E vs I I vs S E vs S

36.9

42.8

50.3

<.02

<.05

<.001

>.10

<.001

-0.21

-0.38

-0.32

>.05

>U)5

.029

.032

.021

<.001

<.05

<.001

33° C BATH

39.4

50.9

54.7

>.10

<.01

<.001

>.50

<.01

-0.46

-0.67

-0.56

>.05

.052

.053

.038

<.O01

>.50

<.001

30.5 C BATH

48.1

52.8

62.8

>.10

>.50

<J05

<M1

<.05

>.05

-0.7

-0.9

-1.1

>.05

.071

.068

.057

<.001

>J05

<.001

2 ,
Table II. Average values of metabolism (M) and heat loss (L) in kcal/m /hr,

fall in rectal temperature (AT J in C and tissue insulation (K.) in C/kcal/m /hr

for the three groups at the three bath temperatures. P values show the levels of

significance which can be attached to the between group differences.

363

MILAN

x +

SOLDIERS

_ +
+

INDIANS

X©

•»-

ESKIMOS

_ X

G G
© ^

X
X X

"xi°

-t- ■♦-

o
u

20
10

©'^ ©
1 1

+
+

"x%©^

1 1

3 4 5

Figure 1. A graphical illustration of the relation between an index of thermal
conductivity and the physiological temperature gradient.

364

HUMAN RACIAL BESPONSES

.080 -

.070 -

.060' -

.050

.040

.030 -

._ .020

.010

.000

^ 0

X ^

X o

■^ %^

% -^

—

x+ +

"'?n

•♦-

SOLDIERS

® )©■**■

INDIANS

-4*

ESKIMOS

1 1

_j 1 1

3 4 5

(Tr-Tw)«C

Figure 2. The relation between tissue insulation and the physiological tempera-
ture gradient.

365

MILAN

In Figure 3 is shown the relation between tissue insulation
and the three bath temperatures. At all temperatures the Eskimos
have significantly lower tissue insulations than the other groups.
The Indians and soldiers are similar to each other and indistinguish-
able at 33 G. The three extrapolated curves intercept at about
36.5 G and at this bath temperature, under the conditions of this
study, tissue insulation would presumably equal zero.

Percent body fat. The mean values for percent fat in the
Eskimos, soldiers, and Indians were 6.6, 15.6 and 12.3. Although
the Indians and soldiers were not significantly different from each
other, the Eskimos were considerably leaner in body build. Coeffi-
cients of the regression line of tissue insulation versus percent
body fat were 0.847, 0.309 and 0.657 at 35° C, 33 C and 30.5 C
respectively. An analysis of covariance was then undertaken in
which tissue insulations were adjusted for their regressions on per-
cent body fat. At 35 C there were no differences between groups.
At 33 C the differences were significant at the .05 level. At 30.5 C
the differences were significant at the .01 level.

DISGUSSION

These experiments show that there are differences in total
body heat loss and heat production between a sample of Eskimos,
Indians, and soldiers immersed in temperature regulated baths.
Although rates of heat loss and production were unchanging during
the 30 minute period of measurement, the most serious criticism
of the results of this experiment concerns non-steady state condi-
tions, for rectal temperatures were falling.

It should be noted that there were no inter- group differences
in the fall of rectal temperatures despite considerable differences
in heat loss and production. In the 33 C bath the differences in

366

HUMAN RACIAL RESPONSES

060 r
.050
~ .040

V,.

w
X

^ .030
u

^ .020

.010 h

.000

+ +

+ X

:C08

SOLDIERS
INDIANS (Duplicate)
ESKIMOS

5 10 15 20

PERCENT BODY FAT

Figure 3. The relation between tissue insulation and bath temperatures.

367

MILAN

total heat loss and production between the soldiers and the Eskimos
were highly significant. The first law of thermodynamics allows us
to say that M ± D = H where M = metabolism, D = heat debt, and H =
the combined losses of heat through conduction, connection, radia-
tion, and evaporation (Carlson, 1954). We can assume that about 8%
of M is evaporative heat loss. In the 33 C bath, then, Eskimo and
soldier average metabolisms are 54.7 and 39.4 kcal/m /hr. By
subtracting 8% of these values we see that the Eskimos have 50 kcal/
m /hr and the soldiers 36 kcal/m /hr available to lose to the
colder bath water without incurring a heat debt. They lost 86 and
66 kcal/m /hr, a difference of 20 kcal, and incurred body heat
debts at the same rates. The differences between heat produced and
total heat loss is then 36 kcal for the Eskimos and 30 kcal for the
soldiers. The Eskimos are characterized by a greater energy flux
through the system (a system which can be described as an iso-
thermal energy converter). In addition a greater mass of the Eskimo
peripheral tissue participates in this cooling. It is tempting to con-
clude that the Eskimos have smaller "cores" and larger "shells."

Others (Carlson et al., 1958; Pugh et al., 1960; Cannon et al.,
1960) have shown that subcutaneous fat is of considerable impor-
tance in reducing heat los^ in cold water. Hatfield et al. (1951)
have reported that the thermal insulation of 1 cm of fat is __^_,
kcal/cm^/sec. The experiments of Cannon et al. (1960) snowed
that fat men achieved a higher maximum tissue insulation in cold

water than thin men. Carlson et al. (1958) have reported tissue

o . / 2 , o ,

insulations that range between 0.10 C/kcal/m /hr and 0.40 C/

kcal/m /hr. Carlson's values are considerably higher than the tissue

insulations reported here and are probably more nearly correct for

steady state conditions above the critical temperature.

368

HUMAN RACIAL KESPONSES
LITERATURE CITED

1. Adams, T. and B. Covino. 1958. Racial variations to a standard

cold stress. J. Appl. Physiol. 12:9.

2. Allen, T. H., M. T. Peng, K. P. Chen, T. F. Haung, C. Chang

and H. S. Fang. 1956. Prediction of total adiposity from skin-
folds and the curvilinear relationship between external and
internal adiposity. Metabolism. 5:346.

3. Andersen, K. L., Y. Loyning, J.D.Nelms, O. Wilson, R. H. Fox

and A. Bolstad. 1960. Metabolic and thermal responses to
moderate cold exposure in nomadic Lapps. J. Appl. Physiol.
15:649.

4. Andersen, K. L., A. Bolstad, Y. Loyning and L. Irving. 1960.

Physical fitness of arctic Indians. J. Appl. Physiol. 15:654.

5. Best, W. R. 1954. An improved caliper for measurement of

skinfold thickness. J. Lab. and Clin. Med. 43:967.

6. Brown, G. M. and J. Page. 1952. The effect of chronic exposure

to cold on temperature and blood flow of the hand. J. Appl.
Physiol. 5:221.

7. Brown, G. M., J. D. Hatcher and J. Page. 1953. Temperature

and blood flow in the forearm of the Eskimo. J. Appl. Physiol.
5:410.

8. Brown, G. M., G. S. Bird, L. M. Boag, D. J. Delahaye, J. E.

Green, J. D. Hatcher, and J. Page. 1954. Blood volume and
basal metabolic rate of Eskimos. Metabolism. 3:247.

9. Brozek, J., J. F. Brock, F. Fidaya and A. Keys. 1954. A skin-

fold caliper estimation of body fat and nutritional status.
Fed. Proc. 13:19.

369

MILAN

10. Burton, A. C. and H. C. Bazett. 1936. A study of the average

temperature of the tissues of the exchanges of heat and
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11. Burton, A. C. 1939. The properties of the steady state com-

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12. Burton, A. C. and O. G. Edholm. 1955. Man in a cold environ-

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13. Carlson, L. D. 1954. Maninacold environment. AAL, APO 731,

Seattle.

14. Carlson, L. D., A. C. L. Hsieh, F. Fullington and R. W. Eisner.

1958. Immersion in cold water and body tissue insulation.
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15. Carlson, L. D., A. Kawahata, K. Miller and R. W. Eisner.

1959. Internal heat of the body. Fed. Proc. 18:23.

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tion to cold. AAL TR 59-18, APO 731, Seattle.

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370

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Thermal and metabolic responses of arcticlndians to moder-
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26. Eisner, R. W., J. D. Nelms and L. Irving. 1960. Circulation of

heat to the hands of arctic Indians. J. Appl. Physiol. 15:662.

27. Giddings, J. L. 1960. The archaeology of Bering Strait. Current

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28. Glaser, E. M., M. S. Hall and G. C. Whittow. 1959. Habituation

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29. Goldby, F., C. S. Hicks, W. J. O'Connor and D. A. Sinclair.

1938. A comparison of skin temperatures and skin circulation
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30. Gottschalk, C. W. and D. S. Riggs. 1952. Protein-bound iodine

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31. Hammel, H. T., R. W. Eisner, D. H. LeMessurier, H. T.

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371

MILAN

32. Hammel, A. T. 1960. Thermal and metabolic responses of the

Alacaluf Indians to moderate cold exposure. W. A. D. D.
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33. Hardy, J. D. 1949. Heat transfer. In Newburgh, L. H. Physio-

logy of Heat Regulation and the Science of Clothing. Saunders,
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34. Hardy, J. D. 1961. The physiology of temperature regulation.

Physiol. Rev. 41:521.

35. Hatfield, H. S. and L. G. C. Pugh. 1951. Thermal conductivity

of human fat and muscle. Nature. 168:133.

36. Hicks, C. S. 1931, 33, 34, 38a. In Carlson, L. D. and H. L.

Thursh. 1960. Human acclimatization to cold. A selected,
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37. Hygaard, A, 1941. Studies on the nutrition and physio- pathology

of Eskimos. Det Norske Videnskaps Akademi, Sk. No. 9,
Oslo.

38. lampietro, P. F., R. F. Goldman, E. R. Buskirk and D. E.

Bass. 1959, Responses of negro and white males to cold.
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39. Irving, L., K. L. Andersen, A. Bolstad, R. W. Eisner, J. A.

Hildes, Y. Loyning, J. D. Nelms, L. J. Peyton, and R. O.
Whaley. I960. Metabolism and temperature of arctic Indian
men during a cold night. J. Appl. Physiol. 15:635.

40. Kawahata, A, and T. Adams. 1961. Racial variations in sweat

gland distribution. Proc. Soc. Exper. Biol, and Med. 106:862.

41. Keeton, R. W., E. H. Lambert, N. Glickman, H. H. Mitchell,

J. H. Last and M. K. Fahnestock. 1946. The tolerance of
man to cold as affected by dietary modifications; protein

372

HUMAN RACIAL PESPONSES

versus carbohydrates, as the effects of variable protective
clothing. Am. J. Physiol. 146:66.

42. Krogh, A. and M. Krogh. 1913. A Study of the Diet and Meta-

bolism of Eskimos. Bianco Luno, Copenhagen.

43. Larsen, H. and J. Meldgaard. 1958. Paleo-Eskimo cultures

in Disko Bugt, West Greenland. Medd. om Gron. 161:2,
Copenhagen.

44. Laughlin, W. S. and G. H. Marsh. 1951. A new view of the

history of the Aleutians. Arctic. 3;175.

45. LeBlanc, J. 1956. Evidence and meaning of acclimatization

to cold in man. J. Appl. Physiol. 9:395.

46. Lehman, G. Praktische Arbeitsphysio logic. Georg Thieme

Verlag.

47. Lewis, H. E., J. P. Masterton and S. Rosenbaum. 1961. Sta-

bility of basal metabolic rate on a polar expedition. J.
Appl. Physiol. 16:397.

48. MacHattie, L., P. Haab and D. W. Rennie. 1960. Eskimo

metabolism as measured by the technique of 24-hour in-
direct calorimetry and graphic analysis. AAL TR 60-43,
APO 731, Seattle.

49. Meehan, J. P., A. StoU and J. Hardy. 19 54. Cutaneous pain

threshold in the Alaskan Indian and Eskimo. J. Appl. Physiol.
6:397.

50. Meehan, J. P. 1955. Body heat production and surface tempera-

tures in response to a cold stimulus. AAL Proj. 7-7951,
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31. Meehan, J. P. 1955. Individual and racialvariations in a vascu-
lar response to a cold stimulus. Military Med. 116:330.

373

MILAN

52. Milan, F. A. 1960. Swedish Lappland: A brief description of

the dwellings and winter living techniques of the Swedish
Mountain Lapps. AAL TR 60-7, APO 731, Seattle.

53. Milan, F. A., R. W. Eisner and K. RodahL 1961. Thermal and

metabolic responses of men in the Antarctic to a standard
coM stress. J. Appl. Physiol. 16:401.

54. Montoye, H. J., W. D. vanHuss, E. P. Reineke and J. Cockrell.

1958. An investigation of the Miller-Franz calorimeter.
Arbeitsphysiol. 17:28.

55. Morrison, P. R. 1957. Body temperatures in aboriginals. Fed.

Proc. 16:90.

56. Page, J. and G. M. Brown. 1953. Effect of heating and cool-

ing the legs on hand and forearm blood flow in the Eskimo.
J. Appl. Physiol. 5:753.

57. Pecora, J. S. 1948. Cold pressor test in the study of acclima-

tization to cold. AAL Rep. 21-01-005, APO 731, Seattle.

58. Prosser, C. L. 1959. The "origin" after a century: prospects

for the future. American Scientist. 47:536.

59. Pugh, L. G. C, O. G. Edholm, R. H. Fox, H. S. Wolff, G. R.

Hervey, W. H. Hammond, J. M. Tanner and R. H. Whitehouse.
I960. A physiological study of channel swimming. Clin. Sci.
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60. Rennie, D. and T. Adams. 1957. Comparative thermoregulatory

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61. Rodahl, K. J. 19 52. Basal metabolism of the Eskimo. Nutrition.

48:359.

62. Rodahl, K. and G. Bang. 19 56. Endemic goiter in Alaska. AAL

TN 56-9, APO 731, Seattle.

374

HUMAN BACIAL RESPONSES

63. Rodahl, K. and G. Bang. 1957. Thyroid activity in men exposed

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64. Rodahl, K. and D. Rennie. 1957. Comparative sweat rates of

Eskimos and Caucasians under controlled conditions. AAL
TR Proj. 8-7951, No. 7, APO 731, Seattle.

65. Scholander, P. F., K. L. Andersen, J. Krog, F. V. Lorentzen

and J. Steen. 1957. Critical temperature in Lapps. J. Appl.
Physiol. 10:231.

66. Scholander, P. F., H. T. Hammel, K. L. Andersen and Y.

Loyning. 1958. Metabolic acclimation to cold in man. J.
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67. Scholander, P. F., H. T. Hammel, J. S. Hart, D. H. LeMessurier

and J. Steen. 1958. Gold adaptation in Australian aborigines.
J. Appl. Physiol. 13:219.

68. Simpson, G. G., C. Pittendrigh and L. Tiffany. 1957. Life.

N. Y., Harcourt Brace.

69. Tobias, P. V. 1961. Physique of a desert folk. Natural Hist.

LXX:17.

70. Ward, J. S., G. A. Bredell and H. G. Wenzel. 1960. Responses

of Bushmen and Europeans on exposure to winter night
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375

MILAN
DISCUSSION

ADAMS; Would your metabolic rates measured in the bath
calorimeter compare with those measured under basal conditions?

MILAN: I would say they would be about the same.

HANNON: Were your basal metabolic rates measured under bed
rest conditions?

MILAN: Yes, and I think, as pointed out by Henderson in 1926,
that there is a relationship between basal metabolic activity and
the circulation. Thus,if you have a slightly higher basal metabolism,
the energy flux is somewhat different, since if you subscribe to the
view of Hardy (1961) the hypothalamus regulates for temperature,
not energy flux.

KLEIBER: I notice that there is a discrepancy from data pub-
lished by Swift,* who reported that his college students began shiver-
ing when their skin temperatures went down to 90 F. But now the
newer data seem to indicate that practically all human beings have
much higher skin temperatures at a critical level than the level at
which the metabolic temperature regulation starts. Is there an ans-
wer to this discrepancy?

MILAN; I do not know.

ADAMS; I might offer one suggestion; the method of taking the
average skin temperature makes quite adifference, if this measure-
ment was calculated in such a way as to give proportionalities to
each site different from conventional standards.

♦Swift, R. W. 1932. The effect of low environmental temperature upon meta-
bolism. II. The influence of shivering, subcutaneous fat, and skin temperature on
heat production. J. Nutr. 5:227-229.

376

HUMAN RACIAL RESPONSES

KLEIBER: I was tempted to conclude that these college students
had a non-shivering metabolic increase, but this is a dangerous
conclusion.

JOHANSEN: I was thinking of the rather profound seasonal
changes in BMR that Yoshimura has reported for his Japanese sub-
jects. Is this not out of proportion with what has been found in other
populations?

MILAN: Yes. Professor Yoshimura said, when he was here,
that he tried to do his studies under strict basal conditions, and
I think the Japanese spend more time and efforts on their measure-
ments of basal metabolism than we do.

PROSSER; WouM you conclude that these higher BMRs in the
Eskimos are not related to specific dynamic action?

MILAN: I should hesitate to conclude anything. I know only that
the experiments of Rodahl (1952) indicated that the high Eskimo
BMR was related to the high protein diet and possibly the specific
dynamic action of this diet. However, the recent experiments of
MacHattie et al. (1960) which investigated the 24 hour metabolism
of the Anaktuvuk Eskimos seem to indicate otherwise. Heat produc-
tion and the energy fraction contributed by catabolism of carbohy-
drate, fat and protein were determined by indirect calorimetry and
measurements of urinary nitrogen. They reported no correlation
between the rate of night metabolism and the amount of protein or
fat fuel energy fraction and suggested that other factors than specific
dynamic action were involved as the cause of the elevated resting
metabolism of these people.

HANNON; In your particular experiments the BMRs are meas-
ured after 5 days on a hospitaldiet. Therefore if the elevated meta-
bolic rate is due to a specific dynamic action it would seem to have
lasted over a period of 5 days.

HART: I wanted to ask about this, too, because we had some
occasion from our Eskimo studies at Pangnirtung to see long last-
ing effects even on somepeople who are living on a white man's diet

377

MILAN

for 4 or 5 days. They still had a 25% elevation in heat production.
Is there any explanation for this? I do not understand how dynamic
action can last so long.

EAGAN: Yoshimura, lida and Koishi (1952)* have shown that
when the protein fraction in the diet is increased there is an increase
in BMR which persists for several days after the protein intake is
reduced to normal. This result was obtained by merely doubling the
protein intake from a normal 75 grams to 150 grams per day.

MORRISON: What is the implication of this? Are the amino acids
stored away and then used gradually? Would the high protein diet
encourage their storage?

HANNON: There is a very confusing picture with respect to the
mechanism of specific dynamic action. We attempted to get at this
one time by infusing an animal intravenously with amino acids to
see how they affected his metabolism. Nothing happened, so we dis-
continued the experiments.

MORRISON: Nothing happened? Are there not reports in litera-
ture showing that infused amino acids give a normal specific dyna-
mic action?

HANNON: This was intravenous infusion where two different
amino acids — glycine and glutamate — were tested. Neither caused
any increase in the metabolic rate. It is interesting that you do
get the specific dynamic action when the animal eats protein. This
might suggest that the mechanism of SDA may have something to
do with gut absorption; I do not really know.

ADAMS: This picture on theSDAeffect of glycine is really con-
fused. Dr. Carlson tried feeding glycine and noted a subsequent

*Yoshimura, H., T. lida and H. Koishi, 1952. Studies on the reactivity of skin
vessels to extreme cold. Part III. Effects of diets on the reactivity of skin vessels
to cold. Jap. J. Physiol. 2:310-315.

378

HUMAN RACIAL RESPONSES

increase in metabolic rate, if I remember correctly. In similar
experiments we did not see anything in Caucasian soldiers. In a
racial study of Eskimos from Anaktuvuk Pass a few years ago we
observed a maintenance of the raised metabolic rate even after
living for 2 weeks on Ladd Air Force Base and eating in the hospi-
tal. The problem of course is they were on an ad libitum diet and
we had no idea of the proportions of the various foods that they
selected for their meals or the supplemental foods they may have
eaten in town. However there was no apparent change in metabolic
rate from when they first brought them down to when they left.

HANNON: It has been my observation, from watching them in
the hospital cafeteria line, that they avoid salads and green vege-
tables. They like potatoes and meat, so they may not be changing
the nature of their diet as much as you might anticipate.

HART: Dr. J. A. Hildes (University of Manitoba) and I meas-
ured the metabolic rate of Coppermine Eskimos who had been
hospitalized at Edmonton, Alta., for several months. We meas-
ured the metabolic rate of Coppermine Eskimos who had been
hospitalized at Edmonton, Alta., for several months. We meas-
ured metabolism all night in the sleeping situation and found that
it was identical to that specified by the DuBois standards corres-
ponding to the weight and height of these men. There did not seem
to be any long term elevation of BMR after they had been living
under white man's conditions.

HANNON: Are these ambulatory patients or bed patients?

HART: They were hospitalized, but there were no active
tuberculosis among the test subjects. They had been suffering
various ailments, but nothing of a severe metabolic nature.

ADAMS: How long had they been down?
HART: This varied a great deal.

IRVING: Some of them were chronic, almost permanent?
HART: Yes. Others were there for several months.

379

MILAN

ADAMS: It might be important to notice the proportional
adjustment of their diet.

HART: These men were eating a normal white man's diet.

HANNON: Your controls were in the same place?

HART: There were no controls in this case. It was just the
Eskimo compared to DuBois standards.

ADAMS'. I do not feel, as Dr. Rodahl pointed out in the recent
reviews, that anxiety plays too much of a ix)le in these basal meta-
bolic rates. In repeated examinations you would expect the effects
of anxiety to be reflected by a successive reduction in the meta-
bolic rate. Thus it may have an effect in one or two measurements,
but not after a series.

HART: That is my impression.

MILAN: Dr. Hannon, there has been considerable interest in
the vascular responses of people who have been acclimatized or
habituated to a cold bath, and Dr. Eagan has some information that
was obtained onthesubjects we had here last winter. I wonder, since
we have some time left, if he might present some of the data he
obtained .

HANNON: All right.

380

HUMAN RACIAL RESPONSES
LOCAL COLD ADAPTATION AND HABITUATION

C. J. Eagan

When experiments are done on any animal that is conscious of
its environment, the role of the higher nervous centers in modifying
physiological responses cannot be ignored. Bernard (1865)* in "An
introduction tothestudy of experimental medicine" (1927) has stated:

no animal is ever absolutely comparable with another —
neither is the same animal comparable with himself at
different times when we examine him, whether because
he is in different conditions, or because his organism
has grownlesssensitive.by getting used to the substance
given him or to the operation to which he is subjected.

Davis (1934)** described modifications in tne galvanic reflex as
a result of daily repetition of a stimulus. Other examples could be
cited. A progressive reduction in response to a repeated stimulus
has been termed "habituation" by Glaser and Whittow (1953)***.
"Habituation" is defined as "the process of forming into a habit or
accustoming" and it is implied that "it depends on the mind, that it
is reversible, and that it may involve the diminution of normal
responses or sensations" (Glaser, Hall, and Whittow, 1959****).

This is a typeof adaptation. Where the habituation is character-
ized by a reduction in response to a cold stimulus, then it is a "cold
adaptation." In man it may be the most common type of cold adapta-
tion which occurs.

I propose that there are two types of habituation, specific and
general. "Specific habituation" is specific to the repeated stimulus
♦Bernard, C. 1865. An introduction to the study of experimental medicine.
Henry Schuman, Inc. 1927. 226 pp.

♦♦Davis, R. C. 1934. Modifications of the galvanic reflex by daily repetition
of a stimulus. J. Exp. Psychol. 17:504-535.

♦♦♦Glaser, E. M. and G. C. Whittow. 1953. Evidence for a non-specific mechan-
ism of habituation. J. Physiol. 122:43P.

♦♦♦♦Glaser. E. M., M. S. Hall, and G. C. Whittow. 1959. Habituation to heating
tand cooling of the same hand. J. Physiol. 146:152-164.

381

MILAN

and specific to the part of the body which is repeatedly stimulated.
"General habituation" might be explained asachangein the psycho-
logical "set" of the subject relevant to the conditions of experimen-
tation so that he is no longer apprehensive, either consciously or
unconsciously, at the time of the test.

These two types of habituation can develop simultaneously.
Both depend upon a change in the manner in which the central ner-
vous system interprets its afferent impulses. Both involve a pro-
gressive diminution in response to a repeated stimulus. Where the
stimulus is the application of severe cold, specific and general
habituation are manifested by reduced pain sensation and by
reduced vasoconstrictor activity, respectively.

Both types of habituation as well as a local vascular adapta-
tion were demonstrated in experiments done at the Arctic Aero-
medical Laboratory (Eagan, 1960a*, 1960b**, 1961***). In all
experiments, regimens of unilateral cold exposure ("test" side
only) followed by simultaneous bilateral comparison ("test" vs.
"control') were used in investigations of local tissue cold adapta-
tion in the fingers of man. A summary of these experiments follows.

Chronic hand cooling of moderate intensity (12 hours per
day with finger temperature between 10 C and 15 C for ten

*Eagan, C. J. 1960a. Topical adaptations to cold in the extremities. Proc.
XI Alaskan Sci. Conf. pp. 184-185.

♦♦Eagan, C. J. 1960b. Unilateral cold adaptation to recurrent ice water immer-
sion. Physiologist, 3(3) :51.

♦♦♦Eagan, C. J. 1961. Habituation to recurrent ice water immersion of the finger.
Physiologist, 4(3) :3l.

382

HUMAN EACIAL BESPONSES

days) resulted in a less intense initial vasoconstriction, less varia-
bility in digital blood flow and a 17% greater average heat loss, dur-
ing a 30-minute period of ice- water immersion. Fingers of the test
hand cooled more slowly than the control fingers during exposure to
cold air. Pain sensation tended to be less for the test hand, espe-
cially for the fingers; this type of cold adaptation was termed "spe-
cific habituation" — specific to the cold stimulus and to the part of
the body stimulated.

Recurrent f inge r cooling of severe intensity (six 5- minute ice-
water immersions per day for 17 days) caused a marked, specific
habituation to cold pain. There was no essential difference between
the vascular reactions of test and control fingers when they were
tested in ice water. Prolonged recurrent finger cooling (six 10-
minute ice-water immersions per day for 125 days) confirmed the
finding that specific habituation to pain could develop in the absence
of local vascular cold adaptation. However, the subjects did show
higher finger temperatures (test and control fingers alike) in ice
water, compared with other subjects being tested forthe first time.
This was concluded to be a "general habituation" to the conditions
of the experiment which resulted in less vasoconstrictor outflow to
fingers in ice water.

It is considered that the results on general habituation are
highly relevant to what has been discussed above by Milan. Many
racial differences in the responses of the extremities to cooling
have been attributed either explicitly or implicitly to localized
vascular adaptations. These differences may on the contrary be
related to the degree of habituation to cold exposure and the
experimental conditions. Further, the energy state of the subject
at the time of the test is not always taken into account.

A comparison of the responses to finger cooling in four groups
of subjects is demonstrated in Table III and Figure 4.

The habituated group consisted of the six USAF airmen who
had each immersed one middle finger in ice water 750 times over the

383

MILAN

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384

HUMAN FACIAL RESPONSES

Subject No. of Energy state of subjects Average

group subjects BMR Rectal finger

(kcal/m^/hr) temp. (° C) temp. (° C)

Indian

Habituated

Control

Starvation

42.20 ± 1.60 36.80 ±0.10 8.74 ±0.77

34.72 ±0.75 36.84 ±0.04 5.93 ± 0.61

35.35 ± 1.04** 36.77 ± 0.10 3.45 ±0.77

30.56 ± 1.59 37.09 ±0.05 2.57 ±0.94

Significance of differences (P)
Indian vs. habituated < 0.01

Indian vs. control < 0.01

Indian vs . starvation < 0-001

Habituated vs. control ns

Habituated vs. starvation < 0.05

***

Control vs. starvation

<0.05

< 0.001

<0.0S

< 0 .00 1

< 0.0 5

<0.01

<0.05

<0 .0 5

♦Standard error
* ♦BMR was measured on only four of the control subjects
♦ ♦ ♦Not significant (P >0.05)

Table III. Relation between energy states of subjects and average tem-
peratures of fingers immersed in 0 C water for 10 minutes (under standard
test conditions for all groups).
I 385

MILAN

previous 125 days. The averaged responses of the control fingers
of this group were compared with the averages for the right middle
fingers of each of the other groups. The average age for the habi-
tuated group was 27 years.

The Indian group consisted of six Alaskan natives from the
Tetlin Reservation. They normally spent the greater part of the
daylight hours out-of-doors, attending trap lines, etc. These sub-
jects were tested during the latter part of December, when it would
be expected that they would have endured considerable recent cold
exposure. At the time of this test, they had lived at the laboratory
for one week under a regimen of restricted indoor activities. Their
meals were taken entirely at the USAF Hospital cafeteria. During
the week, they had been subjected to several oxygen consumption
measurements and finger immersions in ice water, in connection
with another study. Hence, they were accustomed both to the test
and to the experimenter. Their average age was 23 years.

The control group consisted of six subjects who were engaged
in indoor occupations andfiveof whom were employed at the labora-
tory. They were at ease with the experimenter but were not accus-
tomed to the test. It was considered that they were comparable with
the habituated group except for their unfamiliarity with the test.
Their average age was 30 years.

The starvation group consisted of six subjects who were tested
1 or 2 days after returning from a regimen of starvation in the cold.
They had lived for 5 days camped at individual sites on river ice,
without food or sufficient thermal protection, in interior Alaska dur-
ing the month of February. They we re all accustomed to recent cold
exposure and to the experimenter, and four of the six were accus-
tomed to the test. Their average age was 27 years.

Every effort was made to have test conditions the same for
the four groups. In all tests the compared fingers were immersed
equal depths (2.8 ± 0.1 cm ) in 0.0 C water for 10 minutes. The
water bath was stirred equivalently in all tests. Temperature of

386

HUMAN RACIAL RESPONSES

the distal digital volar pads was measured using the one set of
thermocouples which were always placed on comparable positions
on the fingers.

Prior to tests the subjects slept overnight in a comfortable
environment at the laboratory. Standard procedures were followed
such that subjects were post-absorbtive and normothermal at the
time of tests. All tests were done between 0700 and 1000 hours in
the morning. Oral and rectal temperatures were taken and basal
oxygen consumption was measured while the subject remained in
bed. Immediately after the subject arose from bed he was instru-
mented and with arms in the dependent position the middle fingers
were immersed.

In all tests the estimated intensity of pain sensations from
each immersed finger was recorded at each minute. (See pain inten-
sity scale on Figure 4.) "Maximum pain" is the highest single esti-
mate during the test, while "average pain" is the cumulative minute
total divided by the time (10 minutes).

It must be emphasized that it is the responses of the control
fingers of the test subjects (habituated group) that are compared
with the responses of the right middle fingers of the other three
groups. Figure 4 shows that in the capability for maintaining
high finger temperature during ice water immersion the progres-
sion among the groups was Indian > habituated > control > starva-
tion (although the difference between the control and starvation
groups was not significant). The pain suffered by the habituated
and control groups was roughly the same, while that of the starva-
tion group was somewhat less, and in the Indians it was almost
negligible- Thus there was no simple relationship between pain and
finger temperature.

Table III shows the relation between the energy states of the
subjects as they rested in bed just before the finger immersion
test and the average finger temperatures maintained in the ice
water. A direct relationship between metabolic rate and finger

387

MILAN

temperature during immersion is strikingly demonstrated by the
Indian and starvation groups. It is notable that rectal temperature
is higher in the starvation group than in the others, therefore, finger
temperature need not be related to the central thermal state. The
most important results relevant to the assessment of local cold
adaptation in vascular responses are shown in the comparisons
of habituated and control groups. BMR and rectal temperature
were the same for both. Yet the habituated group maintained a
significantly higher average finger temperature (P<0.05). Finger
temperatures of the groups just before immersion were in the
progression: Indian > habituated = control > starvation. The values
in C were, respectively, 35.2 ±0.16, 33.8 ±0.28, 33.7 ±0.40 and
29.5 ± 1.53. The mean finger temperature of the Indians was sig-
nificantly higher than that of the others (P < 0 .05) but the differences
between the other means were not statistically significant.

General conclusions. It was shown that cold exposure of the
human hand can cause a local vascular cold adaptation, or a marked,
specific habituation to cold pain, according to the duration and inten-
sity of the local cooling. Further, it was shown that a general habit-
uation to the test procedure gives results which could be mistaken
for a local vascular cold adaptation.

In conditions where man works outdoors in cold climates, it is
likely that he will endure prolonged periods of moderate hand cool-
ing and occasional periods of severe cooling. Hence, he might main-
tain higher finger temperatures through a vascular adaptation, and
suffer less pain, even when finger temperatures were very low,
through specific habituation. These adaptations, combined with a
general habituation to the environment, could result in marked im-
provements in manual efficiency as the cold season progressed.

Yet another factor, which is incidental to these adaptations, may
favor the maintenance of higher peripheral temperatures in outdoor
workers. This is the higher basal metabolic rate which has been
measured in Eskimos and northern Indians. Whether the higher
BMR of these northern natives is mainly related to diet (Yoshimura
et al., 1952*) or to genetic differences has not yet been resolved

conclusively.

*Yoshimura, H., R. lida, and H. Koishi. 1952. Studies on the reactivity of
skin vessels to extreme cold. Part ni. Effects of diets on the reactivity of skin
vessels to cold. Jap. J. Physiol. 2:310-315.

388

THERMOREGULATION IN MAMMALS
FROM THE TROPICS AND FROM HIGH ALTITUDES*

Peter Morrison

The title presents something of a problem since there may
well be no real entity "thermoregulation in tropical mammals"
such as we see in other environments as the desert or the arctic
which make special demands and have elicited special physiological
capabilities. The tropics are distinguished in a negative rather
than in a positive sense, by the lack of demands, at least of thermo-
regulatory demands, which are placed on the inhabitants. As has
been pointed out, this region has a much better claim to the title
of "temperate" than do our own middle latitude regions where
extremes of temperature and rainfall are characteristic. But there
are certain groups of animals which may be considered character-
istic of these regions so that we can at least discuss thermoregula-
tion in "some tropical mammals." However, these may well be
characterized by a deficiency in regulatory ability rather than any
special attributes for life there. The monotremes, and the edentates,
might be considered in this catagory, but these groups have already
been reviewed as primitive forms by Dr. Johansen. So I propose to
survey first, the marsupials, then a primitive eutherian group, the
Ghiroptera, and finally the more advanced group of the Primates;
all of which we can think of as characteristically tropical, although
some representatives extend beyond this zone.

'• *Much of the data discussed in this paper is as yet unpublished. Studies on
Brazilian monkeys were carried out with J. Simoes, Jr.; on the pigmy marmosette
with E. Middleton; on new world tropical bats with B. K. McNab, who also parti-
cipated together with K. Kerst and W. H. Holthaus in the studies on high-altitude
mammals. Support for these studies has been variously received from the Guggen-
heim Foundation, the U. S. Educational Foundation in Australia, NSF, NIH-PHS,
WARF, ONR, and the Rockefeller Foundation.

389

MORRISON

Marsupialia

The marsupials have often been stigmatized as indifferent
homeotherms usually because of the low reported level of the body
temperature (T^. But this conclusion suffers on three counts;
first, a somewhat lower T is a poor criterion of homeothermism,
we do not consider birds to be more homeothermic than mammals
simply because they maintain a higher T ; second, a fairly limited
assortment of marsupials has been studied; and third, since most
marsupials are nocturnal, their study by diurnal physiologists has
resulted in a falsely low estimate of their T level.

The first figure shows the relation between body temperature
and ambient temperature (T ) in a small American (brown) opos-
sum (Didelphidae) in day and night. The diurnal values are quite
distinct from the nocturnal ones, but both are accurately regulated
(over a range) in response to cold. This relation (T vs T ) des-
cribes the sum of regulatory activities with a horizontal curve rep-
resenting complete regulation and one with a 45 slope (reference
line), representing the absence of regulation seen in a poikilotherm.
In addition to the slope, we must also consider the relation of the
curve to the reference line since an animal may have a fairly labile
T and yet maintain it well above the T . A third criterion of regu-
lation is the variability of the T around the mean curve, but this
may sometime provide a spurius mdex, since the scatter may only
reflect a variation in the circumstances under which the measure-
ments were made.

Figure 2 compares a rat-sized Australian representative (Das-
yuridae) with an even more striking diurnal depression, near noon
its T is about 34 C, but at night it is 38 C. Since the latter
level IS equivalent to that in the dog, Chaetocercus can hardly
be considered defective or primitive in its level of regulation. But
this is a form which can show a daily torpor. Another smaller rela-
tive (Antechinus) shows an even higher level during periods of
activity (to 40 ) although these periods do not follow a 24-hour
cycle. Accordingly, it is necessary to identify any daily (or other)
cycle and choose either or both, the maximum and minimum peri-
ods—the active and resting phases--to characterize the species.

390

ADAPTATIONS TO TROPICS AND ALTITUDES

6 :'

I-

Cr 36 c

h- 36 C

O 34«c
CD

32*C

8 0°f

100' r

METACHIRUS

lO'C

• DAY
O NIGHT

/ - 105* F

o o-

•/

.../•

•• — •

20'C

3 0'C

EXTERNAL TEMPERATURE

as a function of T
datus) showing ttie day-night difference

100 F

95' F

-90 F

4 0'C

Figure 1. T as a function of T in the brown opossum (Metachirus nudicau-

3?.

DASYCERCUS
(MARSUPIAL RAT)

MIL

NOON

MID

Figure 2. T in the Crest-tailed marsupial rat (Dasycercus cristicauda) as
a function of hour of day.

391

MOFRISON

Figure 3 represents an interesting form, the bilby. This is
a desert representative of the small group of bandicoots (Perame-
lidae) which further emphasizes the independence in the day and
night "settings" of the "thermostat." The daytime (inactive) T
declined steadily through the course of the experiments, but time
played no part in the level of the active temperature which stayed
steady at 37 . These two states need not differ very much in activity
but merely "wakefulness." The T after forced activity in the day-
time never reached the natural nighttime level. Similarly, forced
activity at night did not raise the T at all. So these are not passive
noncommitants of extra heat production, but rather are maintained
levels that are set by the animal.

Figure 4 recasts these data into a 24-hour cycle to bring out
this very sharp nocturnal pattern. Like the brown oppossum, the
bilby regulates to a different level during day and night (Fig. 5).
The bilby has excellent regulation to cold and this may seem contra-
dictory since it is a desert species which comes from the Australian
"center" where a high T is the rule. But the bilby shows no evap-

orative cooling and if put in a hot room at 40 C, elevates its T

o
by 4-6 G within an hour and must be removed to avoid heat dea'

(Robinson and Morrison, 1957).

By contrast. Figure 6 shows another bandicoot with fair regula-
tion to heat, with the T curve crossing the isothermal line to give
T lower than the T. Of course, in terms of the slopes, what would
be rather poor regulation to cold represents rather good regulation
to heat, and yet this animal comes from the coastal regions, which
are considerably wetter and cooler than the "center." So it is of
interest that a desert animal need not be characterized by the ability
to maintain itself under desert conditions, while an animal from a
less rigorous environment can do better. The answer, of course, is
in the stringent requirements ofdesert life, such that the bilby must
always use microclimatic evasion to avoid the expenditure of water.

The short-nosed bandicoot showed an interesting feature in rela-
tion to the topic of seasonal modification discussed by Dr. Hart.
These animals always showed good "cold" regulation at night (Fig.
6), and in the winter they regulated well during the day or night.

392

ADAPTATIONS TO TEOPICS AND ALTITUDES

ao o ox

oo
-»0 —

MAGNOTIS

(BlLBVI

ACTIVITY

NATURAL

•

INDUCED

DEC-

-JANi

JARY — I-- ^^EbR'JAhY-

Figure 3. T in the rabbit bandicoot or bilby (Mac rot us lagotus) during con-
tinued captivity.

393

MORBISON

•-<B-«

_ x__x_

-o-

(D O

-®

c?— ®^$^-^-

MACROTIS
(BILBY)

MID

NOON

•-^

MID

Figure 4. Daily T cycle in the bilby (Macrotus lagotis) . Different symbols
show successive periods of time.

40 —

MACROTIS

T^ IN 'C

394

ADAPTATIONS TO TROPICS AND ALTITUDES

'B 36-

Figure 6. T as a function of T in the short-nosed bandicoot (Thylacis
obesulus) . Open symbols, winter; closed symbols, summer; circles, day; squares,
night.

395

MORRISON

But the summer animals did not maintain their temperature in
the daytime. So this si^gests that there is some kind of adaptation
of thermoregulatory control not in the metabolic capacity nor in
the insulation, but in the ability to respond to a stimulus which it
may not encounter.

Figure 7 describes the koala. This is a familiar sluggish mar-
supial (Phalangeridae) which has poor temperature regulation to
cold as can be seen from the very substantial slope to the T curve.
In this regard the koala seems quite inadequate, but since the T
curve continues almost in a straight line across the isothermal
line, it actually has quite effective regulation to heat; much better,
indeed, than many of our higher mammals, such as the rodents,
which cannot maintain the T below the T . There is again a con-
siderable scatter in these points, but much of this could be elim-
inated by proper definitions of the conditions. This is a particular
problem with a sluggish animal which adjusts only slowly to new
circumstances. As one might expect, the afternoon T is warmer
than the morning T . But this is a diurnal animal and so part of

this slope of the T curve reflects the daytime activity.
B

The examples given thus far might tempt us to characterize
the marsupials as animals with very large diurnal cycles, and
even to represent a measure of thermal instability, although this
is a matter of some argument. But Figure 8 shows, for contrast,
a small wallaby (Macropodidae) with no daily cycle at all. Simi-
larly, Figure 9 presents one of the larger macropods in which the
diurnal cycle is again absent. But in part this effect is spurious
as a representation of the animal in nature because an animal as
large as the kangaroo is not able to engage in his normal activity
when maintained in close captivity. If it is normally occupied with
moving and feeding, higher nocturnal values are obtained. How-
ever, Figure 9 is principally of interest in illustrating or suggest-
ing another phenomenon. The checkered circles averaged by the
upper dotted curve represent T values that were taken during the
week following a critical heat test in which the animal was exposed
for 6 hours at 40 . During this exposure the T was not markedly
elevated (only to 35.4 G), since kangaroos are excellent regulators
to heat. Nevertheless, following this heat exposure, an elevated

396

ADAPTATIONS TO TROPICS AND ALTITUDES

PHASCOLARCT'JS '.irjEREJ,
(KOALA)

10 20 3c;

AMBIENT TEMhERATURE IN °C

Figure 7. T as a function of T in the koala (Phascolarctus cinereus).

38-

WALLABIA DORSALIS

"0 c> oi-^6""'Q'(i"'Q"^ "

-Q-6-

«»

—»>"-« - "

r/iD

8 NOON 16

20 MID

Figure 8. Daily T response in the black-striped wallaby (Protemnodon
[=Wallabia] dorsalis). Individuals differentiated by symbols.

397

MORRISON

T was recorded, not only on the following day, but for more than
a whole week thereafter. The crossed circles in Figure 9 repre-
sent the second week after that exposure with some return towards
the normal level, and then finally the lined circles show the return
to normal in the third week. Here, then, is a suggestion of an

adaptation of T in response to a thermal stimulus, a response

B
which as Scholander et al. (1950) point out is not appropriate to

cold. But because a difference of only a degree or two in T in

a hot climate may allow the elimination of evaporative cooling, it

could be a very useful response to heat.

In summary, the marsupials are a primative group which can-
not be characterized by a single thermoregulatory pattern. Some
show excellent regulation to cold while others are cold-sensitive.
Some have very effective regulation to heat while others have none.
There does seem to be some disposition towards thermal lability,
although not necessarily thermal inadequacy in the group.

Chiroptera

The Chiroptera have always been of special interest because
of the seasonal and daily hypothermia exhibited by those temperate
forms which have been studied. However, they are essentially a
tropical and subtropical group, so we should, perhaps, character-
ize the order in terms of the tropical representatives. It is in the
tropics that they show their greatest profusion, both in numbers
and in their specializations for different environmentalor behavioral
situations. The flying foxes, or Megachiroptera, weigh as much as
a kilo and are very substantial animals. In Australia we found that
one megachiropteran (Pteropus) regulated its temperature very well
against cold, and that it had insulative properties and metabolic res-
ponses which were quite comparable to small temperate-zone mam-
mals of the same size (Morrison, 1959). We were, therefore, inter-
ested in Brazil last year to examine a series of the michrochirop-
teran fruit bats, largely from the Phyllostomidae.

Figure 10 shows the daily cycle for one of these genera,
Artibeus. The cycle is substantial, but not extreme, with a range
of about 3 C between the mean minimum and maximum levels.

398

ADAPTATIONS TO TROPICS AND ALTITUDES

38 -

IN ^^

C
36 f-

D *

_. B -e

® o

■ □

® o

o% o

■

•

o ° o •

• t

• o

o
•

•

: .•

•

MACROPUS MAJOR
1 1

(GREY KANGAROO)

1 1

MID 4

8 NOON 16

20 MID

Figure 9. Daily T response in the grey kangaroo (Macropus major). Closed
circles show ordinary temperature in a young animal; open circles in an adult;
squares represent active animals; other symbols follow heat exposure (See text).

HOUR OF DAY

Figure 10. The daily T cycle in Artibeus. Symbols show sample size, mean
value, 2 x standard error, standard deviation and range.

399

MORBISON

A small scattering of points below the main body have not been
included in the heavy average because they represent a distinct
population, but their inclusion as shown by the dotted curve does
not change the picture appreciably. Figure 11 presents the thermo-
regulatory response to cold in this species and shows it to be an
adequate regulator since the slope is a modest one, comparable
to that in many other mammals. Under heat stress, however, there
is almost no regulation, the slope being little less than the value
of 1.0 characteristic of a poikilo therm.

Figure 12 shows a somewhat different T response in a smaller
species. At modest T^ values of 15-20 cf, the T falls subs tan-

^ ^/::..:-:.-:r--B

tially. But when the T is cooled further, the animal seizes hold
and regulates its temperature quite effectively. Thus, the reduced
T did not represent a deficit in capacity or ability to regulate,
Since the animal regulated well at an even lower T . It can be con-
sidered as representing a kind of deficiency — careless thermo-
regulation— but there may be functional implications. This type
of response may be seen in other mammals. The jumping mouse
(Zapus), for example, may cool appreciably at intermediate T
values, but regulates well at or below 0 . Again, there is no deficit
in the capacity or ability to regulate, but the animal retains an
option as to its use.

Figure 13 shows the daily cycle in a larger bat (Phyllostomus)
which differs somewhat. The two peaks are characteristic of a
crepuscular animal which feeds at dawn and dusk. Again, there
are a number of points which exceed the dispersion of the bulk
of the values (d 3 S. D.), and we have in addition some very low
points which approach the T . This polydispersity (seen also in
Artibeus, Fig. 10) suggests that we may be dealing with several
conditions or activity levels, a situation already indicated in the
insectivorous bat Miniopterus (Morrison, 1959). This suggestion
appears to be confirmed in Figure 14 which shows the more com-
plicated response of Phyllostomus to cold. Now in Figure 13 this
bat could be thought of as operating under different conditions —
perhaps "active," "quiet," "sleeping" and "torpid." It was ordi-
narily resting during the daytime but even then could become active

with a higher T . Occasionally it showed a torpid, poikilo thermic
B

400

ADAPTATIONS TO TROPICS AND ALTITUDES

Figure 11. T^ as a function of T . in Artibeus.
B A

Figure 12. T as a function of T in Sturnira. Triangles represent another
species (Vampyrops) which conforms to tfie same pattern.

401

MORRISON

I B

IN 34
"C

6 1 1

•

^ 1 F

, y.,

M^r xH

X \ Jl,

(7) ^ '

■.n\ U

vS^-^

m^y n

■""■(a)

■^ rs® T

0
o *

•

o o
1 o

•

.°

•

PHYLLOSTOMUS

12
HOUR OF DAY

Figure 13. Daily T cycle in Phyllostomus.

T. IN "C

Figure 14. T as a function of T in Phyllostomus (circles) and in Molossus

(squares) .

402

ADAPTATIONS TO TROPICS AND ALTITUDES

state where the T approached the T . Also in bats here, as in
Miniopterus, there can be an intermeoiate zone (sleeping *<) — not
poikilothermic in the ordinary sense, but just a little above 30 C
where the animal can become active rather quickly, but still effect
an appreciable metabolic savings. Now, the T groups in the cold
exposed animals can be associated with these groups , although they
may not be exact projections. The upper curve (Fig. 14) maintains
the "resting" level and at 6 G ambient, as a more vigorous meta-
bolic response is required, even approaches the "active" level.

The intermediate curve with T values near 30 maintained even

o B . .

at 6 G ambient, gives further credence to the concept of a mam-

tained "sleeping" level. Finally a few much lower values (lower

curve) would represent torpor although not as low as the ambient

level.

Figure 14 also compares Molossus, a tropical insectivorous
bat, which uniformly became torpid when exposed to cold, although
not quite to the degree expected of a similar temperate bat. Figure
15 shows the daily T cycle in this species (lower curve) which also
closely resembles tne behavior of our northern bats with elevated
activity at dusk and dawn and torpor during the day. Eisentraut (1950)
has discussed tropical insectivorous bats which he found to have a
broader "range of activity temperature" than their temperate rela-
tives and thus not ordinarily to enter into a state of torpor during
the day. This was certainly the case in the situations where Molossus

was collected (T = 30°+ C) but in the laboratory at a T . of 26 C

o A , ^

to 28 C it certainly entered torpor.

In Figure 15, also, the curves for the 4 frugivorous bats are
compared. This set of curves presents an interesting sequence of
parameters in order of decreasing animal weight. Thus, in this
series, both the resting diurnal and the active nocturnal levels are
increasing, the rate of change between the two activity states is
decreasing, and the diurnal fall is postponed, although the nocturnal
rise is fairlysynchronousfor the several species. The insectivorous
Molossus fits into these sequences in all regards except weight,
since it is the smallest of the lot. It is not now possible to interpret
these systematic regularities, buttheyno doubt fit into some general
pattern of thermoregulatory properties.

403

MORRISON

HOUR OF DAY

Figure 15. Summary of daily cycles in different species of bats: M, Molossus;
P, Phyllostomus; A, Artibeus; S. Stumira; G, Glossophoga.

104.

102

100

98_

HOUR OF DAY

Figure 16. Daily T response in four species of Cebus to illustrate conformity
of pattern. Points on mean curve (heavy) represent some 350 values. Data from
Dr. H. L. Ratcliffe, Penrose Research Laboratory.

404

ADAPTATIONS TO TROPICS AND ALTITUDES

In summary, the chiroptera also show a variety of responses.
Traditionally the insectivorous species are characterized by their
thermolability, but the behavior of some of the frugivorous species
can be indistinguishable from other mammals. However, even in
the larger bats scattered values suggest a latent thermolability
which may be manifested under appropriate conditions. But since
this thermolability, either expressed or latent, appears to be suited
to the environmental and metabolic needs, we should hesitate to
describe it as a primitive feature or an inadequacy.

Primates

The last group to be considered is an advanced one, but with
one exception, is even more strictly limited to the tropics. There
is considerable T data on the Primates partly because of their
use as laboratory animals, but also because of tuberculin testing,
particularly at the Philadelphia Zoological Garden, (Brown, 1909;
Fox, 1923). Some recent data are shown in Figure 16 which compare
four species of Cebus and shows the extreme regularity of their
response. The temperature cycle with an amplitude of 2.5 C is
substantial, but not extreme.

Figure 17 represents a smaller primate, the marmoset
(Callithrix) J which shows a striking diurnal cycle with an amplitude
of almost 4.0 C. Although these animals adapt well to handling
and have been popular as pets for more than a century, there is
almost no physiological information on them. Figure 18 considers
another marmoset which is of interest as the smallest of the pri-
mates and weighs about 100 g. It, too, has a very striking cycle,
although not so large as Callithrix . A unique feature is the minimum,
which is very low for a primate. One may wonder if the cryptorchid
condition sometimes reported in this genus (Hill, 1959) depends on
this low body temperature, in accordance with the general relation
between body temperature and descent of the testes as discussed by
Wislocki (1933). Figure 19 shows the effect of limiting temperature
measurements to six fixed times during the day as has been done
in many measurements on Primates. A substantialdistortion results
with a plurring of the almost "square" wave form seen in Cebuella
and a loss of resolution of secondary waves.

405

MORRISON

HOUR OF DAY

Figure 17.Dailybody temperature response in t±ie common marmoset (Callithrix
jacehus) .

HOUR OF DAY

Figure 18. Daily temperature response in the pygmy marmoset (Cebuella
pygmmea). Dashed curve shows same curve inverted and displaced by 12 hours to
illustrate cycle symmetry.

406

ADAPTATIONS TO TROPICS AND ALTITUDES

Figure 19. Distortion of the daily cycle of the use of fixed time points (03, 07
11, 15, 19 and 23 hr.).

HOUR OF DAY

Figure 20. Comparison of daily temperature cycles in new world monkeys; 1,
Cebus; 2, Ateles; 3, Aotus; 4 , Callithrix ; 5 , Cebuella. Broken curve for the nocturnal
Aotus has been shifted twelve hours to allow comparison to diurnal forms.

407

MOREISON

Figure 20 compares the form of the daily cycle in several of
these new world monkeys. Although at a lower level, the form of
the curve in Ateles is strikingly similar to that of Gebus . By con-
trast, curves of the two marmosets, representing the more primi-
tive Callithricidae, are quite distinct. Also shown in Figure 20 is
the night monkey (Actus) whose cycle, however, has been shifted
by 12 hours so that it could be compared to the others. Nocturnal
forms are rare among the primates and the limited amplitude of
this nocturnal cycle suggests that thedaily cycle may not be merely
a casual concomitant of the time of activity, but be more formally
impressed into the "matrix" of the animal. Thus, in this instance,
the nocturnal Actus has reversed the characteristic primate diurnal
cycle, but has achieved only a limited amplitude.

Figure 21 compares another aspect of regulation in two of
these species to show that while Actus has excellent "cold" regula-
tion, Gallithrix is quite sensitive to cold. A correlation might be
made with the nocturnal habit, but it is only fair to note that Actus
ranges up the Andean slopes to fairly cool situations. The response
of the smallest primate (Cebuella) to cold is shown in Figure 22
and shows even less resistance to cold than the larger Gallithrix.
But its resistance to heat stress is distinctly superior, and at a

T , of 40 G it maintains a T of 40° G.
A B

Figure 23 shows the - metabolic response of Gebuella at vary-
ing T and presents a good example of the problem of fitting a
conductance value to a thermolabile animal. If we describe our
homeotherm in terms of the simplest model then the heat flow or
metabolism will be proportional to the temperature differential

(Scholander et al., 1950a). But, as was seen in Figure 22, the main-

o o

tenance range for T in Gebuella was only between 15 G and 30 G,

and below this we will find reduced T and metabolism. Accordingly,

if the metabolism is plotted directly against T the mean curve will

have too low a slope (low conductance) and will extrapolate above

the T . To adjust for this error, the metabolism may be plotted

against the temperature differential, T -T (top scale in Fig. 23);

or to maintain a more familiar scale, the T may be corrected by

the amount of the T depression (bottom scale in Fig. 22). With

)od

this procedure, a good linear representation is obtained with extra-
polation to the T (38 G) at the abscissa. The conductance curves
B

408

ADAPTATIONS TO TROPICS AND ALTITUDES

Figure 21. Body temperature as a function of ambient temperature in Callithrix
(open symbols) and Aotus (closed symbols). Squares represent night values; circles
are day values.

IN 40

•c

CEB

UELLA

°o -

•o

°°^

-^°

•

x^'

•

•
•

, 1..,

Ta IN C

Figure 22. T in Cebuella pygmaea as a function of T . Open symbols, male;
closed symbols, female.

409

MOEBISON

CCO2

PER

g. hr

CEBUELLA

20 30

Ta -(Tb-38) in "C

Figure 23. Metabolism as a function of ambient temperature in the pygmy
marmoset. Triangles represent points adjusted for fall or rise in body tempera-
ture. Large points represent standard body temperature (38.0 ). Small symbols,
no temperature measurements. Light curves compare metabolic response in
Aotus (lower) and Callithrix (upper).

410

ADAPTATIONS TO TROPICS AND ALTITUDES

for the other two primates are also compared in Figure 21. Most
ol the observed differences relate to the differences in size. The
values for the two marmosetts lie just above the mean curve relat-
ing conductance to body weight in some temperate small mammals,
C = W (Morrison and Ryser, 1951). Aotus, by virtue of its more
effective insulation, has a conductance appreciably below the mean
curve.

In summary, this limited survey of thermoregulation in the
primates has again shovm some regularities in the daily cycles,
but also some variety in this and in the response to cold. Also, to
consider again the general question as to common thermoregula-
tory features shared by .tropical mammals, there appears to be
none. Certainly there is great variation in the maintained levels
both diurnal and nocturnal. The response to cold and as well, to
heat, appear equally variable since either or both may be present
or absent. Even the criterion of inferior insulation cited by
Scholander et al., (1950) does not hold for many of the smaller
tropical species. Indeed, perhaps we can only characterize the
tropical mammals by the complete heterogeneity of the thermo-
regulatory responses.

Altitude and Thermoregulation

The relation between thermoregulation and altitude appears

even more tenuous than that of the tropics. It is true that if oxygen

is sufficiently withheld from a mammal in the cold, its T will

B
fall (Nielsen et al., 1941). But other functions and activities will

be similarly impaired. Of course, to the extent that thermoregula-
tion may require a considerably greater energy output than other
functions, it will be preferentially affected — and also, as a regula-
tion that is, perhaps, less critical than some others, it might be
preferentially dispensed with as in the camel (Schmidt- Nielsen
et al., 1957).

We have recently investigated the altitudinal responses of a
number of Andean rodents, and the matter of their transport capa-
city for 0 at varying altitudes bears on the present point since it
represents a limit for energy output. Indeed, our experimental

411

MORRISON

o o

procedure involved a cold stress (at 5 C to 10 C) to raise the

metabolic level. The oxygen tension was then lowered in successive
steps until a reduction in oxygen consumption was observed. This
was always followed by more or less severe hypothermia depend-
ing on the duration of the experiment.

As an index of performance, we choose the pO at which the
metabolism was reduced to twice the basal level. Of our "low"
species, the least effective was the Chilean degu (Octodon degu),
a rat- sized, histricomorph rodent. The "critical" pressure for
the degu was sometimes reached atanpO of 110-120 mm, a reduc-
tion of only 1/4 from that at sea level. The other extreme was seen
in one of the species of the high-altitude genus of Akodon, a small
cricetid rodent, which could still be effective at a pO of 50-60 mm,
or about a third that at sea level. These were the extremes, and
although animals from high altitude were on the whole much more
effective than animals from sea level, a spectrum of "critical"
pressures was seen. Thus, the best "low" species (Oryzomys 1.
longicaudatus) was more effective than several of the "high" species.
The differental performance of different species from the same
environment appeared to relate to general "fitness" or "athletic
development." Thus, the Oryzomys was markedly the most vigorous
of the low species, and it is quite reasonable that their greater meta-
bolic potential will also be effective under the handicap of hypoxia.
In a similar manner, wild guinea pigs showed significantly greater
performance than their more sedentary domestic relatives taken
from the same altitude.

In sunrvmary, Andean rodents from high altitude do show superior
thermoregulation to cold stress when measured at low oxygen pres-
sures. This facility appears to be unrelated to the moderate increase
in cold stress on the altiplano, and relates rather to the general
improvement in transport capacity by which the species adapt to
the requirements of their hypoxic environment.

412

ADAPTATIONS TO TROPICS AND ALTITUDES
LITERATURE CITED

1. Brown, A. E. 1909. The tuberculin test in monkeys: with notes

on the temperatures of mammals. Proc. Zool. Soc,, London.
-.81-90 .

2. Eisentraut, M. I960. Heat regulation in primitive mammals

and in tropical species. Bull. Mus. Comp. Zool. 124:31-43.

3. Fox, H. 1923. Disease in captive wild mammals and birds.

Lippincott, Philadelphia. 665 pp.

4. Hill, W. C. O. 1957. Primates. III. Pithecoidea, Platyrrhini,

Hapalidae. Edinburgh University Press.

5. Morrison, P. R. 1959. Body temperatures in some Australian

mammals, I: Chiroptera, Biol. Bull. 116:484-497.

6. Morrison, P. R. and F. P.Ryser. 1951. Temperature and meta-

bolism in some Wisconsin mammals. Fed. Proc. 10:93-94.

7. Nielsen, M., W. H. Forbes, J. W. Wilson, and D. B. Dill. 1941.

The effects upon dogs of low oxygen tensions combined with
low temperatures. In Temperature, its measurement and
control. ReinhoM Publ. Corp., New York. 453-461.

8. Robinson, K. W. and P. R. Morrison. 1957. The reaction to

hot atmospheres of various species of Australian marsupial
and placental animals. J. CeU. and Comp. Physiol. 49:455-

478.

9. Schmidt- Nielsen, K., B. Schmidt- Nielsen, S. A. Jamun, and

T. R. Haupt. 1957. Body temperature of the camel and its
relation to water economy. Am. J. Physiol. 188:103-112.

10. Scholander, P. F., R. Hock, R. Walters and L. Irving. 1950.
Adaptation to cold in arctic and tropical mammals and
birds in relation to body temperature, insulation and meta-
bolic rate. Biol. Bull. 99:259-271.

413

MORRISON

11. Scho lander, P. F., R. J. Hock, V. Walters, F. Johnson, and
L. Irving. 1950a. Heat regulation in some arctic and tropical
mammals and birds. Biol. Bull. 99:237-258.

12. Wislocki, G. B. 1933. The location of the testes and body tem-
perature in mammals. Quart. Rev. Biol. 8:385-396.

414

ADAPTATIONS TO TROPICS AND ALTITUDES
DISCUSSION

HUDSON: Dr. Morrison, do any of your studies correlate these
tolerances of the oxygen tension within the aspect of the cardio-
vascular system? In the case of the house mouse you mentioned
the lung and the diaphragms, so I suppose that answers part of my
question.

MORRISON: Our primary objective was an evaluation of over-
all performance, but weexaminedanumber of details. For example,
the hemoglobin level in native mice at high altitude appears no
greater than at sea level; but at both levels , hematocrits are higher
in the "vigorous" species as compared to "less vigorous" species.
We were not prepared to examine the factor which I suspect is the
most significant, namely the capillary dischargeof oxygen. Because
there were only modest changes in the other factors in the chain —
lung and heart size, heart and respiration rates, hemoglobin level,
etc. — we are forced to conclude that there is some specialization,
perhaps an increase in number, or a lengthening and contorting,
of the capillaries. This would really be an optimal adaptation with
minimal distortion of the normal pattern of the animal; and it would
seem that this normal pattern is rather important. The house mouse
does adapt, but I am sure that he is at a concomitant disadvantage
in some way because it has distorted the normal mammalian form
(i.e., lung fraction, heart fraction, hematocrit, etc.) which is a very
constant feature. I cannot say just why the normal proportions are
optimal, but I think it must be so.

Of course, you human physiologists know the problems of get-
ting comparable material. I was impressed by this in Peru where
some studies compared miners from Ororococha to other subjects
from Lima. Some miners had more work capacity at 15,000 feet
than the urbanites had at sea level, but clearly the development
and conditioning of these subjects differed by much more than
altitude.

HART: May I ask Dr. Morrison a question about the study of
mice at high altitude? Were they all small mammals in your high
altitude and low temperature comparison?

415

MOERISON

MORRISON; Yes, up to the size of a rabbit.

HART: Are these all good regulators?

MORRISON: We did not do exhaustive studies of regulation, but
they seemed to regulate well.

HART; With five degrees of cooling do they always double the
heat product?

MORRISON: Yes, for all the mice and rats. And incidentally, in
a regime like this it is desirable to have knowledge of "where you
are going," so that the cold exposure is not too prolonged. Knowing
the animal and the previous experience one can approach the critical
oxygen pressure quickly.

HART; Your critical temperature was quite high in all of them,
I gather from this.

MORRISON: Yes, it was in relation to their size and insulation.

PROSSER: Did you find any differences between the sea level and
the altitude population of the Phy lotus?

MORRISON: By this index, yes, very definitely.

PROSSER: Is there any evidence that this is genetic?

MORRISON: Yes. We took high-altitude mice to sea level. They
bred there and bore the litters which were raised to adults. The per-
formance of these "low- raised" mice approached that of the parents.
They had spent their entire lives at sea level and yet they were phys-
iologically high-altitude mice.

JOHANSEN; In your many curves of the body temperature plotted
against ambient temperature, it seems inevitable to me that the
curve must bear some relation to the time of exposure to these tem-
peratures, particularly below the critical temperature for the
species.

416

ADAPTATIONS TO TROPICS AND ALTITUDES

MORRISON: No, these were not, in general, situations in which
the body temperature was falling progressively. And, in fact, in
many instances in comparing a 1- to a 2-hour or a 2- to a 4-hour
exposure, the second body temperature would be higher than the
first. These are essentially maintenance temperatures.

EAGAN; Did most of your measurements consist of several
measurements on one animal in order to arrive at the statistics,
or a single measure of the single animal?

MORRISON: Measurements of several animals; but not in all
cases. This is one aspect of comparative physiology in which one
cannot be too fancy in experimental design because the most impor-
tant point of departure is to catch an animal. The work on the very
interesting bilby represented a single individual. I do not like to
work on a single individual any more than the rest of you, since it
imposes limitations, but it is amazing what can be found out from
a single specimen if it is husbanded.

EAGAN: Do you lump the data all together then, or do you aver-
age them for animals under the same conditions?

MORRISON: Well, we do both essentially. Usually the data are
plotted with individuals identified to see whether there are different
patterns of response. If none is seen, the data is then grouped and
averaged without respect to the individual. In the "triple response"
of the bat Phyllostomus to cold there were some definite correla-
tions such that one individual always gave high values while two
others always gave low values.

IRVING: Would it be anything more than a scheme for trying to
organize some of the information in my memory to think that their
very interesting elevation of the metabolic rate after its decline in
moderate conditions, when the animal was further cooled resembles
the response that one sees in bats and arctic ground squirrels?
Do you recall that bats and arctic ground squirrels do awaken from
hibernation if the body temperature is cooled below a certain level;
some of the hibemators will reawaken and begin to generate heat
actively. Do you think this phenomenon of yours is perhaps another
phase of the same sort of thing?

417

MORRISON

MORRISON: Exactly. Operationally, it is just the same kind
of situation. In the ground squirrel, the thermogenesis seems to
act as an alarm system rather than a thermostat. If its body tem-
perature drifts down below a fixed point, near freezing, it awakens
and normal body temperature is maintained thereafter. These bats

act in the same manner except that the alarm is set for 30 C to

o
33 C.

JOHANSEN: We saw exactly the same thing in the birchmouse,
Sicista betulina, in regard to these diurnal variations. If you force
on them a large negative heat load their body temperatures rise
quickly.

IRVING: Or you can say the same thing then, perhaps with
reference to the excellent discussion of the torpidity in birds. At
the small power output it is possible that the cold metabolic animal
could not tolerate very low temperatures.

MORRISON: Torpidity is incompatible with temperatures below
freezing.

IRVING: Yes, they either have to reawaken or die.

MORRISON: I do not know whether they would be able to or not.

IRVING: Do you think birds can be reawakened from torpidity
by excessive lowering of temperature?

MORRISON; Yes, very definitely.

IRVING: I was just wondering how you would compare them
with the faculty which you have shown to be so rather widespread
in mammals. I have not seen it mentioned. That is why I inquired.

MORRISON: It would be well worth looking into, particularly
in some of the Califomian species.

IRVING: It is always stuck in my crop that there is something
that distinguishes torpidity in birds but it may be only in the way
that people have looked at it.

418

ADAPTATIONS TO TROPICS AND ALTITUDES

HANNON: As yet, we have not had any comment on temperature
regulation in the shrew. Dr. Morrison's name has long been asso-
ciated with shrew metabolism. Would you care to comment on the
temperature regulation of these animals?

MORRISON; I think all one can say is that temperature regula-
tion represents an adjustment so that heat output equals heat pro-
duction, and that these animals are obviously so adjusted. They
do not really have a problem because of their high metabolic rate;
obviously the heat flux from these animals per gram of tissue is
very great.

HANNON: Have you ever studied the metabolic response of
shrews when they are exposed to different temperatures? Have
you ever determined the lower temperature limit for the main-
tenance of homeothermy?

MORRISON: You mean to exceed their limit of regulation.

HANNON: Yes.

MORRISON: Yes, we have done that, and our Sqrex from

o 0

Wisconsin could not take more cold than -10 to -15 depending

on the wind. We used this limit to estimate the maximum meta-
bolic rate; the value was close to that which we observed for
short periods of sporadic activity. But we did not run them on a
treadmill.

419

TEMPERATURE REGULATION IN DESERT BIRDS AND MAMMALS

Jack W. Hudson

Birds and mammals living in deserts utilize a variety of physio-
logical, morphological, and behavioral patterns for coping with their
environments. Although any pattern is adaptive when it allows a spe-
cies to live and reproduce successfully in its habitat, there are ex-
amples of desert species which illustrate unique physiological mech-
anisms for coping with high temperatures and limited availability
of water. For example, the camel (Camelus dromadarius) shows
striking thermoregulatory adaptations to high temperatures and
limited water supplies (Schmidt-Nielsen et al., 1957) and the kang-
aroo rat (Dipodomys merriami) demonstrates an excellent capacity
to conserve water (Schmidt- Nielsen et al., 1948a, 1948b). However,
some species of birds and mammals are able to occupy the desert
habitat even though they have no unique thermoregulatory capabilities
or special abilities to conserve water. For example, the wood rat
(Neotoma lepida) has no unique thermoregulatory ability, and it has
only a modest capacity to conserve water, acapacity approximately
equivalent to that of the Norway rat (Lee, 1960). Likewise, the House
Finch (Carpodacus mexicanus) and the Mourning Dove (Zenaidura
macrura), which may live in the desert, have no special ability to
minimize water requirements (Bartholomew and Cade, 1956; Barth-
olomew and MacMillen, 1960), while the Abert Towhee (Pipilo aberti)
does not possess any capacity for temperature regulation absent in
other passerines (Dawson, 1955). Furthermore, neither the House
Finch nor the Mourning Dove is able to process salt solutions as
concentrated as might be expected if its kidney were well adapted
for the conservation of water (Bartholomew and Cade, 1956, 1958,
1959; Bartholomew and MacMillen, 1960).

There are many ways birds and mammals can avoid the environ-

421

HUDSON

mental extremes of high temperature and limited availability of
moisture characteristic of the desert. Among these are nocturnality,
fossorial habits, aestivation and hibernation, and dependence on
succulent foods. The many "niches" available are correlated with a
variety of successful adaptive patterns found in desert birds and
mammals. It is not surprising then, that abroad spectrum of phys-
iological abilities for coping with high temperatures and limited
availability of water is found among desert inhabitants. A species
possessing physiological mechanisms meriting a subjective judg-
ment of "well adapted to the desert environment" is one which
occupies a "niche" where high temperatures and a limited avail-
ability of moisture must be contended with. The converse would be
true of "poorly adapted" species.

The difficulty of precisely describing the niche of a small bird
or mammal has been the subject of much discussion among biol-
ogists. However, some insight into the delineation of the "niche" may
be acquired by examining the physiological performance of a species
in the laboratory as an index of the environmental parameters to
which it is adapted. From observation of the variety of adaptive
mechanisms so far found in mammals of the deserts, it is becoming
apparent that no two species which have overlapping distributions
have the same physiological responses and therefore probably do
not occupy the same "niche." Thus competition between these desert
species is minimized, a distinct advantage in an area where re-
sources of food and water may fluctuate either seasonally or yearly.

The role of natural selection in fitting a particular species for
the desert environment is difficult to assess because of the complex
relationship between the phylogenetic background of the species, the
"niche" occupied by a species, and the rate at which evolution can
occur in response to a changing environment. However, it can be
pointed out that natural selections need only act in the direction of
effectiveness of solution for a particular "niche" and need not be
concerned with elegance of mechanism.

While diverse behavioral and physiological adaptations for
coping with the desert environment have already been found among
birds and mammals living and reproducing in this region, many

422

ADAPTATIONS TO DESEBTS

species occupying special niches remain to be studied. Recently
we have examined the physiological performances of the Poor-will
(Phalaenoptilus nuttallii) and three species of ground squirrels
(Citellus mohavensis. Citellus tereticaudus, and Citellus leucurus) .
Our results illustrate some additional types of adaptations to the
desert environment. The ground squirrels are fossorial and diurnal;
hence, they occupy an ecologically intermediate position between
the small nocturnal and large diurnal mammals. The Poor-will is
crepuscular, although it may nest and roost in areas of extremely
high temperatures.

The Poor-will has a basal metabolic rate or^e-third of that
predicted from the equation: cc02/gm/hr =9.3 W ' . Because of
its low standard metabolic rate, the lower critical temperature of
the Poor- will is also very high (Fig. 1). This low metabolism
minimizes the amount of metabolic heat to be dissipated, a useful
adaptation when a small difference between body and ambient tem-
peratures precludes much radiation, convection, and conduction of
metabolic heat.

In order to prevent the elevation of body temperatures to
lethal levels when high ambient temperatures are encountered, many
birds and some mammals pant. The metabolic heat production
associated with panting increases the evaporative water loss and is
expensive to the water economy, a major consideration for animals
of arid regions. However, unlike many birds, the Poor-will does
not pant and therefore has no marked upper critical temperature.
Although the thermal neutral zone begins at a rather high lower
critical temperature, it is also very broad (Fig. 1) and extends at
least to 44 C. At ambient temperatures above 40 C, the extensive-
ly vascularized gular area is fluttered rapidly with the mouth held
open. In this way, the bird is able to dissipate its metabolic heat
(in addition to dissipating heat gained from the environment when
the ambient temperature exceeds the body temperature) while sim-
ultaneously keeping its level of heat production virtually unchanged.
At high' ambient temperatures, the amount of water expended by the
Poor- will for evaporative coolingisless than that expended by other
birds of comparable size (Fig. 2). The combination of a low basal
metabolism and a gular flutter which does not increase the metabolic
rate necessitates only a modest level of evaporative water loss in

423

HUDSON

Figure 1. Oxygen consumption (corrected to STP) of a Poor- will (Phalaenoptilus
nuttallii) plotted against ambient temperature. Each point is the minimum consump-
tion maintained for at least 30 minutes in a post- absorptive bird. The solid line is
fitted by eye and is extrapolated as the dashed line to intercept with the abscissa.
This intercept indicates only an approximate conformity with Newton's Law of
Cooling.

424

ADAPTATIONS TO DESEPTS

W
U
IS

W
I— I

u
w
p.

>«

•s

+->

(/)

•r-l

(\j

00
CO

■+-1

CO -i->

o S

ft CO

CO 0)

6 ^

C5 c^.

CO
CO

-o

(1)

oo"

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'■•->

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a

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425

HUDSON

order for this species to dissipate all of its metabolic heat and
heat gained from the environment when the T exceeds the T
(Fig. 3). Since at high ambient temperatures, other species oi
birds comparable in size with the Poor-will become hyperthermic
and elevate their metabolism when panting (Dawson, 19 54; Dawson
and Tordoff, 1959), it is difficult to use comparisons for evaluating
the reduction in evaporative water loss accruing from the Poor-
will's reduced metabolism. However, it may be noted that if there
is no radiation-convection-conduction of metabolic heat, as would
occur in the Poor-will when the body and ambient temperatures
are equal (40 C), a 40 gram bird with a metabolism one-third of
normal saves 12 cc of water /day (assuming that one cc of oxygen
releases 4.8 calories and 1 mgm of evaporated water dissipates 0.58
calories).

Scholander (1955) has suggested that evolutionary adaptation for
temperature regulation in homeotherms has principally involved heat
dissipation and that heat production has not been modified since all
species, regardless of habitat, typically follow the mouse to ele-
phant curve. Thus, arctic mammals at low ambient temperatures
keep their heat dissipation minimal by virtue of good insulation and
possess special means for dissipating heat during activity or at
relatively high ambient temperatures. In contrast to arctic mammals
and birds, animals from desert areas more frequently encounter
problems of maximizing heat dissipation when there is a small diff-
erence between body and ambient temperatures. For this reason,
it might be expected that at least some species, particularly those
which are diurnal, would demonstrate a reduction in the level of
basal metabolic heat production. The Poor-will is an example of
such a species, and thus it is an exception to Scholander's general-
ization that metabolism is not adapted to climate. Although Scho-
lander et al.(1950) relate the low metabolism of tropical caprimul-
gids to their capacity to hibernate, such a correlation does not
differentiate between cause and effect. Thus, hibernation may either
allow or follow a lowbasal metabolism. Also, considerable evidence
has accumulated to suggest that the low metabolic rate of many
hibernators may be attributable to the fat deposits which in them-
selves probably exert little effecton the overall metabolism (Barth-
olomew and Hudson, 1960; unpublished observations on Citellus
tereticaudus and Cercaertus nana). Therefore, it is probably neces-

426

ADAPTATIONS TO DESEETS

CALORIES EVAPORATED
CALORIES PRODUCED

Figure 3. The relation of evaporative cooling to metabolic heat production in the
Poor-will exposed to various ambient temperatures. The calculations assume that
the consumption of one cc of 0 yields 4.8 calories and that the evaporation of one
mg of water requires 0.58 calories.

427

HUDSON

sary to use fat-free weights for comparing the basal metabolic
rates of hibernators and non-hibernators, in order to be certain
that a low metabolic rate is a phenomenon typical of hibernators.

o
The high lower critical temperature (35 C) in the Poor -will

means that much of the time this species lives outside its thermal
neutral zone. It is interesting to note that the Poor-will undergoes
seasonal torpidity when food is less available and when the main-
tenance of a normal body temperature would be metabolically ex-
pensive (Bartholomew, Howell, and Cade, 19 57). While there are
other species of birds which spend much of their time outside the
thermal neutral zone (Dawson and Tordoff, 1959; Scholander et al.,
1950), torpor is particularly advantageous in the Poor-will, because
this species represents an unusual combination of specialized mor-
phological and behavioral adaptations for foodgetting, with its food
sources subject to marked fluctuation in availability.

The low basal metabolic rate of the Poor-will is reflected in
a low heart rate (Fig. 4) at thermal neutrality. Birds which are com-
parable in size to the Poor-will but which possess a normal meta-
bolism (Odum, 1945) have heart rates about twice that of the Poor-
will. While both heart rate and metabolism increase when the
ambient temperature decreases below the lower critical tempera-
ture, the heart rate reaches its maximum level at a T . of about

o A

15 C, whereas the metabolism continues to increase as the T ,
o A

decreases below 15 C.

Seasonal torpidity as a thermoregulatory adaptation for low
temperature is a well documented phenomenon among mammals.
Although numerous natural history accounts have suggested that
seasonal torpidity may also be a response to conditions of high
temperatures and limited availability of food and moisture, there
are only a few studies of the physiological performance of animals
which utilize summer torpor or aestivation (Bartholomew and
Cade, 1957; Bartholomew and Hudson, 1960; Bartholomew and Mac -
Millen, 1961).

The ecological stimulus for aestivation is difficult to identify
precisely in all of the species known to aestivate because of the

428

ADAPTATIONS TO DESERTS

=> 400

^- 300
<

t t

I I I I I I I I I I I I I ' I I I I I ' I ' ' ' ' I ' I ' I ' lip

10 15 20 25 30

AMBIENT TEMPERATURE °C

Figure 4. Heart rate of a Poor-will at different ambient temperatures. The
closed circles represent the heart rate of an inactive bird following at least 30
minutes of exposure to each ambient temperature.

429

HUDSON

complex interrelationship between availability of food and water and
the prevailing temperature. However, some of the pocket mice, which
can maintain themselves on a dry diet (Perognathus longimembris,
P. xanthonotus, P. formosus, P. penicillatus and P. fallax) become
torpid when food is withheld (Bartholomew and Cade, 19 57);
furthermore, P. californicus has a daily cycle of torpidity which is
related to the degree of deprivation of food (Tucker, 1961).

Adaptation of two species of ground squirrels, C. mohavensis
and C. tereticaudus, to the desert environment depends in part on
their capacity to become torpid. The mohave ground squirrel (Citel-
lus mohavensis) readily becomes torpid at laboratory temperatures
throughout the year, despite the continuous availability of food. Epi-
sodes of torpor are less frequent from March to August, which is
their period of activity under natural conditions. When entering
torpor at ambient temperatures between 22 C and 26 C, they as-
sume the usual sleeping posture, their oxygen consumption declines
rapidly, and body temperature approximates environmental tem-
perature within 3 or 4 hours. During torpor , oxygen consumption is
less than 0.2 cc/gm/hr, and the animal breathes irregularly, with
marked periods of apnea. Following the onset of arousal, oxygen
consumption increases 10- to 20-fold, and it usually peaks within
20 minutes. Body temperature increases more slowly, and the levels
of body temperature characteristic of normal activity are usually
attained in 45 to 60 minutes. Typically, rectal and oral temperatures
are within 0.5 C of each other during arousal. This pattern for the
onset of torpor, torpor itself , and arousal from torpor in the mohave
ground squirrel is typical of the classical picture of hibernation and
occurs at ambient temperatures between 10 C and 27 C (the high-
est measured). Under natural conditions, this species is torpid
during part of the hot, dry periods and continues this pattern
throughout the winter at a time when food and water are relatively
scarce. Thus, the physiological mechanisms for torpidity appear to
be the same during both summer and winter, although the level of
body temperature may differ.

In contrast to Citellus mohavensis, C. tereticaudus kept in the
laboratory throughout the year with food and water available demon-
strated intermittent periods of torpidity from June to October only.
Animals with body temperatures within a degree of room tempera-

430

ADAPTATIONS TO DESEETS

ture demonstrated the tjqjical arousal pattern when disturbed (Fig.
5). The difference between oral and rectal temperatures during
arousal was never more than 3 C, and arousal was accompanied
by strong visible shivering. Animals attained a normal body tem-
perature within 45 to 60 minutes after the onset of arousal at room
temperatures. No instance of torpor was observed between November
and May in a captive round-tailed ground squirrel. Furthermore,
between November and May, the body temperatures of animals were
much less variable and averaged higher than those found between
June and October (Fig. 6). It appears from the laboratory perfor-
mance of C. tereticaudus that this species may aestivate, but not
hibernate. This suggestion is supported by collection records (Donald
R. Dickey collection) , which indicate that this species has been
trapped in December, January, and February in the Coachella Valley,
California. Since C. tereticaudus has been readily trapped during
the summer and early fall, aestivation under natural conditions must
occur on either a daily or an intermittent basis.

It is striking that aestivation is characteristic of one member of
a sympatric pair of desert ground squirrels. The ranges of C.
tereticaudus and C. mohavensis are overlapped by C. leucurus, but
C. tereticaudus and C. mohavensis do not occur in the same area.
C. leucurus neither aestivates nor hibernates, but remains active
above ground at all times of the year. Thus, in the area of sympatry
for these desert ground squirrels, only C. leucurus is active during
the more demanding anddifficultpartsof theyear. It seems reason-
able, therefore, to postulate that between these sympatric ground
squirrels competition, in the sense of utilization of a common re-
source which is in short supply (Birch, 1957, p. 6) , perhaps is
reduced, except in verypooryears,becauseof the differences in the
seasonal patterns of their metabolism.

In contrast to the diurnal ground squirrels which aestivate or
to the nocturnal rodents which are fossorial,C. leucurus must cope
with muchof the rigor of the desert environment throughout the year.
The antelope ground squirrel depends on some of the types of
physiological mechanisms similar to those utilized by the Poor- will,
the kangaroo rat, and the camel in adapting to desert conditions
(Hudson, 1962). Like the Poor- will, the antelope ground squirrel
has abroad thermal neutral zone with a relatively high lower critical

431

HUDSON

Figure 5. Body temperature and respiratory rate of a round-tailed ground
squirrel (Citellus tereticaudus) during an arousal at room temperature (22 C to
25 C). The bottom line is the rectal body temperature; the middle line is the oral
body temperature; and the top line is the respiratory rate.

432

ADAPTATIONS TO DESERTS

I6r

29 31 33 35 37

BODY TEMPERATURE °C.

Figure 6. Body temperatures of 12 Citellus tereticaudus measured periodi-
cally during the year. Individual measurements were grouped into 0.5 degree
intervals. The heights of the histogram represent the frequency at each interv^al.
The separation of June to October and November to May measurements were based
on the occurrence of spontaneous torpor at room temperature in the first category
and its absence in the second category.

433

HUDSON

temperature and no marked upper critical temperature (Fig. 7).
Unlike the Poor-will, the antelope ground squirrel has a basal
metabolic rate conforming to the predicted value cc 02/gm/hr
= 3.8 W * ). C. leucurus can tolerate ambient temperatures of
42.6 C for periods of at least 2 hours, whereas many of the noc-
turnal rodentsof similar size cannot withstand ambient temperatures
above 40 C for equivalent periods of time (Dawson, 19 55; Lee,
1960; unpublished observations, Carpenter, 1961; and Tucker, 1961).
The body temperature of C. leucurus increases linearly with ambient

temperature when the ambient temperature increases from room

o
temperature to 40 C (Fig. 8). Thus, the antelope ground squirrel

depends on hyperthermia both to minimize heat gain from the envir-
onment at high ambient temperatures and to maximize loss of
metabolic heat by radiation, convection, and conduction. When the
difference between T and T is inadequate for dissipation of meta-
bolic heat by radiation-convection-conduction and pulmonary evap-
oration of water (Fig. 9) , C . leucurus drools copious amounts of sal-
iva, which it actively spreads over parts of the body.

Under natural conditions, C. leucurus probably avoids prolonged
exposures to very high ambient temperatures, which would be ex-
pensive to the water economy, by periodically returning to the cooler

burrow. An animal requires only 3 minutes to reduce its body tem-

00 o

perature from 42 C to 38 C when taken from a T . of 42 C to

o A

25 C. In this way, a hyperthermic animal can unload accumulated

heat within the burrow and then return above ground. From this,
it is apparent that behavior can be an important factor in relating
the thermoregulatory capacity of this species to the prevailing en-
vironmental temperatures.

Any consideration of the problem of thermoregulation at the
high ambient temperatures of the desert must take into account
the availability of water and the capacity of a species to conserve
water. The ability of the antelope ground squirrel to maintain a
positive water balance under desert conditions is a complex inter-
relationship between several factors: its type of food, its level of
pulmocutaneous water loss, and its capacity to conserve water
incidental to excretion and defecation. While each of the above
factors may be studied separately under laboratory conditions,
their synthesis in relation to natural conditions is extremely dif-

434

ADAPTATIONS TO DESEETS

600

500

\^/

400

300

1 1 1 1

LETHAL

200

;>"

1 TEMP

100

t
1

10 15 20 25 30 35 40

AMBIENT TEMPERATURE °C

Figure 7. Metabolic rate at different ambient temperatures expressed as per-
centage of basal values for three species of rodents: the arctic lemming (Scholander
et al., 1950), the nocturnal kangaroo rat(Dipodomys merriami) (unpublished observa-
tions, Carpenter, 1961), and the diurnal ground squirrel (Citellus leucurus) (Hudson;
1960).

435

HUDSON

o 10

AMBIENT TEMR 'C

Figure 8. Evaporative water loss in 19 Citellus leucurus at different ambient
temperatures. The line between 30 C and 40 C is described by the equation Y =
(0.0431) (1.159) . The break in the two lines denotes the onset of copious salivation.

436

ADAPTATIONS TO DESERTS

»-

>-
o
o

—

-I

—

i 1 1

- 44

- 36

25 30 35 40

AMBIENT TEMP. *'C.

Figure 9. Body temperatures of normally active Citellus leucurus. The vertical

lines indicate the range; the horizontal lines indicate the mean (M); the rectangles

indicate the interval M + 2s toM-2s . The temperature below each vertical
,.,,,. m m

hne IS the ambient temperature.

437

HUDSON

ficult. However, it is possible to compare the abilities of C. leu-
curus and other desert rodents to minimize excretory water loss.
Such a comparison serves as a basis for acquiring insight into
their relative dependence on water ingestion.

The capacity of some of the heteromyids to keep urinary water
loss at a minimum by the production of a very concentrated urine is
well known. However, there is little information on other desert
species. Direct comparison of renal concentrating capacity among
species which may differ slightly in kidney performance is com-
plicated by the variability of kidney function; this is in part related
to variations in ambient temperature, diet, and fluid intake. For
example, animals given water ad libitum show a correlation between
the urine concentration and ambient temperatures (Fig. 10). Further-
more, because of the possibility of active transport of urea in the
renal tubules (B. Schmidt- Nielsen, 1960), a high protein diet may
increase solute excretion without causing an appreciable increase
in excretory water loss. Single measurements of urine concentration
in animals deprived of water tells little of the minimum daily water
loss required for the discharge of excretory wastes.

One useful technique for comparing different species is to
measure the concentration of urine produced over a 24 hour period
(with comparable diets) when a species is drinking only enough water
to maintain body weight. Data on average urine concentration per
24 hours while drinking a quantity of water minimal for weight
maintenance are presented for C. tereticaudus (Fig. 11).

In order to compare the renal concentrating capacity of C.
tereticaudus with other species, it is necessary to assume that the
serum has a solute concentration of approximately 350 milliosmols
and then to divide the urine concentration by this figure. On the
basis of this assumption, the daily urine concentration of C. teret-
icaudus averages eight times the serum concentration. The average
ratio of urine and serum concentrations in the kangaroo rat (D.
merriami) as estimated from the data of Schmidt-Nielsen et al.
(1948a,' 1948b) is 10.3 when the animals are on a normal diet and 12.1
when animals are eating soybeans. The antelope ground squirrel
has a urine-serum ratio of 9.7 when deprived of water (Fig. 12).
Although values from all of the species are difficult to compare, it

438

ADAPTATIONS TO DESERTS

12.0 .

10.0

8.0

6.0

2.0

_ 12.0

22°C ^-_35C.

22 C

N = 9

N = 3

N = 5

N = 4

10.0

8.0

6.0

4.0

2.0

DIST.

DIST.
H20

5DAYS
WATER
OEPRIV.

Figure 10. Ratio of urine and serum osmolar concentrations for Citellus
leucurus subjected to the various conditions of water availability described below
each rectangle. Arrows denote the ambient temperature to which animals were
exposed. N indicates the number of animals.

439

HUDSON

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440

ADAPTATIONS TO DESERTS

-. I**

0. MERRIAMI
(ON SOYBEAN)

Figure 12. Renal concentrating capacity of various rodents maintained on a
dry diet. The urine;serum osmolar ratios of species other than C. leucurus are
estimated from the data of Schmidt- Nielsen et al. (1948a, 1948b).

441

HUDSON

appears that the ground squirrels produce a urine less concentrated
than that of the kangaroo rat (D. merriami), but more concentrated
than the urine of the wood rat (N. albigula) . Also, the antelope ground
squirrel (C. leucurus) produces a urine more concentrated than that
of the round-tailed ground squirrel.

Significantly, the kangaroo rat, which is the species producing
the most concentrated urine, is primarily a seed eater, and can
maintain body weight on a dry diet. It is suggested that under natural
conditions the daily water requirements of the diurnal ground squir-
rels are too large toallowdependenceonthe water content of a typ-
ical seed diet even if the kidney were better able to concentrate
urine. Thus, while ground squirrels cannot maintain themselves on
a dry diet, they have a renal concentrating capacity sufficient to
balance the routine water losses with the water available in their
diet of succulent foods.

SUMMARY

Birds and mammals living in the deserts utilize a variety of
physiological, morphological, and behavioral patterns which may be
subjectively judged as varying from "well adapted" to "poorly adap-
ted. " In all cases, the ability of a desert species to live and repro-
duce in its environment indicates adaptation regardless of the ele-
gance of the mechanisms utilized. The role of natural selection is
such that effectiveness of solution rather than any special mechanism
is the primary criterion.

The multiplicity of adaptive mechanisms attests to the diversity
of niches available, and it may turn out that no two desert species
of similar distribution have identical morphological, physiological,
and behavioral adaptations. While there are many species which re-
main to be studied, data for the Poor-will (Phalaenoptilus nuttallii)
and three species of ground squirrels (Citellus leucurus, Citellus
tereticaudus, and Citellus mohavensis) further demonstrate the
diversity of adaptive mechanisms.

442

ADAPTATIONS TO DESEPTS

The Poor-will has a basal metabolism which is one-third the
predicted value and is thus an exception to Scholander's general-
ization that metabolism is not adapted to climate. The combination
of a low basal metabolism and a gular flutter which does not sig-
nificantly increase metabolic heat production enables the Poor- will
to dissipate all its metabolic heat at high ambient temperatures,
with a minimum expenditure of water. At thermal neutrality, the low
basal metabolism of the Poor-will is accompanied by a heart rate
which is one-half the v.alue found in birds of comparable size.
Because of a low basal metabolism, the Poor-will also has a high
lower critical temperature and may therefore spend much of its
time outside the thermal neutral zone. It is significant that this spe-
cies hibernates during the winter when it would require a great deal
of food for maintenance of a normal body temperature.

While the stimulus for the onset of torpidity in those species
of desert mammals known to aestivate is not clearly defined, lim-
itation of food in at least two species, Perognathus longimembris and
Perognathus californicus. causes periodic torpor.

Hibernation and aestivation in the mohave ground squirrel illus-
trate the same physiological characteristics and are differentiated
only by the level of body temperature during torpor and the season
in which torpidity occurs.

Under laboratory conditions, the round-tailed ground squirrel
(C. tereticaudus) is intermittently torpid during the summer and
fall, but does not become torpid during the winter or spring. There-
fore, in terms of natural history, this species could be considered
to be an aestivator and not a hibernator.

It is postulated that competition, in the sense of utilization of
a common resource which is in short supply, between the sym-
patric desert ground squirrels is minimal because of differences in
their patterns of metabolism.

The antelope ground squirrel, which is not capable of torpidity
has a broad array of thermoregulatory mechanisms adaptive for its

443

HUDSON

niche. Among its adaptive patterns are:(l) tolerance of ambient tem-
peratures up to 42.6 C for periods of 2 hours, (2) a thermal neutral
zone extending from 30 C to 42.6 C without a marked upper criti-
cal temperature, (3) supplementary evaporative cooling by active
spreading of a copious secretion of saliva over the body when the
ambient temperature exceeds 39 C , (4j dependence on hyperthermia
even at low ambient temperatures (30 C) for radiative-convective-
conductive dissipation of heat, and (5) effective capacity for unload-
ing accumulated body heat, by periodically returning to the cooler
subterranean environment.

In an ecological context, problems of thermoregulation for
desert birds and mammals become intimately linked to the complex
interrelationship between availability of moisture, level of pulmo-
cutaneous water loss, and capacity for water conservation. A com-
parison of renal concentrating capacity among several desert rodents
offers some insight into the extent of adaptation for water con-
servation. Ranking those species for which data are available in
order of ability to concentrate urine one obtains the list: D.
merriami > Citellus leucurus > C. tereticaudus >Neotomaalbigula.

Only D. merriami, whicn is primarily gramnivorous, is able to
maintain body weight on a dry diet while the ground squirrels and
wood rats depend on availability of succulent foods to satisfy their
water requirements.

444

ADAPTATIONS TO DESERTS

LITERATURE CITED

1. Bartholomew, G. A. and T. J. Cade. 1956. Water consumption

of house finches. Condor 58:406-412.

2. Bartholomew, G. A. and T. J. Cade. 1957. Temperature regu-

lation, hibernation, and aestivation in the little pocket mouse,
Perognathus longimembris. J. Mamm. 38:60-72.

3. Bartholomew, G. A. and T. J. Cade. 1958. Effects of sodium

chloride on the water consumption of house finches. Physiol.
ZooL 31:304-310.

4. Bartholomew, G. A. and T. J. Cade. 1959. Sea-water and salt

utilization by savannah sparrows. Physiol. Zool. 32:230-238.

5. Bartholomew, G. A., T. R. Howell, and T. J. Cade. 1957. Tor-

pidity in the White- throated swift, Anna hummin^ird, and

Poor-will. Condor 59:145-155.

6. Bartholomew, G. A. and J. W. Hudson. 1960. Aestivation in the

mohave ground squirrel, Citellus mohavensis. Bull. Mus.
Comp. Zool. 124:193-208.

7. Bartholomew, G. A. and R. E. MacMillen. 1960. The water re-

quirements of mourning doves and their use of sea water and
NaCl solutions. Physiol. Zool. 33:171-178.

8. Bartholomew, G. A. and R.E. MacMillen. 1961. Oxygen consum-

tion, estivation and hibernation in the kangaroo mouse, Micro-
dipodops pallidus. Physiol. Zool. 34 (in press).

9. Birch, L. C. 19 57. The meanings of competition. Am. Nat. 91:

5-18.

445

HUDSON

10 . Dawson, William R. 19 54. Temperature regulation and water re-

quirements of the brown and Abert towhees , Pipilo fuscus and
Pipilo aberti. Univ. Calif. Pub. Zool. 59:81-124.

11. Dawson, William R. 1955. The relation of oxygen consumption

to temperature in desert rodents. J. Mammal. 36:543-553.

12. Dawson, W. R. and H. B. Tordoff. 1959. Relation of oxygen

consumption to temperature in the evening grosbeak. Condor
61:388-396.

13. Hudson, J. W. 1962. Role ofwaterinthe biology of the antelope

ground squirrel, Citellus leucurus. Univ. Calif. Pub. Zool.
(in press) .

14. Lee, A. K. 1960. The adaptations to arid environments in wood

rats of the genus Neotoma. Ph.D. thesis, Univ. Calif. Los
Angeles Libr. Ill pp.

15. Odum, E. P. 1945. The heart rate of small birds. Science 101:

153-154.

16. Schmidt- Nielsen, B. 1960. Urea excretion, p. 82-100. In Kurt

Kramer and Karl J. Ullrich, (ed.), Nierensymposium.

17. Schmidt- Nielsen, K., B. Schmidt-Nielsen, A. Brokaw, and H.

Schneiderman. 1948a. Water conservation in desert rodents
J. Cell, and Comp. PhysioL 32:331-360.

18. Schmidt- Nielsen, K., B. Schmidt- Nielsen, A. Brokaw, and H.

Schneiderman. 1948b. Urea excretion in desert rodents ex-
posed to high protein diets. J. Cell, and Comp. Physiol. 32:
361-379.

19. Schmidt- Nielsen, K., B. Schmidt- Nielsen, S.A. Jarnum.andT.

R. Houpt. 1957. Body temperature of the camel and its rel-
ation to water economy. Am. J. PhysioU 188:103-112.

446

ADAPTATIONS TO DESERTS

20. Scholander, P. F. 1955. Evolution of climatic adaptation in

homeotherms. Evolution 9:15-26.

21. Scholander, P. F., R. Hock, V.Walters, and L. Irving. 1950.

Adaptation to cold in arctic and tropical mammals and birds
in relation to body temperature, insulation, and basal met-
abolic rate. Biol. Bull. 99:259-271.

22. Tucker, Vance. 1961. MS.

447

HUDSON
DISCUSSION

VEGHTE: What is your definition of torpor; and is it reprodu-
cible?

HUDSON: Do you mean is torpor reproducible in the particular
species'? Can I get an animal repeatedly in torpor? Yes, it is very
reproducible. We define torpor in two ways.Firstof all, the animal
has a body temperature which is within a degree or so of the envi-
ronmental temperature, and then secondly, he must be capable of
spontaneously arousing so that we could not include any application
of heat in order to get arousal for the animals. Incidentally this
spontaneous arousal is accompanied by shivering and other classical
manifestations of hibernation.

HANNON: While you are defining things, would you define
"estivation"? Is there any difference between the two?

HUDSON: Well, it looks like there is not, at this point. I
think a lot more work has to be done. I am not absolutely convinced
that there are not some subtle differences in the physiological
mechanisms of estivation and hibernation so that, as of now, esti-
vation is the hibernation response which occurs in the summer,
and, therefore, occurs at fairly high ambient temperatures.

HANNON: I am asking about torpor versus estivation. Is it
the same or different?

HUDSON: Well, it seems to me this kind of thing right now is
only a matter of opinion about usage of the word "torpor" rather
than being based on very much factual information. I am of the
opinion that estivation is a much more intermittent and brief kind
of a response than hibernation. Certainly both cases illustrate
torpor.

WEST: I would like to comment on the difference between
results on heart rate responses of desert birds compared with
the sub-arctic birds that we have been working on. We find that
there is a continual linear relationship of heart rate to decreasing

448

ADAPTATIONS TO DESERTS

temperature as far down as we record it, and this goes to a
little below 0 C. We found we cannot get any leveling off as
high as we have measured it, which is about 32 C. You do not
find a leveling off or thermo-neutral zone type of thing, as Dr.
Hudson found in the Poor-will. We found also that at the very low
temperature, the shivering was so intense that it obscured the heart
rate except at very short intervals, when the heart rate would come
through. I wondered how you recorded your heart rate.

HUDSON: Of course, we started off by measuring it in the
thermal neutral zone and the Poor-will is probably a particularly
good bird for this sort of thing, since it is quite tractable. As
we get below the lower critical temperature of course the shiver-
ing begins to appear on the EKG record, but does not make it
impossible to pick out the QRS complex until we begin to get down
to ambient temperatures around 20 C. Now, at those tempera-
tures, we have found that by giving the bird, and it appears to
have an extremely rapid and sensitive response to this, a quick
burst of heat, not enough to seriously interfere with its meta-
bolism or its body temperature in any way, that it will imme-
diately cut out shivering and then we can pick up a clearer EKG
record. Then in a matter of minutes, of course, it starts to shiver
again. 1 wouM like to counter by asking you a question, and that
is; do you find any sort of a correspondence between the lower
critical temperature of the heart rate and metabolism, or are all
your measurements of heart rate made in the thermo-neutral
zone?

WEST: I never find a thermo-neutral zone for the small birds
I have studied. 1 never go to high enough temperatures. Unfor-
tunately, we are so concerned with cold, we do not go much over
30° C.

HUDSON: Most of the small birds have a thermo-neutral
zone or point that would be around or above 30 C.

WEST: But we get perfect linear correlation of temperature
on metabolism and on heart rate, as far as we can go up and down.

449

HUDSON

HUDSON: This is the kind of thing that will just take more
measurements of different kinds of birds.

WEST: I am interested in seeing the way your heart rate falls
off at the lower temperature, then goes flat; yet the metabolism
continues to fall.

HUDSON: This may be a factor that is associated with hiber-
nation, because these are all species of birds and mammals which
have the capacity to hibernate or estivate.

WEST; There must be a change in the stroke volume.

HUDSON: Yes, if I can assume you mean that it is suggestive
that the stroke volume changes at the place where the heart rate
levels off?

WEST: Yes.

HART: Or the utiUzation.

HUDSON: Yes, utiUzation or both.

VEGHTE: What is the duration of the burst of heat?

HUDSON: No more than a couple of minutes.

WEST: I think this is probably a safe technique; we are try-
ing to measure heart rates in flight. We let the birds fly for a
few wing beats and as soon as they hit the ground, we get the
heart rate, which is extremely fast. We get it the instant that
they stop flying. I know there is a small lag there but I think that
this same heart rate does carry through.

HUDSON: We have also been able to pick out rates that corres-
pond with the ones that we get where we have given them bursts of
heat from records that have very intense shivering on them.

450

ADAPTATIONS TO DESEFTS

WEST : I think that with the technique I mentioned yesterday,
the power frequency distribution, we can single out the heart
rate. It is so constant. It comes out as a peak in the power spec-
trum, no matter how much shivering is masking it on the oscillo-
graph record.

IRVING: Do you give a Poor- will any test to find what its
mental state is in a thermo-neutral zone? Is it entirely alert?
Can it still do multiplication?

HUDSON: Well, he recognizes me in the thermo-neutral zone.
I do not know whether that is a very good test or not.

IRVING: You do not see any noticeable signs of a mental state
characterizing torpidity? That would be my main question; is
that a normal resting basal rate?

HANNON: I noticed in your oxygen consumption of the Mohave
ground squirrel, going in and out of torpor, that he lowered his
oxygen consumption as he went into torpor. It looked like he may
have lowered it more than he should. When he came out it appeared
that there was an oxygen deficit. The oxygen consumption went way
up.

HUDSON: This is overshoot. Yes, this is characteristic in
arousing from hibernation, and I am not entirely clear on what
this may all mean in terms of the internal physiology of the animal,
at that time, whether there is some sort of a heat storing going
on, assuming that the overshoot does not coincide with attainment
of a normal body temperature. It is easier to explain in animals
that restrict the development of body temperature to the fore
quarters which is different from our desert ground squirrels. That
is, for instance, the 13 lined ground squirrel on arousing from
hibernation, typically has the anterior end of the animal develop-
ing normal body temperature first before the posterior end does,
and we get no such responses. That is, we have never observed
anything like this and we assume that it is related to the fact that
these animals have rather high body temperatures to begin with.

451

HUDSON

EAGAN: Do these animals shiver as they are coming out of
torpor?

HUDSON; Yes. The magnitude of the shivering tends to vary
from one individual to the next, but there seems to be no difference
in rate of arousal correlated with this. One gets almost the impres-
sion that there is some inefficient use of shivering going on in some
individuals .

EAGAN: I think this could explain the higher metabolism. Be-
cause after all, when the animal is completely back to body tem-
perature, then it does cease its shivering.

HUDSON; This would be the explanation for the actual heat
production itself.

EAGAN; And the overshoot?

HUDSON; Yes. Shivering of course will continue on beyond the
overshoot.

JOHANSEN: Have you tried to look for any vascular changes
in the legs by measuring superficial temperatures?

HUDSON: No, we have not.

HANNON: Has there been any measurement of changes in blood
chemistry during the course of torpor? I am getting back to this
increase in oxygen consumption, and particularly, I would think
of lactic acid. Is there an accumulation of lactic acid?

HUDSON: I do not know. The intubation technique that Lyman
has extended promises to be a good means for finding this kind
of information.*

*Lyman, Charles P. and Regina C. O'Brien. 1960. Circulatory changes in the
thirteen- lined ground squirrel during the hibernating cyde. Bull.Mus. Cornp. Zool.
124:353-372.

452

ADAPTATIONS TO DESERTS

EAGAN; I was surprised at the rapid and dramatic drop in
body temperature in the species you mentioned. Was that the
antelope ground squirrel?

HUDSON: When he was overheated?

EAGAN; Yes.

HUDSON: This is the antelope ground squirrel.

EAGAN: And how many minutes was that, did you say?

HUDSON: Three minutes. Of course this is a small animal.

EAGAN: Is this accomplished just through transfer through
cooler air, or is it through conduction in the burrow walls?

HUDSON: Well, he was transferred into an environment where
the temperature was all the same, so this is artificial, but the
substrate temperature was the same as the air temperature, so
conduction would be an important factor here. They show an inter-
esting behavioral response to this; when they become overheated
or become relatively warm and have the opportunity to spread out
on a cooler surface, they do this by extending their legs out, lying
very flat, and very close to the surface; this has also been reported
by people living in the desert where they can observe these animals
coming into the shaded areas or on to moist concrete.

o
MORRISON: If you put the animal back at 42 C, how long does

it take him to rewarm?In other words, if it took three minutes to

cool, how long will the reverse process take?

HUDSON: We have not done that.

HART: Have you calculated the basal metabolic rate of the
Poor-will in absolute units at the thermo- neutral zone?

HUDSON: In terms of calories?

453

HUDSON

HART: Yes.

HUDSON: No, I just did it on the basis of oxygen consumption.

HART: You made the point that it was very low. I was won-
dering if this was in relation to body size.

HUDSON: This is in relationship to body size. It is using the
equation from Brody in assuming that one cc of oxygen consumed
releases 4.8 Calories.

PROSSER: Does this metabolism fall below the standard
curve?

HUDSON; Yes. It falls about 66% below the standard curve.

IRVING'. What does torpor mean in the dictionary? Does it
not mean a decline in brightness? I am still interested in the nap-
ping state. I was thinking there might be some other observation
that you could make other than whether the Poor-will recognized
you or not at the ther mo- neutral zone.

WEST: Any way to test his reaction?

IRVING: To show whether he was alert or not, or whether he
was taking a nap.

HUDSON: Well, they will feed. I know that the animal is not
in a torpid state at what we call thermo-neutrality because he
will feed quite regularly. Now, if you force feed him when he is
torpid, he will die, apparently because of the decomposition of
food in the gut under those situations, and yet when they are not
torpid they can be fed successfully. Of course a torpid animal
will have his eyes closed.

IRVING: But in the the rmo- neutral state, they feed and eye
reflexes are apparent, seem to be perfectly normal?

HUDSON: Yes, perfectly normal.

454

ADAPTATIONS TO DESEPTS

IRVING; I thinkthat isveryrarewiththe metabolism diminished
to one-third of the normal. But every means possible should be
taken to be sure we are dealing with a more or less regular animal.

HUDSON; Well, they can fly.

IRVING: Can they take off instantly?

HUDSON: Oh, yes, if you open the cage a little too laxly, why
they are gone.

KLEIBER; What saves these torpid animals from predators?
Is there something which protects them?

HUDSON: As you may or may not know, a lot of the success of
this laboratory in working with Poor-wills is because of human
predators who have found torpid Poor-wills on their front lawn and
back yard and in the library. This is the way in which we have
acquired most of our Poor- wills, and I assume that predation must
be rather severe.

IRVING: Maybe they do not taste good.

HUDSON; You do not know that until after you have eaten them.

455

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