AMER. ZOOL, 16:699-710 (1976).
Fat, Energy and Mammalian Survival
RUTH A. YOUNG
Metabolic Unit, Department of Medicine, University of Vermont College of Medicine,
Burlington, Vermont 05401
SYNOPSIS Adipose tissue plays a critical role in mammalian life history strategies, serving
as an organ for the storage of food and energy, as a source of heat and water and as thermal
insulation. The food and energy storage roles are especially important in allowing the
animals to survive food shortages and stresses associated with competition for mates,
territorial defense, gestation and lactation, and to accomplish migrations. The composition, cellularity and anatomical site of adipose depots in a mammal can influence both the
amount of fat stored and its availability and usefulness in any given situation. The fatty
acids and complex lipids in adipose tissue, blood vessels, nerves and brain change in
response to ambient temperature and the low body temperatures during hibernation.
Early nutrition may influence the number of fat cells developed by a mammal, and thus
affect its ability to survive adversity. Desert species develop localized depots which will
not interfere with temperature regulation, while animals in cold environments use their
extensive superficial fat layers as insulation.
INTRODUCTION
The literature pertaining to the role of
lipids in mammalian lifehistory strategies
is quite extensive but scattered. This review will discuss primarily the uses of
adipose tissue with only peripheral mention being given to other forms of lipids.
Mammals use adipose tissue in a variety of
ways in many life situations. Some seemingly strange compromises have had to be
made to enable them to take advantage of
the benefits that these lipid depots offer
while minimizing the disadvantages.
ADI POSE TISSUE AS A FOOD AND ENERGY STORAGE
ORGAN
The lightness and high energy yield of
fat relative to carbohydrate or protein
Author's present address is: Harriet G. Bird
Memorial Laboratory, Stow, Massachusetts 01775
Much of the original research on woodchuck
adipose tissue cellularity mentioned here was supported by PHS AM 10254 and was included in a
thesis submitted to the Department of Zoology, University of Vermont, in partial fulfillment of the requirements for the degree of Doctor of Philosophy.
The thesis research was done in the laboratory of and
with the guidance of Ethan A. H. Sims, M.D., Metabolic Unit, Department of Medicine.
makes it the favored storage form for potential energy in mammals. Unlike carbohydrate and protein, minimal water is
stored with the fat. However, size and
metabolic rate considerations preclude
the possibility of a small mammal such asa
squirrel surviving through a winter four
or five months in duration without food on
body fat alone (Morrison, 1960). Small
mammals must either hoard food in easily
accessible places for winter use or lower
the body temperature and thus the
metabolism so that less body fat is utilized.
A whole spectrum of adaptations have
evolved ranging from maintaining a reduced metabolism with no food hoarding
(the woodchuck), through various combinations of hoarding and torpidity, to dependence on stored food alone (gray
squirrels). The annual weight, fat and food
consumption cycles of the hibernators
have been discussed already in this symposium (Mrosovsky, 1976).
Larger mammals usually have adequate
stores of body fat to last through the winter. No mammal larger than the marmot,
which rarely exceeds 20 kg, is known to
hibernate. The body temperature of the
bear in its winter sleep dropsonly toabout
34°C (Nelson, 1973) rather than the 4-6°C
common for the true hibernators. In fact,
699
700
RUTH A. YOUNG
the relatively warm body temperature of
the bear during winter sleep has generated
much interest recently. The bear can remain in winter sleep for as much as five
months, but is instantly arousable and
capable of defending itself and giving
birth to cubs and nursing them without
eating, drinking, urinating or defecating
during the whole period. There is no net
change in the lean body mass of a nonlactating bear during the winter sleep and urea
production is very considerably reduced
(Nelson et al., 1975). The bear must be living entirely on stored fat, recycling the
nitrogen in the urea back into protein.
This might occur if the urea was reabsorbed from the bladder, converted to
ammonia, and the ammonia was then fixed
by glutamic acid synthesis (Nelson et al.,
1975). In fasting humans 75% of the substrate of the brain is from ketone bodies
and the rest from glucose synthesized
from glycerol and amino acids (Newsholme and Start, 1973). It remains to be
determined whether the bear in winter
sleep has any special mechanism by which
the brain and other organs can subsist entirely on the products of fat catabolism
with no gluconeogenesis from protein.
The bear in summer cannot survive starvation without extensive protein loss,
ketosis, and dehydration (Nelson et al.,
1975).
mals. Hibernation enables the woodchuck
to survive the long period of cold and food
shortage in the winter. The gray whale
must migrate from the cold arctic waters
to warm seas where the newborn calves, as
yet unprotected by thick layers of blubber,
can survive. Both the gray whale and the
woodchuck must deliver their young early
enough in the season to allow them to
grow, feed at the time of maximum food
availability and arrive at the necessary degree of adiposity to survive the next winter's hibernation or migration. The males
and nonpregnant female whales migrate
and breed in late November and December
while at the calving grounds (Rice and
Wolman, 1971). The young are born 13
months later in late December or January.
Wood chucks breed right after hibernation
ends in early March and the young are
born about 30-32 days later in April
{Snyderet al., 1961; Hoyt and Hoyt, 1950;
Grizzell, 1955).
Both the woodchuck and the gray whale
continue to lose weight during the breeding season, as little food is available. The
lack of food is probably not the only factor
involved in the weight loss during this
period, however. Reproduction itself is a
drain on the body energy reserves. As in
the case of the bear in winter, how the
whale can subsist for a period of as much
as eight months without eating, during
Weight cycles associated with seasonal which she produces a massive calf, generavailability of food, reproductive stresses, ates tons of milk and travels thousands of
and migration are found in many mam- miles is a metabolic puzzle. In animals
mals other than those which hibernate or with a yearly weight cycle, pregnancy and
sleep through the winter. An excellent lactation have been shown to delay the
example of such a yearly cycle of lipid phase of gain in weight. This is true for
deposition and usuage can be found in the several animals including the woodchuck
gray whale (Eschrichtius robustus) (Rice and (Snyder^a/., 1961; Young, 1975), ground
Wolman, 1971). In fact the yearly cycles of squirrels (Heller and Poulson, 1970;
the gray whale are similar in many ways to Hock, 1960), the pronghorn (Bear, 1971)
those of hibernators such as the wood- and the Rocky Mountain bighorn (Woolf,
chuck {Marmota monax). Both have periods 1971). Pengelley and Asmundson (1975)
of rapid weight gain and fat deposition in have shown that female Citellus lateralis
the summer. This is followed by a some- which go through gestation and lactation
what longer period of weight loss as- in the spring commence hibernation later
sociated with hibernation in the wood- in the fall than females which do not (Fig.
chuck and migration in the whale. Of 1), possibly because they do not reach
course the analogy is not perfect at this weight adequate for hibernation until latpoint as the periods of weight loss serve er. This effect is still in evidence one year
quite different functions in the two ani- later.
701
y-
FAT, ENERGY AND MAMMALIAN SURVIVAL
0>
I
>»
3
c P
CM
K)
0)
0>
FIG. 1. Graphical representation of circannual
periods of 18 female Citellus laterahs for over three
years. Upper group of nine had a litter in spring 1970,
lower group had no litters. Black bars indicate period
of hibernation; clear space homothermic period; x =
1
>»
3
->
<n
death; "to cold" indicates transfer of animals from
22°C to 3°C. Artificial photoperiod throughout of 12
hours. (From Pengelley and Asmundson. 1975.
Comp. Biochem. Physiol. 50A:622. Courtesy Pergamon Press Ltd.).
Indirect evidence suggests that the musculus (Myrcha et al., 1969; Myrcha,
energy demands of reproduction in the 1975), and two species of bats, Myotis
female must be very large, especially dur- thysanodes and M. lucifugus (Studier et al.,
ing lactation. One gray seal lost 43 kg in 15 1973). In each case lactation was found to
days while nursing a pup and the pup require three to five times more energy
gained 27 kg in the same time interval than gestation. The energy drain during
(Amoroso and Matthews, 1952). Gray lactation seems to be so great in Myotis
whale calves grow from 3 tons to 23 tons thysanodes that the females become hypowhile nursing (Small, 1971). Food intake thermic in an attempt to maintain body
and body fat of mice change little during stores at an acceptable level (Studier and
pregnancy, but body fat decreases a- O'Farrell, 1972).
bruptly during lactation in spite of a large
Females often have more body fat than
increase in food consumption (Barnett, males. The larger amount of fat in females
1973). There is some evidence from desert may enable them to give birth and nurse
wood rats that females with large litters the offspring in a time of food shortage. In
have a higher mortality rate than those this regard, it has recently been shown
with smaller litters, probably because of in humans that undernutrition delays
the greater drain on the mothers' body re- menarche in adolescent girls (Frisch,
serves (Cameron, 1973).
1972). In females over 16, weight loss
The energy requirements of pregnancy causes cessation of menstrual cycles and
and lactation have been measured in sev- weight gain restores them (Frisch and
eral species including the bank vole Cle- McArthur, 1974). Frisch and McArthur
thrionomys glareolus (Kaczmarski, 1966), the (1974) postulate that a minimum level of
European common vole, Microtus arvalis stored fat is necessary for ovulation and
(Migula, 1969), the laboratory mouse, MILS menstrual cycles in the human female and
702
RUTH A. YOUNG
that the average amount of stored fat (16
kg or 144,000 kcal) would be sufficient for
a pregnancy and 3 months' lactation.
Pinter (1970) has suggested that the
onset of sexual maturity in two species of
grasshopper mice occurs at the time when
the growth rate of the animals markedly
decreases. That happens at about 7-8
weeks of age in one species and at 8-9
weeks in the other. If the body weight to
body length ratios for the mice at each
point are calculated from the data given in
Pinter's report (1970) and the results are
plotted (Figs. 2A and B), the ratios reach a
plateau at about the age suggested by
Pinter as the age of attainment of sexual
maturity. The plateaus are more obvious
in the females than in the males. Possibly
the attainment of a certain body weight for
body length is also necessary for reproduction in these animals.
The breeding period is also a time of
stress for males. Male arctic ground squirrels (Hock, 1960) and male woodchucks
(Snyder et al., 1961) arouse from hibernation several weeks before the females,
even in captivity (Young, 1975). Early
spring is a time of cold and food shortages
so the animals continue to lose weight. As
in many other hibernating rodents, the
testes of these animals are found in the
scrotum only during the spring breeding
season. The first stages of spermatogenesis take place in the fall, but the last stages
probably do not take place until after hibernation ends in the spring (Hock, 1960;
Christian et al., 1972). It is possible that the
earlier arousal of the males is necessary for
the final development of the spermatozoa
and the descent of the testes (Hock, 1960).
In several other animals there is a seasonal fattening of the males curiously called the "fatted" male phenomenon. This
was first described and named for the
squirrel monkey (Saimiri sciureus) by
DuMond and Hutchinson (1967). In these
animals the mating season is associated
with active spermatogenesis, increased
weight and skinfold thickness and increased aggressiveness among the males.
T h e increased weight probably gives the
dominant males an advantage in any
fighting over females and also serves as a
signal of ability to breed. During the rest
of the year the males are thinner, more
passive and retiring, and their testes are
inactive.
A similar phenomenon has been described for male sea lions (Schusterman
and Gentry, 1971). There is a rapid gain in
weight in the spring just before the breeding season which coincides with an increase in aggressiveness and territorial
defense. Male pinnipeds are known to go
several months without eating during the
breeding season. The increased weight in
this case is necessary for fasting as well as
for social communication and success in
fighting. In one study of elephant seals,
4% of the males, presumably the fatter,
more dominant ones, inseminated 85% of
the females (LeBoeuf and Peterson, 1969).
ADIPOSE TISSUE AND ADAPTATION TO TEMPERATURE EXTREMES
The role of adipose tissue as a heat
source will not be discussed here. As in
any other metabolic degradation, heat is
released when fat is oxidized. The role of
brown adipose tissue in arousal from
hibernation, in the newborn, and in cold
acclimation has been reviewed sufficiently
elsewhere (Smith and Horwitz, 1969;
Lindberg, 1970; Hochachka, 1974). Instead, the discussion will center on
another way adipose tissue is used in
adaptation to temperature extremes, its
use as insulation by aquatic mammals. Although fur is an excellent insulator for
animals which live on land, fur loses most
of its insulative value when wet (Scholander et al., 1950). Most marine mammals
rely on subcutaneous fat or blubber instead. Effective insulation in cold water is
especially necessary as water transports
heat away from a submerged mammal's
body about twenty-five times as fast as air
(Ridgway, 1972). Blubber can be very effective. Bryden (1964) found that the
blubber of the southern elephant seal had
a heat conductivity similar to thatof asbestos fiber. The skin temperature of harbor
seals is nearly the same as the surrounding
water, varying with the seasons and allowing little transfer of heat to the water (Irv-
FAT, ENERGY AND MAMMALIAN SURVIVAL
703
Onychomvs torridus torridus
LJ
0.20
O
§0.15
e>
0.10
0.05
>
Q
O
2 4 6 8 10 12 14 16 18
m
WEEKS OF
Onychomys
0.25
e>
z
2 4 6 8 10 12 14 16 18
AGE
leucoqaster articeps
B
?
0.20
>
S015
0.10
w
0.05
Q
O
ffi
2 4 6 8 10 12 14 16 18
WEEKS OF
2 4 6 8 10 12 14 16 18
AGE
FIG. 2. Body weight/body length ratios for two
times of attainment of sexual maturity. (Calculated
from data of Pinter. 1970. J. Mamm. 51:240-241).
species of grasshopper mice (Onychomys). Arrows mark
704
RUTH A. YOUNG
ing and Hart, 1957; Hart and Irving,
1959).The successful human swimmersof
the English Channel usually have more
than the usual thickness of subcutaneous
fat (Pugh and Edholm, 1955). When there
is a need for marine mammals to lose heat,
blood vessels which bypass the blubber
allow heat dissipation from the skin. Flippers and flukes also allow heat loss, the
amount being controlled by changes in
blood circulation (Tarasoff and Fisher,
1970).
When the animal hauls out on the land
or on ice, however, thick b lubber can be a
great barrier to heat dissipation. Sea lions
can lose to sand less than 25% of the
metabolic heat formed (Ohata and Whittow, 1974). Elephant seals and sea lions
are so well insulated for life in the sea that
they cannot maintain thermal equilibrium
on land above certain low ambient temperatures without resorting to such behavioral techniques as flipping sand,
changing posture or wetting themselves
with sea water (White and Odell, 1971;
Whittow et al., 1972). The Weddell seal
seems to be an exception. In spite of its
thick layer of blubber, it can acclimatize to
temperatures of 20°C or more without resorting to behavioral thermoregulation
(Ray and Smith, 1968). Although they are
probably helped by their insulating fur
(Ray and Smith, 1968), the recently discovered (Molyneux and Bryden, 1975) arteriovenous anastomoses beneath the
epidermis of the body and flippers of
these animals are probably of great importance in heat dissipation.
Many marine mammals have their pups
on land or on the ice. Davydov and
Makarova (1964) have done an excellent
study of the Greenland seal, studying the
pups which initially have a hairy juvenile
coat and no subcutaneous fat as they develop the thick layer of blubber seen in the
adults. As the blubber develops, the pups
increase their tolerance to cold sea water
and the blood circulation transfers less
heat to the surface tissues where it would
be lost. Similar changes occur during
growth of the young Weddell seal (Ray
and Smith, 1968).
As mentioned above, all animals which
spend a great proportion of their time in
cold arctic seas do not depend entirely on
blubber for conservation of heat. Polar
bears combine the use of blubber with a
thick coat of fur (0ritsland, 1970; FrischeZ
al., 1974). Another animal which has received a lot of attention lately is the sea
otter. The sea otter has little or no subcutaneous fat and depends entirely on its
thick fur for insulation (Kenyon, 1969;
Morrison et al., 1974; Tarasoff, 1974). If
the fur becomes soiled, it absorbs water
and the animal becomes chilled and dies.
Sea otters eat approximately one quarter
of their body weight in food a day (Kenyon, 1969; Morrison et al., 1974) and have
an extremely high metabolic rate (Morrison et al., 1974), probably because of the
low insulative ability of fur.
Animals which are subjected to cold are
not the only ones which need to be concerned about insulation. The desert
mammals need enough fat to serve as food
in times of food shortage, but cannot afford to allow subcutaneous fat to prevent
heat loss. The camel, the fat-tailed and
fat-rumped sheep and the fat-tailed marsupial mouse (Sminthopsis crassicaudata) and
others have solved the problem by having
localized fat depots in body regions where
they will not interfere with heat regulation. Some African tribes which inhabit
desert regions have developed a similar
solution, steatopygia. These fat deposits in
the buttocks are found mainly in the females and develop at puberty (Shattock,
1909). They very likely serve as extra energy reserves for pregnancy and lactation.
Shattock in his classic paper in 1909 described the localized fat depots in the various animals and humans, and then had this
to say about the Hottentots: ". . . among an
uncivilized, wandering people this local
accumulation of fat would be of a decided
advantage as a food reserve in enabling the
individuals so favored to survive through
an adverse extremity."
ADIPOSE TISSUE AS A WATER SOURCE
Fat is an excellent water source, yielding up to approximately 1.07 gm of
metabolic water for every gram of fat
FAT, ENERGY AND MAMMALIAN SURVIVAL
oxidized. The Schmidt-Nielsens have
done very careful studies of the water balance of the kangaroo rat, a desert rodent
which does not drink and which subsists
on dry plant material (Schmidt-Nielsen
and Schmidt-Nielsen, 1951 and 1952;
Schmidt-Nielsen, 1964 and 1975). The
kangaroo rat's main source of water is the
metabolic water obtained from its food. It
is able to keep in water balance in relative
humidities of about 20% or more because a
countercurrent mechanism in its nose allows air to be expelled from the body at a
lower temperature than the body core,
thus allowing water vapor to condense in
the nasal passages. Below 20% relative
humidity the kangaroo rat loses more
water in respiration than it forms in oxidation. Large mammals like the camel, on the
other hand, lose much more water by
evaporation from the lungs than they
could gain from the oxidation of fat
(Schmidt-Nielsen and Schmidt-Nielsen,
1952; Schmidt-Nielsen et al, 1956). The
camel survives by tolerating severe dehydration, up to a 30% loss in body weight,
until it can reach a water supply
(Schmidt-Nielsen et al., 1956; Siebert and
MacFarlane, 1975).
Other mammals which might need to
make use of metabolic water are the
marine mammals and the hibernators.
There has been much discussion on
whether marine mammals need to drink
sea water. All indications are that the sea
lion (Pilson, 1970) and the harbor seal
(Irving ^ al., 1935; DepocasgZa/., 1971) at
least can stay in water balance on preformed and metabolic water alone when
able to feed. The harbor seal may not be
able to do this while fasting (Depocas^a/.,
1971).
The hibernators, especially those such
as the woodchuck, which do not eat or
drink during the winter, must receive all
of the necessary water from the oxidation
of fat. In an animal which loses 30-40% of
its body weight in fat during hibernation,
the water formed can amount to an intolerable-volume. Fisher and Manery (1967)
have suggested that, instead of using extreme measures to conserve water, hibernators go through the well-known periodic
705
arousals to allow kidney function and urination to get rid of the excess water and
other end products of metabolism.
ADIPOSE TISSUE CELLULARITY
The size of adipose tissue stores can
change in only three ways: a change in the
sizes of the individual fat cells, a change in
the number of fat cells, or a combination of
the two. There has been some speculation
recently as to which occurs during the
prehibernatory fattening of hibernators.
Weight gain and weight loss in adult rats
(Hirsch and Han, 1969) and in adult humans (Salans et al., 1971) are associated
with changes in fat cell size, but probably
not in fat cell number. To determine
whether this is also true for the adult
woodchuck, studies were recently carried
out in our laboratory at the University of
Vermont (Young, 1975).
Adult woodchucks were captured in the
wild at four different times of the year.
Total body fat was estimated by the dilution of tritiated water and fat cell number
was estimated by the method of Hirsch
and Gallian (1968). Body weight, percent
fat and fat cell sizes increased dramatically from May to October, but there was
no increase in total fat cell number.
There is considerable evidence indicating that the ultimate fat cell number of a
mammal is not fixed at birth, but can be
influenced by diet or severe exercise during early life, before or shortly after weaning (Knittle and Hirsch, 1968; Peckham et
al., 1962; Oscai et al., 1972). It is well
known that animals that can be kept successfully in captivity are usually fatter
than their counterparts in the wild. The
woodchuck is no exception. We have
found that woodchucks born and raised in
the laboratory or those captured at weaning and subsequently kept in captivity are
not only fatter, but develop approximately
40% more fat cells by 14 months of age
than animals allowed to remain in the wild
until captured at one year of age (Young,
1975; Young et al., in preparation). Thus
early nutrition may influence the number
of fat cells formed in the woodchuck and
706
RUTH A. YOUNG
alter the animal's chances of surviving an
especially severe winter.
Rats which are kept at 5°C from weaning
develop an increase in fat cell number if
they are kept constantly in the cold (Therriault and Mellin, 1971). This is probably
not of much importance to burrowing rodents which can create a warm microenvironment in their burrows, but might
be of some significance to animals which
have their young in locations where they
would be exposed to the cold.
SUBCELLULAR AND MOLECULAR ORGANIZATION
OFLIP1DS
All adipose tissue is not the same. Two
areas of the same animal may differ in
structural organization and molecular
composition. It is now well known that the
iodine number, melting point or saturation of the fatty acids of the adipose tissue
in the limbs of both humans and animals
changes in a gradient from the phalanges
to the body (Schmidt-Nielsen, 1946; Irving et al., 1957; Mengetal., 1969) and from
the superficial to the deep body areas
(Cuthbertson and Thompsett, 1933; Dean
and Hilditch, 1933; Garton et al., 1971;
Shultz and Ferguson, 1974), with the more
distal or more superficial area soft he body
having the fatty acids with the lower melting points or more unsaturation. The fatty
acids of pinniped and whale blubber are
also quite unsaturated (Sokolov, 1962).
Irving et al. (1957) have pointed out that
the low melting points for the fats in distal
or superficial areas would be important in
animals which had to withstand very cold
temperatures. If the fats had higher melting points, the limbs might stiffen in the
cold and become unusable. The same authors also mentioned, however, that the
melting point changes could not represent
adaptations to cold as tropical ungulates
and man, supposedly also a tropical
mammal, also had the same gradients.
The fatty acid composition of fat depots
can be influenced by the ambient temperature, however. Pigs (Henriques and Hansen, 1901), rats (Mefferd et al., 1958)
and humans (Schmidt-Nielsen, 1946;
McDonald, 1961) all show variations in
fatty acid saturation in the superficial depots when exposed to changes in temperature. Henriques and Hansen (1901) suggested that the saturation of the fats laid
down depended on the temperature at
the site: the lower the temperature, the
lower the degree of saturation. Shultz and
Ferguson (1974) have cited evidence that
the turnover rate of fatty acids is less in
peripheral tissues than in central ones.
They suggest that the internal depots not involved in insulation are mobilized first. In
support of this, Rice and Wolman (1971)
have reported that the weight loss of migrating gray whales was due more to utilization of internal body fat than to utilization
of blubber.
Hibernators change the fatty acid saturation of their depot fats during the year
(Fawcett and Lyman, 1954; Laukola and
Suomalainen, 1971; Platner et al, 1972;
Ambid and Sable-Amplis, 1974), and these
changes are not diet-dependent (Fawcett
and Lyman, 1954). How do these animals
selectively synthesize and/or deposit fatty
acids of different saturations in different
parts of the body and then change them
depending on the time of the year or the
ambient temperature?
A similar situation occurs in tissues
other than adipose tissue which have
lipids as an integral part of their structure.
Chaffee et al. (1968), found that cold acclimation changed the fatty acid saturation of liver mitochondrial membranes
and microsomes of hamsters. Gloster et al.
(1971) found more unsaturated fatty acids
in the phospholipids of the myocardium
of animals which lived at high altitude
than those which lived at lower altitudes,
probably because of the lower temperatures found at higher altitudes (Gloster et
al., 1972). The hearts of hibernating
ground squirrels (Citellus lateralis) differ in
phospholipid composition from those of
nonhibernating squirrels (Aloia et al.,
1974). Beaver caudal nerves continue to
function when the temperature is as low as
—5CC, tibial nerves to 0°C and phrenic
only to4.5°C (Miller, 1970). A similar situation is found in the arteries of harbor
seals. The arteries in the flippers of these
seals respond to epinephrine down to
FAT, ENERGY AND MAMMALIAN SURVIVAL
707
1-2°C while the renal arteries stop re- which control the composition and locasponding at 15°C (Johansen, 1969). As the tion of deposited lipids.
enzymes of the peripheral and central arteries of the harbor seal are identical
(Somero and Johansen, 1970), the authors
REFERENCES
concluded that the difference must be in
the membrane lipids and the ability of the Aloia, R. C, E. T. Pengelley, J. L. Bolen, and G.
membrane lipids to interact with the horRouser. 1974. Changes in the phospholipid commone at that temperature.
position in hibernating ground squirrels, Cilellus
laterahs, and their relationships to membrane funcLyons and Raison (1970) found a phase
tion at reduced temperatures. Lipids 9:993-999.
change in the isolated liver mitochondria Ambid, L. and R. Sable-Amplis. 1974. Influence de la
of rats and of active ground squirrels at
lethargie hibernale sur la repartition des acides
gras tissulaires chez le Lerot. J. Physiol. 69:135A.
23°C, below which the activation energy
for succinate oxidation increased. This Amoroso, E. C. and L. H. Matthews. 1952. Quoted in
Irving, L. 1972. Arctic life of birds and mammals
change was not found in fish (Lyons and
including man. Springer-Verlag, New York.
Raison, 1970) nor in hibernating ground Barnett, S. A. 1973. Maternal processes in the coldsquirrels (Raison and Lyons, 1971) indiadaptation of mice. Biol. Rev. 48:477-508.
cating that the physical properties of the Bear, G. D. 1971. Seasonal trends in fat levels of
pronghorns, Antilocapra amencana, in Colorado. J.
mitochondrial membranes differ in
Mamm. 52:583-589.
poikilotherms and hibernating animals. Bryden,
M. M. 1964. Insultating capacity of the subGoldman (1975) has found that memcutaneous fat of the southern elephant seal. Nature
brane-bound lipids of the brain of warm203:1299-1300.
adapted and hibernating hamsters differ Cameron, G. N. 1973. Effect of litter size on postnatal growth and survival in the desert woodrat. J.
both in complex lipids and fatty acyl
Mamm. 54:489-493.
chains possibly accounting for the cold- Chaffee,
R. R. J., \V. S. Plainer, J. Patton, and C.
resistant properties of the brain during
Jenny. 1968. Fatty acids of RBC ghosts, liver
hibernation. There is evidence that the acmitochondria, and microsomes of cold-acclimated
hamsters. Proc. Soc Exp Biol. Med. 127:102tivity of membrane-bound enzymes is in106.
fluenced by the unsaturation and fluidity
J.J., E. Steinberger, andT. D. McKinney.
of the membranes (Hazel, 1972; Tanaka Christian,
1972. Annual cycle of spermatogenesis and testis
and Teruya, 1973). How the membrane
morphology in woodchucks. J. Mamm. 53:708lipids are selectively deposited remains a
716.
Cuthbertson, D. P. and S. L. Thompsett. 1933. The
mystery.
SUMMARY AND CONCLUSIONS
Adipose tissue has a critical role in
energy storage and utilization and in the
control of body temperature in mammals.
The composition, cellularity and anatomical site of adipose depots in a mammal
can influence both the amount of fat
stored and its availability and usefulness
in any given situation. The fatty acids and
complex lipids in adipose tissue, blood
vessels, nerves and brain change in response to ambient temperature and hibernation.
It is clear that mammalian lipids play a
greater role than simply that of providing
passive insulation and food storage. It is
hoped that this review will stimulate
further investigation into the factors
degree of unsaturation of the fats of human
adipose tissue in relation to depth from skin surface. Biochem. J. 27:1 103-1106.
Davydov.A. F. and A. R. Makarova. 1964. Changes in
heat regulation and circulation in newborn seals
on transition to aquatic form of life. Fiziol. Z. SSSR
imeni I. M. Sechenova 50:894 (Fed. Proc. 24
[Translation]: T563-T566.)
Dean, H.K. andT. P. Hilditch. 1933. The body fats of
the pig. The influence of body temperature on the
composition of body fats. Biochem. J. 27:19501956.
Depocas, F., J. S. Hart, and H. D. Fisher. 1971. Sea
water drink ing and water flux in starved and in fed
harbor seals, Phoca vituhna. Can.J. Physiol. Pharmacol. 49:53-62.
DuMond, F. V. andT. C. Hutchinson. 1967. Squirrel
monkey reproduction: the "fatted" male
phenomenon and seasonal spermatogenesis. Science 158:1067-1070.
Fawcett, D. W. and C. P. Lyman. 1954. The effect of
low environmental temperature on the composition of depot fat in relation to hibernation. J.
Physiol. 126:235-247.
Fisher, K. C. andj. F. Manery. 1967. Water and elec-
708
RUTH A. YOUNG
trolyte metabolism in heterotherms. In K. C.
Fisher, A. R. Dawe, C. P. Lyman, E. Schonbaum,
and F. E South, Jr. (eds.), Mammalian hibernation III,
pp 235-279. American Elsevier, New York.
Frisch, J., N. A. 0ritsland, and J. Krog. 1974. Insulation of furs in water. Comp. Biochem. Physiol
47A:403-410.
Frisch, R. E. 1972. Weight at menarche: Similarity for
wel 1-nourished and undernourished girls at differing ages, and evidence for historical constancy.
Pediatrics 50:445-450.
Frisch, R. E. and J. W. McArthur. 1974. Menstrual
cycles: fatness as a determinant of minimum
weight for height necessary for their maintenance
or onset. Science 185:949-951.
Garton, G. A., W. R. H. Duncan, and E. H. McEwan.
1971. Composition of adipose tissue triglycerides
of the elk (Cervus canadensis), caribou (Rangifer
tarandus groenlandicus), and white-tailed deer
(Odocoileus virginianus). Can.J. Zool. 49:1 159-1 162.
Gloster, J., D. Heath, and P. Harris. 1972. Lipid
composition of the heart and lungs of rats during
exposure to a low atmospheric pressure. Environ.
Physiol Biochem. 2:125-132.
Gloster, J., Y. Oertel, D. Heath, J. Arias-Stella, and P.
Harris. 1971. The lipid composition of the
myocardium of animals indigenous to high and
low altitudes. Environ. Physiol. 1:77-82.
Goldman, S. S. 1975. Cold resistance of the brain
during hibernation. III. Evidence of a lipid adaptation. Am. J. Physiol. 228:834-838.
Grizzell, R. A. 1955. A study of the southern woodchuck, Marmota monax monax. Am. Midland
Naturalist 53:257-293.
Hart, J. S. and L. Irving. 1959. The energetics of
harbor seals in air and in water with special consideration to seasonal changes. Can. J. Zool.
37:447-457.
Hazel,J. R. 1972. The effect of temperature acclimation upon succinic dehydrogenase activity from
the epaxial muscle of the common goldfish (Carassius auratus L.). II. Lipid reactivation of the soluble
enzyme. Comp. Biochem. Physiol. 43B:863-882.
Heller, H. C. and T. O. Poulson. 1970. Circannian
rhythms. II. Endogenous and exogenous factors
controlling reproduction and hibernation in
chipmunks (Eutamias) and ground squirrels (Spermophilus). Comp. Biochem. Physiol. 33:357-383.
Henriques, V. and C. C. Hansen. 1901. Vergleichende Untersuchungen uber die chemische
Zusammensetzung des thierischen Fettes. Skand.
Arch. Physiol. 11:151-162.
Hirsch, J. and E. Gallian. 1968. Methods for the determination of adipose cell size in man and animals. J
Lipid Res. 9:110-119.
Hirsch, J. and P. W. Han. 1969. Cellularity of rat
adipose tissue. Effects of growth, starvation and
obesity. J. Lipid Res. 10:77-82.
Hochachka, P. W. 1974. Regulation of heat production at the cellular level. Fed. Proc. 33:2162-2169.
Hock, R. J. 1960. Seasonal variations in physiologic
functions of arctic ground squirrels and black
bears. Bull. Mus. Comp. Zool. Harv. 124:115-171.
Hoyt, S. Y. and S. F. Hoyt. 1950. Gestation period of
the woodchuck. J. Mamm. 31:454.
Irving, L., K. C. Fisher, and F. C. Mclntosh. 1935.
The water balance of a marine mammal, the seal. J.
Cell. Comp. Physiol. 6:387-391.
Irving, L. and J. S. Hart. 1957. The metabolism and
insulation of seals as bare-skinned mammals in
cold water. Can.J. Zool. 35:497-511.
Irving, L., K. Schmidt-Nielsen, and N. S. B. Abrahamsen. 1957. On the melting points of animal
fats in cold climates. Physiol. Zool. 30:93-105.
Johansen, K. 1969. Adaptive responses to cold in
arterial smooth muscle from heterothermic tissues
of marine mammals. Nature 223:866-867.
Kaczmarski, F. 1966. Bioenergetics of pregnancy and
lactation in the bank vole. Acta Theriol. 11:409417.
Kenyon, K. W. 1969. The sea otter in the eastern
Pacific Ocean. North American Fauna, Number 68.
Government Printing Office, Washington, D. C.
Knittle, J. L. and J. Hirsch. 1968. Effect of early
nutrition on the development of rat epididymal fat
pads: cellularity and metabolism. J. Clin. Invest.
47:2091-2098.
Laukola, S. and P. Suomalainen. 197 1. Studies on the
physiology of the hibernating hedgehog. 13. Circumannual changes of triglyceride fatty acids in
white and brown adipose tissue of the hedgehog.
Ann. Acad. Sci. Fenn, Series A, IV Biology. 180:111.
LeBoeuf, B. J. and R. S. Peterson. 1969. Social status
and mating activity in elephant seals. Science
163:91-93.
Lindberg, O. 1970. Brown adipose tissue. American
Elsevier, New York.
Lyons, J. M. and J. K. Raison. 1970. A temperatureinduced transition in mitochondnal oxidation: contrasts between cold- and warm-blooded animals.
Comp. Biochem. Physiol. 37:405-41 1.
McDonald, I 1961. Ambient temperature and depot
fatiodinenumberinchildren. Nature 192:363-364.
Mefferd, R. B., Jr., M. A. Nyman, and W. W. Webster.
1958. Whole body lipid metabolism of rats after
chronic exposure to adverse environments. Am. J.
Physiol. 195:744-746.
Meng,M.S.,G.C. West, and L.Irving. 1969. Fatty acid
composition of caribou bone marrow. Comp.
Biochem. Physiol. 30:187-191.
Migula, P. 1969. Bioenergetics of pregnancy and lactation in European common vale. Acta Theriol.
14:167-179.
Miller, L. K. 1970. Temperature-dependent characteristics of peripheral nerves exposed to different
thermal conditions in the same animal. Can.J. Zool.
48:75-81.
Molyneux.G. S.and M. M. Bryden. 1975. Arteriovenous anastomoses in the skin of the Weddell seal,
Leplonychotes weddelli. Science 189:1100-1102.
Morrison, P. 1960. Some interrelations between
weight and hibernation function. Bull. Mus. Comp.
Zool. Harv. 124:75-91.
Morrison, P., M. Rosenmann, andj. A. Estes. 1974.
Metabolism and thermoregulation in the sea otter.
Physiol. Zool. 47:218-229.
Mrosovsky, N. 1976. Lipid programmes and life
strategies in hibernators. Amer. Zool. 16:685-697.
Myrcha, A. 1975. Bioenergetics of an experimental
FAT, ENERGY AND MAMMALIAN SURVIVAL
709
garoo rats and an experimental verification. J. Cell
population and individual laboratory mice. Acta
Comp. Physiol. 38:165-181.
Theriol. 20:175-226.
Myrcha, A., L. Ryszkowski, and W. Walkowa. 1969. Schmidt-Nielsen, B., K. Schmidt-Nielsen, T. R.
Houpt, and S. A. Jarnum. 1956. Water balance of
Bioenergetics of pregnancy and lactation in white
the camel. Am.J. Physiol. 185:185-194.
mouse. Acta Theriol. 12:161-166.
Nelson, R. A. 1973. Winter sleep in the black bear. A Schmidt-Nielsen, K. 1946. Melting points of human
physiologic and metabolic marvel. Mayo Clin. Proc.
fats as related to their location in the body. Acta
48:733-737.
Physiol. Scand. 12.123-129.
Nelson, R. A., J. D.Jones, H. W. Wahner, D. B. McGill, Schmidt-Nielsen, K. 1964. Terrestrial animals in dry
heat: desert rodents. In D. B. Dill, E. F. Adolph, and
and C. R. Code. 1975. Nitrogen metabolism in
bears: urea metabolism in summer starvation and in
C. G. Wilber (eds.), Handbook of physiology, Section 4,
winter sleep and role of urinary bladder in water
Adaptation to the environment, pp. 493-507.
and nitrogen conservation. Mayo Clin Proc.
American Physiological Society, Washington.
50:141-146.
Schmidt-Nielsen, K. 1975. Animal physiology: Adaptation and environment. Cambridge University Press,
Newsholme, E. A. and C. Start. 1973. Regulation in
London.
metabolism. John Wiley and Sons, London.
Ohata, C. A. and G. C. Whittow. 1974. Conductive Schmidt-Nielsen, K. and B. Schmidt-Nielsen. 1952.
Water metabolism of desert mammals. Physiol Rev.
heat loss to sand in California sea lions and a harbor
32:135-166.
seal. Comp. Biochem. Physiol. 47A:23-26.
0ritsland, N. A. 1970. Temperature regulation of the Scholander, P. F., V. Walters, R. Hock, and L. Irving.
1950. Body insulation of some arctic and tropical
polar bear, Thalarclos mantimus. Comp. Biochem.
mammals and birds. Biol. Bull. 99:225-236.
Physiol. 37:225-233.
Oscai.L. B.,C. N.Spirakis, C. A. Wolff,and R.J. Beck. Schusterman, R. J and R. L. Gentry. 1971. Development of a fatted male phenomenon in Californiasea
1972. Effects of exercise and of food restriction on
adipose tissue cellulanty. J. Lipid Res. 13:588-592.
lions. Devel. Psychobiol. 4:333-338.
Peckham, S. C, C. Entenman, and H. W. Carroll. Shattock, S. G. 1909. On normal tumour-like formation of fat in man and lower animals. Proc. Roy. Soc.
1962. The influence of a hypercaloric diet on gross
body and adipose tissue composition in the rat. J.
Med. 2 (3, Pathological Section):207-270.
Nutrition 77:187-197.
Shultz, T. D. and J. H. Ferguson. 1974. The fatty acid
Pengelley, E T. and S. J. Asmundson. 1975. Female
composition of subcutaneous, omental and inguinal
gestation and lactation as zeitgebers for circannual
adipose tissue in the arctic fox (Alopex lagopus inrhythmicity in the hibernating ground squirrel,
nuilus). Comp. Biochem. Physiol. 49B:65-69.
Citellus laterahs. Comp. Biochem. Physiol. 50A:621- Siebert, B. D. and W. V. MacFarlane. 1975. Dehydra625.
tion in desert cattle and camels. Physiol. Zool.
48:36-48.
Pilson, M. E. Q. 1970. Water balance in California sea
Small, G. L. 1971. The blue whale. Columbia University
lions. Physiol. Zool. 43:257-269.
Press, New York.
Pinter, A. J. 1970. Reproduction and growth for two
species of grasshopper mice (Onychomys) in the Smith, R. E. and B. A. Horwitz. 1969. Brown fat and
thermogenesis. Physiol. Rev. 49:330-425.
laboratory. J. Mamm. 51:236-243.
Platner, W. S., B. C. Patnayak, and X. J. Musacchia. Snyder, R. L., D. E. Davis, and J. J. Christian. 1961.
Seasonal changes in the weights of woodchucks. J.
1972. Seasonal changes in the fatty acid spectrum in
Mamm. 42:297-312.
the hibernating and norihibernating ground squirrel &te//«.5 tndecemhneatus. Comp. Biochem. Physiol. Sokolov, W. 1962. Adaptations of the mammalian skin
to the aquatic mode of life. Nature 195:464-466.
42A:927-938.
Pugh, L. G. C. and O. G. Edholm. 1955. The physiol- Somero, G. N. and K.Johansen. 1970 Temperature
effects on enzymes from homeolhermic and
ogy of Channel swimmers. Lancet 2:761-768.
heterothermic tissues of the harbor seal (Phoca xntRaison, J. K. and J. M. Lyons. 1971. Hibernation:
ulina). Comp. Biochem. Physiol. 34:131-136
alteration of mitochondrial membranes as a requisite for metabolism at low temperature. Proc. Nat. Studier, E. H., V. L. Lysengen, and M. J. O'Farrell.
1973. Biology of Myotis thysanodes and M. lucifugus
Acad. Sci. U.S.A. 68:2092-2094.
(Chiroptera: Vespertilionidae). II. Bioenergetics of
Ray, C. and M. S. R. Smith. 1968. Thermoregulation
of the pup and adult Weddell sesi, Leptonychoteswed- pregnancy and lactation. Comp. Biochem. Physiol.
44A:467-471.
delli (Lesson), in Antarctica. Zoologica 53:33-48.
Rice, D. W.and A. A. Wolman. 1971. The life history Studier, E. H. and M. J. O'Farrell. 1972. Biology of
and ecology of the gray whale (Eschnchtius robustiis). Myotis thysanodes and M. lucifugus (Chiroptera: Vespertilionidae). I. Thermoregulation. Comp.
Special Publication 3, Amer. Soc. Mammalogists.
Biochem. Physiol. 41A:567-595.
Ridgway, S. H. 1972. Homeostasis in the aquatic enviof
ronment. In S. H. Ridgway (ed.), Mammals of the sea: Tanaka, R. and A. Teruya. 1973. Lipid dependence
activity-temperature relationship of (Na+, R e Biology and medicine, pp. 590-747. Charles C.
activated ATPase. Biochim. Biophys. Acta
Thomas, Springfield, 111.
323:584-591.
Salans, L. B., E. S. Horton, and E. A. H. Sims. 1971.
Experimental obesity in man: cellular character of Tarasoff, F. J. 1974. Anatomical adaptations in the
river otter, sea otter and harp seal with reference to
the adipose tissue. J. Clin. Invest. 50:1005-1011.
thermal regulation. In R. J. Harrison (ed.), FuncSchmidt-Nielsen, B. and K. Schmidt-Nielsen. 1951. A
tional anatomy of marine mammals, Vol. 2, pp. 111-141.
complete account of the water metabolism in kan-
710
RUTH A. YOUNG
Whittow, G. C, D. T. Matsuura, and Y. C. Lin. 1972.
Academic Press, New York.
Tarasoff, F.J.andH.D. Fisher. 1970. Anatomy of the
Temperature regulation in the California sea lion
(Zalophus califomianns). Physiol. Zool. 45:68-77.
hind flippers of two species of seals with re fere nee to
thermoregulation. Can. J. Zool. 48:821-829.
Woolf, A. 1971. Influences of lambing and morbidity
Therriault, D. G. and D. B. Mellin. 1971. Cellularity of
on weights of captive Rocky Mountain bighorns. J.
adipose tissue in cold-exposed rats and the
Mamm. 52:242-243.
calorigenic effect of norepinephrine. Lipids 6: Young, R. A. 1975. The woodchuck, Marmota monax,
486-491.
asabiomedical model for the study of obesity. Ph.D.
White, F. N. and D. K. Odell. 1971. Thermoregulatory
Diss., University of Vermont. Diss. Abstr. Internat.
behavior of the northern elephant seal, Mirounga
36:2112-B.
anguslirostris. J. Mamm. 52:758-774.