The Emperor Penguin: A Strategy to Live and Breed in the Cold: Morphology,

physiology, ecology, and behavior distinguish the polar emperor penguin from other
penguin species, particularly from its close relative, the king penguin
Author(s): Yvon Le Maho
Source: American Scientist , November-December 1977, Vol. 65, No. 6 (November-
December 1977), pp. 680-693
Published by: Sigma Xi, The Scientific Research Honor Society

Stable URL: https://www.jstor.org/stable/27848168

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 Yvon Le Maho
The Emperor Penguin: A Strategy
to Live and Breed in the Cold
Morphology, physiology, ecology, and behavior
distinguish the polar emperor penguin from other
penguin species, particularly from its close relative,
the king penguin

Although most people picture pen the emperor represents the furthest tion by Kooyman and his co-workers
guins in a setting of ice and snow, the evolutionary stage toward cold ad (1971) that emperor penguins may
sixteen penguin species (representing, aptation (Jouventin 1971b). The only dive to depths of 265 m and stay as
six genera of the family Spheniscidae) living relative of the emperor penguin long as 18 minutes underwater.
are in fact widely distributed in the same genus, the king penguin Studies on the stomach contents of
throughout the Southern Hemi (A. patagonicus), breeds in the more emperor and king penguins have
sphere, from tropic to polar regions temperate climate of the sub-Ant shown that they feed mainly on fish,
(see Simpson 1976). Some species? arctic islands when the lowest ambi cephalopods, and crust?cea (Stone
for example, the Gal?pagos penguins ent temperatures are usually around house 1967). By contrast, information
(Spheniscus mendiculus), which live ?5?C (temperatures as low as ?10?C concerning their terrestrial biology is
on the tropical Gal?pagos Islands? have been recorded). The king pen abundant and well documented (see
never even see snow. Truer to their guin would, therefore, represent an Wilson 1907; Sapin-Jaloustre 1952;
image, seven species do live and breed intermediate stage of evolution Stonehouse 1953,1960,1967; Pr?vost
in the Antarctic region. Of these, toward cold adaptation. A compari 1961,1963; Budd 1962,1975; Mougin
however, only the emperor penguin son of the two species should allow us 1966; Birr 1968; Isenmann 1971;
(Aptenodytes for steri) broods its eggs to understand which vital biological Jouventin 1971a, b, 1975; Bougaeff
and raises its young during the severe characteristics of the emperor enable 1974a; Barrat 1976).
Antarctic winter, when ambient it to live and breed in a colder cli
temperatures may drop as low as mate. King penguins breed primarily north
about -48?C (Wilson 1907)?pre of 60?S, on sub-Antarctic islands lo
sumably colder breeding conditions The largest living penguin, the em cated between Cape Horn and Mac
than any other bird can tolerate (see peror (Fig. 2) has a body mass ranging quarie Island?Macquarie, Marion,
Fig.l). from about 20 to 40 kg, twice that of Prince Edward, Kerguelen, Crozet,
the king penguin (Fig. 3), which and Heard?and South Georgia and
Studies on fossil penguins and pale weighs about 10 to 20 kg, and nearly (perhaps) Northern islands in the
otemperatures suggest that penguins 30 times that of the smallest penguin, South Sandwich Archipelago (Fig. 1).
are primarily birds of cold temperate the blue penguin (Eudyptula minor). This species seems to have been ex
to subtropical environments (see As a rough estimate, the emperor's terminated in Tierra del Fuego and
Simpson 1946, 1975, 1976; Stone body length is about 1 m, while the the South Shetland Islands during
house 1969). As Stonehouse has king and the blue are approximately the last two centuries, but is recolo
pointed out (1953,1960), some genera 0.8 and 0.35 m long, respectively. It is nizing the Falkland Islands (Conroy
would have penetrated southward impossible to give a precise body and White 1973). Although the size of
and succeeded in the sub-Antarctic length for penguins: their size de the entire population is unknown, it
and Antarctic environments. Thus pends on their behavior. An emperor is much larger than that of the em
penguin standing still in the cold, peror: Marion and Prince Edward
supported on its heels (intratarsal islands alone have about 2,000,000
joints) and its tail, and pulling in its kings (Van Zinderen Bakker 1971),
Yvon Le Maho, a graduate of the Universities
of Paris and Lyon, is Attach? de Recherche ?n
head, may be less than 0.8 m high, and the Crozet Archipelago, about
Physiology at the Centre National de la Re while a walking emperor, extending 900,000 (Barrat 1976).
cherche Scientifique. Since 1971 he has been its neck, may be as tall as 1.3 m.
in charge of a project (sponsored by the The emperor penguin breeds between
French organizations TAAF, EPF, and As in all penguin species, the life of 66?S (Wilkes Land) and 77?S (the
ERBAA) on the energy metabolism of Ant
arctic penguins. Part of this paper is based on emperor and king penguins is char coast of the Ross Sea). Only six indi
a seminar given in the Department of Biology acterized by the alternation of feeding viduals have been observed north of
at Harvard in January 1976. The author periods in the sea with fasting periods 60? S (Conroy 1975). Most colonies
thanks Drs. P. Jouventin, J. L. Mougin, and B. imposed by terrestrial sojourns for
Pinshow for helpful discussions and sugges
are established on sea ice along the
breeding and molting. Little is known coasts of the Antarctic continent,
tions. Address: Laboratoire de Thermor?gu
lation, CNRS, Universit? Claude Bernard, 8, about the marine biology of these two with a few exceptions such as the
Avenue Rockefeller, 69373 Lyon Cedex 2, penguins. Among the most inter Taylor Glacier colony (67?28/S,
France. esting data available is the observa 60?53 ), which is situated on the ice

680 American Scientist, Volume 65

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Figure 1. The breeding colonies of the emperor 0"
penguin, Aptenodytes forsteri, and the king
penguin, A. patagonicus, are clustered around
Antarctica and the sub-Antarctic islands. The
rookeries of the emperor penguin, which
probably breeds in a colder climate than any
other bird, are located between 66?S and 77?S; Atlantic Ocean Indian Ocean
no breeding colonies?and few individuals?
are found north of 60? S. Their closest relatives,
Marion and
the king penguins, breed in the more temperate South Prince Edward is.
climate of the sub-Antarctic islands. (After South Sandwich Is. Crozet Is.
Pr?vost and Mougin 1970 and Watson 1975.) Georgia f
Falkland Is.
uth d *Kerguelen Is.
Wecddell
shelf of the Antarctic continent, and Sao Heard- le
the Dion Islands colony (67?52/S, 90W 90*E
68?43'W) in the Antarctic Peninsula.
60*S
About 30 colonies are known, and the
80S
entire population of the species is Rose Sea
estimated to be only 300,000-350,000 - - Adel le
breeding birds. The largest known - and
colony, on Coulman Island in the
Ross Sea (73?25'S, 169?50 ), was Macquarie Is.
estimated by Harrington (1959) to
consist of about 100,000 birds. Only Pacific Ocean e
300 birds breed in the Dion Islands
colony. In the other colonies there are eNew
generally 2,000 to 3,000 breeders. * emperor penguin Zealand
Some colonies probably still remain * king penguin
to be discovered. For example, in ? uncertain 1n0
October 1975, an emperor penguin
rookery, designated the Riiser-Laf sen
Peninsula rookery, was discovered on
the sea ice by Japanese test-flight
crewmen (Hoshiai and Chujo 1976),
and, in another Antarctic site, on In
Molting molt in 30 to 40 days, decreases from
about 35 to 20 kg (Le Maho et al.
accessible Island, emperor penguins In comparison with other birds, the 1976). Besides the additional energy
have attempted to start a new colony duration of the molt is particularly needs associated with decreased in
(Jonkel and Llano 1975). short (about one month) for both king sulation from feathers during the
and emperor penguins. The molting molt, the energy required for the
While king penguin rookeries are lo season lasts three months (Novem synthesis of new feathers may explain
cated on the sand seashores of the ber-January) for emperors and five the rapid loss of body mass. The loss
sub-Antarctic islands, emperor pen months (between the end of Sep for a molting emperor penguin in 20
guins establish their rooteries on sea tember and the end of January) for days at a mean air temperature of
ice that is particularly strong and well kings. All the penguins of a species do +1?C was similar to that for a non
anchored, in areas usually located not molt at the same time: immature molting bird of the same initial body
between the coast of the Antarctic nonbreeding adults, successful mass in 73 days of fasting in winter at
continent and small off-shore rock breeders, and unsuccessful breeders a mean air temperature of -14?C (Le
islands. Although such breeding molt at different times during the Maho et al. 1976).
grounds are a precaution against season. Both species molt during the
storms that might destroy more ex austral summer, when air tempera The process of molting is similar for
posed sea ice, and with it the eggs and tures, for the kings range between both species. The earliest visible sign
chicks, the disadvantage is that the about +5 and +20?C, and those for is the appearance of new tail feathers
rookeries may be far from the open the emperors, between about -5 and that push out the old feathers. Next,
sea. Thus, by contrast with king +1?C. Kings molt on the shores of the ventral and dorsal plumage ap
penguins, emperors may have to cross sub-Antarctic islands, emperors on pears to fade, and new feathers be
hundreds of kilometers of unbroken unbroken sea ice or on islands along come visible within a few days. Al
sea ice before reaching the sea, their the Antarctic coast. though the old feathers remain at
only source of food. Since the ice on tached to them (Fig. 10) to minimize
which the colonies are established After feeding in the sea to store lipids the decrease in insulation, this period
disappears during the summer and proteins as fuel, both species is a critical stage of the penguins' en
months, the birds must have a come ashore and fast during the en ergy metabolism. Decrease in feather
breeding cycle that is synchronized tire month or more of molting. During insulation may partly explain why
with the sea-ice cycle. By contrast, the 31 to 34 days of the king penguin's molting emperor penguins were ob
king penguins are not subjected to molt, its body mass decreases from served to shiver at an air temperature
any restrictive cyclic terrestrial con about 20 to 10 kg (Stonehouse 1960). of about 0?C, while nonmolting em
dition. The body mass of emperors, which perors do not shiver above about
1977 November-December 681

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 anti. ,i
.. z:. t.'! rf
! .. i 9.N}N::e.. n::
e ': P,:n. a; rsa_::.
n..?
.
.,... "a.
eF'"'e:
L": _F. ..n
:.r.
l.:r'lrs
,. "oF,
I: rn"rl: .."..
:.r..T. E. h,
;,,qi{ r'LT..,.
!R'1. .:..?: .x:3'
:..;Pd
_rd' .:...r.A"n.r'+'
li'e'? .it.,
:s':?::'-.:.Q.:A !; ...f.:'";:
4..L::e.a..rr
. rs r. ..::":'.
F : t:.; "--",..
+.:. , r'4,.16,'r:..r:'a5..,
+s. ; ;8 t.:" .--.:
'q S: ..]
:.r...1 .;yr ln: ..-
,. ' .'..11:..1 3. i ;yi,.:.:.
:.i3. hY.!3"_~ytn.i.u, "xigp"-n; ^.N .?? .FI". -,.
... ... :....::.:. ,. I(T W A: -,T;..:..::. ^. e...:r::".:,,. .:I,........ 4.:f:,:" Y;:?.;:' ;:"r,......:.i;: n;aar.: n _i;
u4:A. ",ti .{,
,,"~IU1 :-:.[
,.."r.
?[3R" ; '!!7
:.:4.':r! n r ef, - .";; .
,r ["r"'i
.1..: yyxraP' p0.. 'I
laF.!--. ,:.-:....:': "%ij.
.: .rr;4.e ": y ;..1j .::R ri .?.?Y;.: ;':::,..- .
Orr. ..... . I....n.... .. ..z..... .... .... .... r.. .. .... i'i- 1:

$
. r" gt A {r g 3..
aarr a a"...... le ... .r ? a...
. e fa ...
. ntl .. " "rYfe..
.. 4 . s9 _n:T. .. :.:.r:... .. . .. ... .. .-. . ..5:...
n ...5 _..al
ry'... a , lm.,i.
n "e....
Y ?7r
"_.n ..i
S :r ' Qn.
" ......
i " { u 1. . . ....r .... c:;
e - Q .1U , . .. r.. Jf } F e"n n. I
4 ya

-'i" e3:. ' '

F.-g sr
.R.L -?
3. _ ...
r+ cif - .. ; "!:/.
cede iI x.:. {.' . . : .
Figure 2. The emperor penguin is the on
5 rg" ' 4
penguin species that incubates its eggs a
.

I i .. .. .,. :
.. .. ..:..... .;!'F::: erY9;2:.
. ..:'' ....; !" :1:;::J::in?. iu.::::s :::.'"' ::t?"vSB "alei
A "d
raises its young in the below-freezing temp
i.: atures of the Antarctic winter. Several mo
mar-s'e, ' ... :.9*: :-,i:::::= phological, physiological, and behavioral
'' , ,r:.. - - l am _a ;' :: . .
aptations have allowed the emperor not only
: a survive but to breed under these drastic
matic conditions. Among them may be t
di'':f :A:.g.,. :" '.d :f.: ;d"?n' :, .-: .... A}.. :'" ::
emperor's size: at approximately 1 m high, it
r...rsyl.. ;.?x
the largest living penguin species. (All pho
graphs are by the author.)

qr.. .. -4'5y'+ e'if(.'i-yT-aT ej ," yl

^ ..:r$ a" .:Ye:% pi..4::SQr. ""

-. ,.:....... :.... ..;e a s:. ?..:: ..". ... ....: :/: :" . .11 ... "d. p. " " ! F . ial..:Ss '1NF';,..
,e
'
plna. :.... :. . , . t..: L'!.e'; ' ::,.. .5,.68".x,3. 'r'i:k._:
:....:.

d. 1. t
.. ...... ......u5 ..+":: r.n ..... s.. .. .. ....,, . ... r :.: i.=T:",.f} 5 '::;.;.:n. : i
charge of the egg. Then she leaves
.. f
s .3. ..r_:?..:':
::..,:;..r?:.;: v.:::::;:::45.
:.: :... ... f
:r.y'yd? 8. ..rA'..n' ' ; 4'.Q
ry': rry y
rn r...TArti ; 'y; ...
. . 1;,..:.. :lux.^ ; ,
. .. . .. ..:....
l. .'Y. +.,",u:,f'}y
with the male while she goes to the
to feed. The incubation lasts 54 or
3
I.E.~ 4. S5
... '3. ft.
saA s;

days; the first 55% is assumed by t

male, before he returns to the sea, a
11

the last 45% by the female, who ha

Y

just come back from feeding. (Da

. are from South Georgia Island; ther
may be slight differences in oth
breeding areas.)
".i" :::.; "e ry : _ ,..,rtae: n,

" '?eL"^.ix'; i, . 1 x34':7 eii?':t::S';:

There are no nests: the single egg
u.R

..d.,,;.,......'::...rr
.:.,d:
y...,:.::..,." . :....
n.. :.-:::.:
. .....;.":};.,: ::.. .:..;.:.....
".... .
.... "
... .'.a III 'sr
..,?.
...."... :.x:
^. .,..,:,m
l4'-4'.1:1.:':::"16;
.'; s"i::'.. :'Y. ra?.r:
:"...'"
:Ar.r.8:.dtiT.."....n:pe-.";.:::::x:.v'r';.:."''i:::: : :' l!e.?r :'
. ....:.:... .
x

held between the feet and the body

.F :..rfa::11
e. ;}.r'' x1,g ..al.. reji?.r..i:.:::..
III

the standing adult. It rests on th

ventral surface of the tarsometatars
and the plumage and an extensiv
:1 . .. U.T. ;
fold of abdominal
.ie"... .
skin serve as
f..::.C

y
r:
.
brood pouch. The fold of abdomin
e1 ll . skin is a small ellipsoidal patch of sk
:"ssx: - .A ' . that remains free of feathers and b
comes dilated as incubation begin
.ar<-;::. : yr.: ,.. . .
This mode of incubation allow
jt
certain amount of mobility, since th
:Z. ' . .'fix . incubating adult can take very smal
cautious steps. The king penguin
fends its incubating territory, whi
is defined by the radius of bea
:.::... .... ...:-e ':. . V ,y,.
_
...?f. .L.":
:.",;: '' .'a.4 .::
.':':- :f:k'i:"v:M:s;,.
:' ..
,.,>rYQ
'.
ie' :Siy%
IdA'.;. .,M 4':. :. ?S
' pecking or flipper-slapping within i
reach, and the sum of thousands
these mobile territories offers a fa
cinating sight to visitors of the su
Antarctic islands (see cover). T
duration of the male king pengui
fast, including preincubation a
incubation time, is about 40 day
During this period the climate
mains temperate?the lowest te
peratures being around -5?C.

The chick does not move from t

-10?C. When the new dorsal and
ventral feathers protrude about 1 cm
upper surface of its parent's fe
during the first week of its li
tection against predators, such a
Breeding behavior(Stonehouse 1960). This allows pr

or more from the surface ofAfter

the skin,
they have molted andskuas and giant petrels, as well a
then fed
the old ones fall out. When for
these new
several weeks in the sea, king
against cold, until the chick is able
feathers have almost reached theirreturn to their rookery
penguins controlfor
its own body temperature. B
mature length, some of the courtship
upper and and breeding. When they
the fourteenth or fifteenth day th
lower parts of the bodyarrive,
are still
males weigh 16-17 chick
kg and fe remain off its parent's fe
may
males
molting. After renewing their 14-15 kg (Stonehouse
plum for 1960).
an hour or so, preening in the s
Sometime
age king penguins enter the sea to between November andfor food from time to tim
and calling
feed for 2 to 5 weeks (Stonehouse As the of
April, the female lays a single egg chick progressively acqui
1960). Emperors go to sea for 2 to
about 3 g. During the first
300 few temperature regulatio
independent
months (Pr?vost 1961). hours of incubation she takes
adultfull
protection becomes less esse
682 American Scientist, Volume 65

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 "IN

... ..., y

5 ,4. """. .,u'3Y 1 S b x . ySV y< i 'C ",

x r . rot Zr; f f y, -; "rrs " r qe ; r

Figure 3. This king penguin is resting on its f V L FF},? '. r.. ! ?'??.c ' sN .L"" Y F>? s ,i.'.. 1 A

heels (intratarsal joints) and fail, a typical ':

s.
"S
Fr"..
'. 'r
L ty
its " #.. .'$ " '-

stance of both emperors and kings. Both , "so .f M I III f, " ?

species also assume the stance when they are +j".,

incubating eggs on their feet and when they are Jg ;;(," .Y: ,. ., ' ;5 ., k ?.i x' e..".- to - !a~ 4 .: +V ys

standing on ice or snow. King penguins, which

are about 0.8 m high, raise their chicks in the f y '. "'
Y
i. s
relatively temperate climate of the sub-Ant
arctic islands. The piece of marine alga in the d Elw wy i l i . A L L rri;$r : .= f4 x? s ' 7 l d 1 ' y yaR' s
lower right-hand corner is probably the giant
species, which grows as long as 50 m, found in
the waters surrounding these islands.

tial, though still useful in limiting

heat loss. By the time it is two months
old the chick is tall enough to reach 9 r i

up to its parent's beak.

The parent feeds its chick by regur

gitating its stomach contents, as is
common among marine birds, which
are able to keep food in the stomach ~fR

without digesting it in order to feed

their young. After the postnatal pe
riod of regular feeding and rapid in
crease in body mass, the chicks are
Aid },5 r, L
fed irregularly for 10-13 months.
During the austral winter (April to f
**
T
g R
p r i A Y l

September) they are frequently left

alone, and temporarily abandoned
chicks often huddle together to min
imize individual heat loss. Without
food during these periods, their
growth is curtailed and they may lose
body mass. It was recently found that
some chicks go without food for up to
3 months before they are fed again {

(Barr?, pers. comm). Growth starts

again around October, when an im 1'. " " #. ? _ . _ +' TTY.. dh ? a .l ,e.
portant increase in solar radiation
'T"

causes a tremendous proliferation of

the marine organisms on which king yy y

penguins feed and both parents once

again regularly feed their offspring.

After molting in 3 to 4 weeks?re

placing their down with feathers?the
chicks leave the rookery to enter the
sea in December or January (Stone
house 1960). The adults also enter the
sea, and for a few weeks they accu
mulate body fat prior to molting and
beginning the next breeding cycle. It
is interesting that the cycle is not
synchronized with the year. There are
about 15 months between one egg and accum
the
the next. Thus an early breeder one (Pr
the op
year may be a late breeder the next, feedin
and wijl be unable to breed success theEmw
fully in the third year. ice flo
bre
of ne
(Jo
Since emperor penguins start to pear,
late
breed at the beginning of winter, their sea is
May
breeding cycle is quite different from pengu
we
that of the kings. During the austral sea, of
196
summer, from January to the end of as 50-
ter
March, emperor penguins feed and mil
rooke
197

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 . . )^[ P?? ?; ^ : . .. ;5 ^ ? ? :. : ^

".'.'V - : ' ;-::'--'? j':'.' ' ^. - ^ :. \. ?

-;!-^^W^?:: ' -^' - . ??? j? ' ' ' - .

. ...;?. " : * ;;; ;;.-i- '''?falas: '^l??G 'W^?^X^?hr#l|$t??

Figure 4. Emperor penguins leave the sea 120 km, to the rookery, where they will court guins shown here are part of a spectacular
toward the end of March, as the short austral and breed. They cover about 2 km an hour; march of 4,000 emperors returning to the
summer draws to a close and the water freezes most walk, a few toboggan by sliding and rookery at Pointe G?ologie Archipelago in
over. They march in single file, often as far as pushing with their feet and flippers. The pen Ad?lie Land in March 1972.

song (Jouventin 1972a). After aDrastic

fast climatic conditions prevail
characteristic of individual penguins
during the period when the male
of 40-50 days, through the time when are presumably the only possible
she lays the egg, the female has lost means of recognition for both em
emperor penguins incubate their eggs.
about 25% of her initial body massNear the colony of Cape Crozier, peror and king penguin couples; in
Wilson recorded average minimal
(Pr?vost 1961). She leaves the newly dividuals have no characteristic
laid egg with her mate and returnsambient
to temperatures of ? 48.4?C in and it seems impossible for
markings,
the open sea to feed. July of 1903 (Wilson 1907). Average a bird to recognize its partner on the
climatic conditions at the Halley basis
Bay of topographical features. Jou
From the beginning of May to mid rookery from 25 May to 24 July ventin 1962 (1972b), who studied the
July, about 65 days, the male incuwere -28?C ambient temperature components of emperor penguin sig
and
bates the egg on the upper surfaces of wind velocity of 6.3 metersnals perby spectrographic analysis, found
his feet, without a nest (Pr?vost second (Jarman 1973). Average daily that the signals break down into wave
1961)?a mode of incubation prac wind speed may reach 40 m/s intrains, the separated by silent pauses, to
ticed only by emperor and king penPointe G?ologie rookery (Pr?vost constitute a simple code with multi
1961).
guins (Fig. 5). The major difference in And in July, solar radiation pleis"unique" combinations.
the way the two species incubate extremely
is limited. It is under these
that in the emperor incubation issevere
as climatic conditions that thethe female is reunited with her
When
males must endure a fast lasting
sumed exclusively by the male, while 115
mate, she takes over the egg or newly
days, including the preincubationhatched
male and female king penguins share and chick. A most striking find
the task. By contrast with king penincubation periods (Isenmann 1971). ing is that, if the egg hatches before
guins, the "territory" of emperorsTheis birds lose about 40% of their the female returns, the long-term
restricted to their brood pouches initial body mass?10-15 kg from an male is capable of feeding the
fasting
(Isenmann and Jouventin 1970). This chick its first meals with an esopha
initial body mass of 34-40 kg (Pr?vost
allows them to huddle together, 1961).
as geal secretion similar to pigeon milk
fasting king penguin chicks do during (Pr?vost and Vilter 1963). However,
the winter. In the colony of Pointe
About mid-July the chicks hatch, and if the male reaches a body mass of
G?ologie Archipelago, which around has this time the females return to about 22 kg before the female has
the rookery. They locate their mates
about 6,000 breeding couples, huddles come back, he will abandon the egg or
of 500 to 1,000 birds are observed
byatmeans of a vocal search. Isenmann chick and return to the sea.
(1971) has described such reunions:
the first stage of incubation. Later,
the male, inactive in the midst of a
during the winter, the incubating After leaving the egg or chick to the
males usually remain huddledhuddle,
to raises his head as if awak female, the male starts off on his long
ening at the call of the returning fe
gether in one giant mass. Sometimes journey back to the sea. Sometimes
birds leave the huddle, especially
male, leaves the huddle, and responds the hungry males encounter seal res
with his own call, thus directing his
during calm days, to eat fresh snow, piratory holes or natural fissures in
mate toward him. Acoustic signals
the only external source of water. the sea ice along the way, but emperor

684 American Scientist, Volume 65

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 ^k^k^kSliit^klk^k^kK? ^^^^^^V?^fl^B^'''''''''^1

penguins do not dive into these holes creased to the minimal level of about havior?a bird may make a mistake in
to feed without risk, for they may be 22 kg), and it may have to go without recognizing its chick's call, it may
attacked by waiting leopard seals (as food while awaiting the presumed want to replace its dead chick, or an
was my personal observation). return of a parent (Fig. 6). During unsuccessful breeder may try to steal
Leopard seals, which weigh about 400
unusually cold days, when snow or ice a chick.
kg and are 4 m long, prey on fish? storms blow outward from the glacial
and penguins, when they are lucky continent, these abandoned chicks The parents' trips between the rook
enough to catch them. huddle together (Fig. 7) as do the ery and the open sea become shorter
adults. and shorter as the ice breaks up. At
The female keeps the chick on her the end of winter, when the chicks
feet (Fig. 5), protecting it against the In addition to starvation, snow and start to molt, the only ice surface that
cold and feeding it by regurgitating ice storms contribute to the tremen always seems to remain is the firmly
sea food from her stomach. The male, dous mortality rate of chicks that are anchored sea ice of the rookery. The
who is once again in the sea, spends abandoned or lost. They may also be proximity of the open sea and the
about 4 weeks accumulating fat and killed by being blown away from the proliferation of marine organisms at
protein reserves and then returns to rookery by strong winds, by falling this time of year allow emperor pen
the rookery in August. He resumes into crevices in the sea ice, or by guins to respond to the increasing
the parental duties and the female predators. During the winter of 1972, demands of their chicks. In Novem
takes her turn to go to the sea to more than 90% of the chicks at the ber, an adult may, in the period of a
feed. Pointe G?ologie rookery died. This few hours, regurgitate as much as 4 kg
excessive mortality was probably due of stomach contents to its chick
A regularly fed chick starts to become to the fact that an unusually long (Pr?vost 1961).
independent of the brood pouch when stretch of unbroken sea ice between
one month old. At first it presents the rookery and the open sea (pre In December, following molting, the
only part of its body to the sunshine; sumably more than 500 km) pre chicks leave the rookery when the ice
then it temporarily leaves the feet of vented the adults from returning to breaks up beneath them. Chicks that
its parent and walks around, return feed their chicks. have not yet completed their molt
ing to the parental pouch at sunset. cannot possibly survive in the sea,
Finally the day arrives when the chick Chicks abandoned by their parents because only feathers afford the
has reached such a large size that only are rarely fed by other adults. Em necessary insulation and "water
its head can be protected from the peror penguins usually feed only their proofing"; incompletely molted
cold by the parental pouch, and then own chick, which they recognize by its chicks may be seen floating out to sea
it is on its own to protect itself from voice. Two or more penguins have on ice floes.
the cold weather. The chick may even sometimes been seen to fight for the
be abandoned before this stage (by a same calling chick (Fig. 8); there It is interesting to note that when
parent whose body mass has de could be several reasons for this be leaving the rookery emperor chicks
1977 November-December 685

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weigh only about 50% of the adult an organ or between different organs). (Bakken 1976). However, as a simple
body mass (Isenmann and Jouventin When we speak of the body temper way to make comparisons between
1970). Chicks of most sea bird species, ature of a homeotherm, we mean the animal species, an older, simplified
when they leave the breeding colony, core temperature: in mammals, rectal model, called the Scholander model,
have attained a body mass equal to temperature is considered a good has proved very fruitful for the last 25
that of the adults, and in some species index of body core temperature; in years. The Scholander model will be
they weigh even more than adults. birds, body core temperature is mea used here to present a simple picture
Chicks of the Ad?lie penguin (Pyg sured in the cloaca. of the comparison of data for energy
oscelis adeliae) are also relatively metabolism in the emperor penguin
small when they leave the rookery; The temperatures in the shell and at with those available for other
they too breed along the coasts of the the surface of the shell vary greatly. species.
Antarctic continent (although on land The surface temperature of a
instead of sea ice), and their breeding homeotherm that is in heat balance is The Scholander model considers the
generally lower than the core tem heat production of animals at rest?
cycle is also short, though, in contrast
perature. In cold air the surface tem
to the emperors, it takes place during the resting metabolic rate. To facili
the brief Antarctic summer. Raising
perature may be lowered further by tate comparison?and to determine
a chick of relatively small body mass
decreasing the blood flow: the arterial the particular physiological charac
compared to the adult therefore blood that flows from the core to the teristics that separate one species
seems to be an important biological shell loses heat, and when the blood from another?the experimental data
adaptation that evidently allows a flow is decreased, the temperatures in should be obtained on the resting
bird to reduce its breeding cycle. the shell and the rate of heat loss are animal under standard conditions in
decreased. a temperature-controlled room
Their parental duties over, the adult (darkness, animal at rest but not
emperors return to replenish their Investigations of the physiology of sleeping, postabsorptive; see King
energy reserves in the sea, and by the energy expenditure generally include and Farner 1961). Moreover, other
end of January they have molted on measurements of core and surface factors must be considered, for ex
unbroken sea ice or on islands along temperatures, as well as of heat pro ample, circadian rhythmicity and
the Antarctic coast. Thus by contrast duction, at various air temperatures. differences in the experimental tem
with king penguins, and although Before looking at the importance of perature programs (Pohl 1969).
they are of much greater size, emperor these measurements, let us consider
penguins raise a chick in a consider how animals achieve heat balance. In According to the Scholander model,
ably shorter time (8 months vs. about the steady state condition, heat loss the resting metabolic rate (M) is
15 months), obviously the conse must equal heat gain to maintain a self-adjusted to equal the rate of heat
quence of the linkage of the breeding constant body temperature. Heat is loss (Q) in order to maintain a con
cycle to the sea-ice cycle?an ex exchanged between the body and the stant body core temperature (T?>).
traordinary adaptation to the Ant environment by conduction, radia The rate of heat loss is directly pro
arctic environment. In order to better tion, and evaporation. Conductive portional to the gradient between
understand how this strategy works, heat transfer is an exchange between body temperature (T&) and air tem
we must explain the physiological the body and ground, air, or water; in perature (Ta)
adaptations of the emperor penguin's the case of air or water, it is increased
energy metabolism. by the process of convection?which
depends on the mass movement of M=Q = K(Tb-Ta)
the fluid that is in contact with the
Energy expenditure body. Evaporative heat transfer from where is thermal conductance (the
Like other birds and like mammals, the body to the surroundings is res opposite of thermal insulation). In a
emperor penguins are homeo piratory and cutaneous. Although particular range of air temperatures,
therms?able to maintain a high heat transfer is usually from the body called the thermoneutral zone, the
constant body temperature (Pr?vost to the environment, when radiation resting metabolic rate is fairly con
1961; Goldsmith and Sladen 1961; from the environment to the body is stant (Fig. 9) and is at its minimum
Pr?vost and Sapin-Jaloustre 1964; strong, the net heat-transfer rate may value?the basal metabolic rate. The
Boyd and Sladen 1971; Pinshow et al. be toward the body. The most im animal maintains this value by de
1976; Le Maho et al. 1976). Most of portant environmental factor in creasing the thermal conductance as
the heat production of a homeotherm fluencing heat exchange is tempera air temperature is lowered. The
takes place in the core of the body. In ture. minimum value of thermal conduc
man at rest, for example, 72% of the tance is reached at the lowest air
total body heat is produced in the In recent years sophisticated models temperature in the thermoneutral
main internal organs, which weigh of heat exchange have been developed zone, called the lower critical tem
only about 5 kg (Aschoff et al. 1971). (see the pioneering studies of Gates perature.
The rest of the body, which includes 1962; Birkebak 1966; Bartlett and
skin and muscles, may be considered Gates 1967; and Porter and Gates When air temperature falls below the
as a shell. The temperature in the core 1969), and the concept of an "opera lower critical temperature, the ?nimal
may reasonably be considered to be tive" environmental temperature? must increase its metabolic rate to
regulated at a rather uniform and the effective temperature of the en maintain its body temperature at a
constant value (in fact, differences in vironment for a specific animal, constant value. The slope of the
temperatures may be as much as combining conduction, convection, metabolic curve below the lower
0.5?C between the different sites of and radiation?has been presented critical temperature depends on the
686 American Scientist, Volume 65

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Hfl when broods
Figure 5. The male emperor penguin the males
thus the fold
egg in a pouch formed by an abdominal
the are relieved by
"bulges"
of
sionally
the
The eggs
conceal either
peaking
absenceor
r^fWlW^ .
at the world from its safety.
females;
of territoriality
newly in emperors,
skin and the tops of the feet. hatched chicks. The chick stayscompared
The photograph in the to kings (see cover), is evident in the
mother's
brood
was taken at about the time of the firstpouch crowded
for the first weeks
hatches, of group shown
life, here.
occa

body insulation of the animal: the
slope is small for animals with a good
insulating layer of fur or feathers.
One way to adapt to cold?though
not a common strategy?is to main
tain a relatively high metabolic rate
and a high body-surface temperature.
The importance of the basal meta
bolic rate of a species in cold-adap
tation may be evaluated by compar
ing the metabolic curves of individu
als within the same species, and then
by comparing the average curve of
that species with average curves for
other (related or unrelated) species.
Th? basal metabolic rate measured
under standard temperature-con
trolled conditions for emperor pen
guins (43 watts) was noi found to be
particularly higher than what could
be predicted from their body mass
(Pinshow et al. 1976) based on general
equations relating basal metabolic
rate and body mass of other bird
species (Aschoff and Pohl 1970;
Lasiewski and Dawson 1967).
This finding is not surprising: a
strategy involving a particularly high
metabolic rate obviously necessitates
a great deal of energy expenditure
and, in consequence, a high caloric
intake. The strategy of emperor
penguins, considering their long food
deprivation, involves saving energy.
Therefore, we must look at the vari
ous mechanisms by which these pen
guins conserve their energy stores.
Energy conservation
There are two possible strategies for
efficient use of energy stores. The first
is to use a fuel with a high caloric
value, and the second is to limit en
ergy expenditure.
Energy in birds and mammals is
stored in three forms?as carbohy
drate, fat, and protein reserves.
Having energy reserves in the form of
fat is a great advantage, since fat
yields more than twice as much en
ergy as the same mass of carbohy
drate or protein and thus fat stores
last twice as long. In addition, storing
fat, in contrast to protein and carbo
hydrate, does not require much water.
Birds, in particular, have a tremen
dous capacity to accommodate an
hydrous lipids that they retain as a
source of energy. Fat is added to the
body without appreciable change in
the body's water content (Odum et al.
1964).
Emperor penguins have important fat
stores: for a body mass of 37.5 kg,
about 10 kg is in the form of fat
(Groscolas and Cl?ment 1976). Dur
ing their long fast, fat is the primary
fuel (Le Maho et al. 1976)?a signifi
cant part of their strategy for using
energy stores at a low rate. It should
be remembered that, in addition to
the energy needed to survive the
winter fast, the emperor penguin
must have enough energy stores left
to enable it to return to the sea: about
1.5 kg of fat is needed for a 200-km
walk (Pinshow et al. 1976).
According to the Scholander model,
an animal may save energy in the cold
by lowering its basal metabolic rate,
by lowering its lower critical temper
ature, and by decreasing that part of
the slope of the resting metabolic rate
curve which is below the lower critical
temperature (see Fig. 9). Energy can
also be saved by maintaining the core
temperature at a lower value. It is well

1977 November-December 687

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 Figure 6. The mortality of emperor penguin
chicks is high. When abandoned by their par
ents, they are rejected by other adults and
therefore forced to fast until one or the other
parent returns. Parents tend the chick by
turns, and should the absent parent be delayed
or killed, its mate will be forced, when its body
mass reaches a critical level, to abandon the
chick and go to the sea to feed. Here a chick
approaches a parent already occupied with its
own young.

of emperor penguins to be about

-10?C. Under natural outdoor con
ditions (which presumably involve
great heat loss by radiation and con
duction), the lower critical tempera
ture was still found to be about
-10?C (Le Maho et al. 1976). The
lower critical temperature of king
penguins under both standard tem
perature-controlled and natural
conditions was found to be around
-5?C (Barr?, Despin, and Le Maho,
unpubl.). Thus according to the
known that the basal metabolic rate Scholander model, it may be con
of mammals decreases during fasting cluded that emperor and king pen
(see, for example, Grande 1964), but guins are able to maintain their body
this energy-conserving adaptation temperatures, without increasing
has not yet been established for the their metabolic rates, in ambient
emperor penguin. However, a similar temperatures that fall to as low as
mechanism was recently found in -10? and -5?C, respectively. By
king penguins (Le Maho and Despin comparison with the lower critical
1976), which suggests that it exists temperatures for other birds, these
also for emperors and may therefore are extremely low. In fact, the lower
contribute greatly to their conserva critical temperature of the emperor
tion of energy. penguin is the lowest known among
birds, with the possible exception of
Measurements taken under standard the Arctic gull (Scholander et al.
temperature-controlled conditions by 1950).
Pinshow and co-workers (1976) have
shown the lower critical temperature How can such a low critical tempera
ture value for the emperor penguin be
explained? Is it mainly the conse
quence of morphology, or is it due to
exceptionally effective thermal in
sulation (and therefore extremely low
thermal conductance)?

To answer this question, the thermal

conductance of emperor penguins was
determined from measurements
performed under both standard
temperature-controlled and natural
conditions. Pinshow and co-workers
(1976) showed that the thermal con
ductance of emperor penguins in still
air reaches its minimum value, which
corresponds to the highest degree of
insulation (a combination of plumage,
'^' ^^^^^ '^^^jj^^?^1 ^^^^^^^^^^^ '
WJ^^? ?iww^^^Bki Ml iilIBi. 11111 w^^^^^^K^^^^^^^^^^K?11^

Figure 7. Abandoned emperor penguin chicks

usually huddle together for warmth while
awaiting the presumed return of a parent.

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subcutaneous fat, and blood flow at other penguins (Stonehouse 1967).
the surface of the body, and a func The value for the king penguin is in
tion of the air movement around the termediate between that of the em
animal), at around the lower critical
peror and those of other penguin
temperature (?10?C), as would be species. The emperor also has pro
expected from the Scholander model. portionately the smallest feet of all
The experimental minimum value of penguins: they are shorter than those
thermal conductance was found to be of the king penguin and less exposed
1.6 watts/m2/?C (Pinshow et al. to cold because of the long tibiotarsal
1976); under natural conditions it was feathers, which fringe and protect the
very similar?1.3 W/m2/?C (Le Maho tarsometatarsus (Stonehouse 1967).
et al. 1976). These values are not ex
tremely low; values for other birds Body-surface areas, including the
range from 0.9 to 3.5 W/m2/?C (Drent beak and feet, of unplucked adult
and Stonehouse 1971). Considering emperor penguins with flippers close
the severe cold in which they live, to the body ranged from 0.55-0.65 m2
emperor penguins do not have the (Le Maho et al. 1976). These values
extremely low thermal conductance are 15-30% below those predicted
that might be expected. Instead, the
explanation for the very l?w critical
temperature of the emperor seems to
be linked to its morphology and be
havior.

Large body/small
extremities
Old laws known as Bergmann's law
and Allen's law state that body mass
tends to be greater and extremities
smaller as an animal is less tropical
and more polar. The most striking
characteristic of emperor penguin
morphology is its large body mass,
which has the advantage of requiring
a much lower basal metabolic rate per
gram of body mass than a smaller
animal (Fig. 11). The rate of the em
peror penguin is about 20 times lower
than that of the hummingbird, for
example. The large emperor penguin
has, therefore, a low rate of energy
expenditure per unit of body mass, 5q
and thus it is capable of fasting much
longer than a small bird; in main
taining its high metabolic rate, the
hummingbird cannot fast more than
a few days. from general equations relating
Figure 8. Occasionally two or more emperor
penguins vie for possession of one chick. It is
body-surface area and body mass of
not known what causes this behavior; perhaps
If in addition to a large body the ex birds. Its large body mass, its shape,
it is a mistake in recognizing the chick's cry or
tremities are very small, the body and its short extremities combineantoadult's desire to replace a dead chick.
surface/volume ratio decreases. give the emperor penguin the smallest
Theoretically, the smallest such ratio, relative surface area of any bird
as far as heat loss is concerned, is ob species. (It is not surprising that its
tained by a large "spherical" animal "nearest" relatives, the king penguins,
with small extremities. The sizes of have body-surface areas 10-15%
the beak, flippers, and feet of the below those predicted and a relative
emperor penguin are not in the same surface area that falls between that of
proportion to its body mass as are the emperor and other birds; Le
those of other penguin species. The Maho, unpubl.) The characteristic
emperor has proportionately a much morphology of the emperor seems
shorter beak (compare Figs. 2 and 3) partially at least to explain its par
and flippers than the small and mid ticularly low critical temperature,
dle-sized penguins; the surface area of which, in turn, contributes to its
the flippers is 23% below that pre strategy of minimizing energy ex
dicted from the regression line for all penditure in cold air.
1377 November-December 689

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Other ways to conserve
energy
Another possible way that a homeo
therm can conserve energy is to de
crease the set point value at which its
core temperature is maintained. The
best examples of this strategy are hi
bernation in mammals and torpor in
bats and birds. Hibernating and tor
pid animals can drop their body
temperature from about 40? C to
about 15?C or below, and since low
ering body temperature decreases use
of energy, their energy reserves last
longer. For example, a torpid bat may
use energy at a rate only one-fortieth
that of an active bat, and its fat re
serves thus last 40 times as long. (For
details on the physiology of torpor
and hibernation, see Schmidt-Nielsen
1975.) The emperor penguin does not
use such a strategy, presumably be
cause its body mass is too great (large
body masses would require too much
time to warm up after hibernation),
and, obviously, because it could not
incubate an egg if its body tempera
ture were considerably lower.
But even excluding this strategy, the
question might be asked whether the
emperor's energy expenditure could
perhaps be reduced by a small but
significant lowering of body temper
ature. In emperor penguins, cloacal
temperatures as low as about 35?C
have been recorded (Mougin 1966;
Pr?vost and Sapin-Jaloustre 1964). It
is not known if these low values cor
respond to a strategy that involves
lowering the body core temperature
(which is usually around 38? C), be
cause, in penguins, cloacal tempera
ture may not be the "true" core tem
perature, as it is for other birds.
Cloacal temperature may normally be
1.5?C below stomach temperature,
and thus may actually be a shell
temperature (Le Maho et al. 1976).
Still another way to minimize energy
expenditure is to decrease heat loss at
the surface of the body. In addition to
the savings achieved by having small
extremities and a relatively small
Figure 10. During the molting of both king and
emperor penguins, the old feather remains at
tached to the new until the new one is about 1
cm long. This presumably limits the decrease
in insulation that would be caused by a loss of
feathers, for although both species molt during
the austral summer, temperatures may go as
low as about +5?C for kings and ?5?C for
emperors.
690 American Scientist, Volume 65
200.145.52.210 on Fri, 26 May 2023 19:04:19 +00:00
Air temperature
Figure 9. The Scholander model describes a
"thermoneutral zone," a range of air temper
atures at which the resting metabolic rate of an
animal remains relatively constant and at its
minimum value?the basal metabolic rate. Air
temperature increases from left to right on the
abscissa.
body-surface area, energy may be
conserved by decreasing heat loss in
the extremities and the surface of the
body.
The temperature at the surface of a
penguin's plumage is close to air
temperature, which may go down to
?40? C in the Antarctic (Stonehouse
1967). As the lowest temperature
measured at the surface of the skin of
an emperor penguin is as high as 32?C
(Bougaeff 1972, 1974b), it can be
calculated that feathers provide most
of the insulation. Plumage resistance
accounts for 85% of the total resis
tance to heat transfer from the core to
the environment in an emperor pen
guin with a core temperature of 38? C
at an air temperature of ?10? C (Le
Maho et al. 1976; see also Jarman
1973). The subcutaneous fat, which
may be 2-3 cm thick, therefore plays
only a minor role in thermal insula
tion. The feet and flippers, however,
are only slightly insulated by feathers
and blubber, and high arterial flow in
such extremities, even when they are
small, would contribute to ? high rate
of heat loss. How does the emperor
penguin avoid excessive heat loss
from its feet and flippers? How does
it prevent venous blood, returning
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from the extremities, from cooling the
body core?
As in the flippers and flukes of whales
(Scholander and Scheville 1955),
there are vascular structures in the
feet and flippers of penguins that
prevent excessive energy expenditure
in cold air (Trawa 1970; Frost et al.
1975). The blood vessels in the ex
tremities are grouped so that they
function as heat-exchange units: each
artery is surrounded by several veins.
The arterial blood is cooled by the
colder venous blood surrounding it on
all sides, and the venous blood is
warmed by heat transfer from the
arterial blood. If this type of heat
exchange system?known as a coun
tercurrent heat exchanger, because
the flood flows in opposite directions
in the venous and arterial vessels?is
efficient, the venous blood can reach
almost arterial temperature before
returning to the body core. Thus, at
the surface of the appendage, there is
a temperature gradient between core
temperature and air temperature. It
must be noted that, when the air
temperature is well below 0?C, the
temperature at the distal extremity of
an animal's appendage is maintained
at about 0?C to prevent the tissues
from freezing. Surface temperatures
of the flippers and feet of the emperor
penguin increase from about 0? to
38?C when measured from the most
distal to the most proximal portions
(Bougaeff 1972,1974b).
Countercurrent heat exchangers are
also known in the limbs of seals, sea
cows, and different species of marine
birds. Moreover, these structures are
not restricted to aquatic animals; they
are found in the limbs of the sloth
(Scholander and Krog 1957); and
even in man there is some exchange of
heat between the main arteries and
adjacent larger veins (see Aschoff and
Wever 1959). Countercurrent heat
exchangers are particularly well de
veloped in penguins. The brachial
artery in the flippers, for example,
divides to form a humeral plexus
(Filhol 1885; Trawa 1970). This
 25
branching is in connection with a ing, and shape of their p
proliferation of associated veins, and therefore partly explain why
the resulting increase in the surface moderate speed have little e
area of the zone of contact between fr heat loss. In addition, it m
arteries and veins ensures a greater
capacity for heat exchange (Frost et
I i* pointed out that large anim
only loosely bound to the law
al. 1975). There are 5 branches of the convective regime (Porter a
brachial artery in the flipper of the toh 1969). Thus the large body
Ad?lie penguin, 7 to 8 in the king, and the emperor is again advant
12 to 15 in the emperor (see Trawa
1970). At the opposite extreme, on r
warm days, body temperatu
In areas of the body where prolonged become dangerously high
association between artery and vein o:ooi pM (u i icr
ample, at air temperatures of
is not possible, there may be extensive 0?C, temperatures of abo
Figure 11. The specific basal
havemetabolic rate
been recorded at the sur
branching of the artery and associ increases with decreasing body mass. Thus the
ated veins to ensure a greater capacity tiny hummingbird has aAd?lie penguins
high specific basal when summ
for heat exchange. Such a structure, radiation
metabolic rate, which must is high
be maintained by and winds a
called a rete mirabile, is known in the (Le
an almost constant supply of Maho,
food. Largerunpubl.).
birds In warm
can go for longer periods without eating.
er, penguins can widen the
heads of birds and apparently ensures
a supply of cooled blood to the brain between the tips of the fea
(see Kilgore et al. 1976). The presence allow air to penetrate into t
of a rete mirabile in the heads of cer mize water loss. Heat age. Opposing
exchange muscles, one
in the
tain mammals is associated with the nasal passageways of the
istic emperor
pair for each feather, co
ability to maintain the brain at tem change
penguin has not yet been in spacing
studied, but (see Sto
peratures below the core temperature 1967).
the mechanism could In addition, the surf
presumably
(see Baker and Hayward 1968; Taylor peratures
contribute to limiting of flippers and f
energy expen
and Lyman 1972). A large rete mira diture, as well as toalmost uniformly
limiting water increase
bile is found in the heads of penguins loss?an important 35?C,
consideration,
and thus these appenda
(Watson 1883; Frost et al. 1975). In an important
since it may be extraordinarily role as heat dis
diffi
addition to the possibility of cooling cult for a penguin This
to leave a dense
is achieved by bypas
the brain in heat-stressed penguins, huddle of thousandscountercurrent
of birds to eat heat exchan
Frost and coauthors have suggested fresh snow as a water source!
the flipper of the jackass p
that the main selection pressure re (Spheniscus demersus), Fr
sponsible for the evolution of this To consider only the relationships
coauthors (1975) observed tha
large rete mirabile has been the need between cold air temperature
marginal vein and
bypasses the
to reduce heat loss from poorly insu energy expenditure would
system andbecan
to therefore u
lated areas of the head. Studies in this the arterio-venous
oversimplify thermor?gulation in the heat exc
field would be of interest. As wind
emperor penguin. High the marginal
velocity vein appar
is a well-known major factor
curs in the
in many penguin spec
Another site of the body where heat severity of Antarctic son 1883),and
weather, it is probably the m
yet
loss can be minimized is the nasal the resting metabolic the
ratecountercurrent
of emperor heat ex
passage. In an air temperature of 5?C, penguins was not significantly
are bypassed in
in these birds.
Ad?lie and gentoo penguins (Pygos creased by winds up to 5 m/s (Le
celis papua ellsworthii) have been Maho et al. 1976). This
Sinceobservation
emperor penguins do
found to recover 83% of the respira can be explained onlycrease
by thetheir
unusualmetabolic rat
tory heat added to the cold inhaled air temperatures
resistance of the emperor penguin'sas low as ?10
(Murrish 1973). This important re since winds
plumage to disorganization up to 5 m/s ha
by the
covery of heat is achieved mainly in a wind. As Stonehouse (1967)
effect has
on their heat loss, it is
chamber within the nasal passage. pointed out: "The penguin feathers
that they are gifted with b
During inhalation, the walls of the seem especially welladaptation
adapted for to
recold. Howev
passageways lose heat to the air, and sisting wind movement.
they The
mustshort,
rely on addition
the temperature of the walls is low stiff rachises of adjunct feathers,
gies when air temperatures
ered (due to evaporation, it may even overlapping like tiles on aand
-10?C roof, are velocity is
wind
fall below the temperature of the in pressed more closely m/s,
together, rather
and the severity of the
haled air). During exhalation, the increased
than parted, by strong byare
winds, and snow and ice
moistened air coming from the lungs likely to be more Under such
efficient drastic climat
than
is cooled, and water condenses on the mammal fur in retaining an undis
tions isolated emperor pengu
cool surfaces of the walls. Such a been
turbed stratification of air found
close toto increase the
the
heat-exchange system exists in vari skin." Down filaments at the
bolic ratebase of
by shivering (Le Ma
ous species (see Schmidt-Nielsen penguin feathers form a What
1976). thickother
un strategies
1972). Its efficiency is increased as dershirt (Pycraft 1907), and emperors
possible for them to survive l
nasal passageways become narrower have, in addition, the fasting
longest in severe cold? It ca
feathers
and wall surfaces larger, characteris of all penguin species.sumed thathave
They also behavior compl
tics that are particularly well devel an unusually complete covering
picture of how of
they minimiz
oped in small desert rodents to mini expenditure.
feathers. The density, double-layer
1977 November-December

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How does behavior save
energy?
Two aspects of behavioral adaptation
should be considered. First, the use of
energy depends on activity. An ex
tremely low level of activity allows the
total rate of energy expenditure to
remain around the resting metabolic
rate. It has been observed that em
peror penguins progressively decrease
their activity shortly after arriving in
the rookery. This reduction is as
sumed to be partly responsible for the
observed decrease in the daily loss of
body mass in free-roaming penguins
after only 4 or 5 days of fasting (Saint
Romas and Le Maho 1976). There are
of course seasonal variations in em
peror penguin activity: birds are more
active in summer than winter, when
they may remain motionless and si
lent for days (Pr?vost 1961; Mougin
1966; Isenmann 1971; Jouventin
1971b).
Second, behavior can help to lower
the metabolic rate by minimizing the
body-surface area exposed to cold air,
and emperor penguins do this
through both individual and group
behavior. Like other penguin species,
when isolated and standing on the ice
they rest on three points: the two
heels (intratarsal joints) and the tail.
The plantar surfaces of the feet are
lifted off the ground, and the toes are
covered by the long lower abdominal
feathers. At the same time, the head
is pulled in and the flippers are held
close to the body. This posture is,
without doubt, important in mini
mizing heat loss and partly explains
the low critical temperature of this
species. To save energy under more
severe conditions, individual isolated
emperor penguins (even with egg or
chick resting on the feet) often lie
down. This has two advantages: heat
loss from high-speed winds is mini
mized because wind velocity is lower
at ground level, where, in addition,
the snow acts as a partial wind bar
rier, and less body surface is exposed
to the air.
When emperor penguins are in a
group, they usually huddle together
during the severe weather. Although
huddling is common in emperor and
king penguin chicks (and has been
observed in chicks of various other
penguin species), the emperor is the
only species in which adults huddle
continuously throughout a large part
of the breeding cycle. A huddle of
emperor penguins often includes as
692 American Scientist, Volume 65
200.145.52.210 on Fri, 26 May 2023 19:04:19 +00:00
many as 5,000 to 6,000 birds, with
about 10 birds/m2 (Pr?vost 1961).
The huddles are not motionless;
movement is extremely slow, but
continuous. The huddle is urged
along by the wind, the rear-flank
birds (those most exposed to the
wind) advancing slowly along the
sides of the huddle in order to be
protected from the wind. Thus, birds
that at first are in the center of the
huddle become members of the rear
flank and move, in their turn, up the
sidelines. During an ice storm that
blew continuously for almost 48
hours, a huddle was seen to move
100-200 m (Pr?vost 1961).
Obviously, huddling allows, in addi
tion to a favorable microclimate
within the huddle, a considerable
decrease in the body surface exposed
by each individual to the air. It is
difficult to determine the efficiency
of huddling as an energy-saving
strategy, because it is awkward to
measure metabolic rates of individual
birds within the huddle; however,
efficiency can be evaluated indirectly
from the rate of loss of body mass.
Pr?vost (1961) observed, by periodic
measurements of the body mass of
penguins alternately left free to
huddle and experimentally isolated,
that huddling cut back the daily loss
of body mass by 25 to 50%. It has been
found also that the metabolic rates
calculated from the daily loss in body
mass of penguins huddling at air
temperatures often well below ? 10?C
were around the basal metabolic rate
for the species (Le Maho et al. 1976).
These findings suggest that huddling
(combined with a low level of activity)
allows the emperor penguin to main
tain its basal metabolic rate in air
temperatures lower than the lower
critical temperature of the isolated
bird. By contrast, the sub-Antarctic
king penguin does not seem to require
huddling to maintain its basal meta
bolic rate, since the air temperature
in the region where it breeds never
falls much below its lower critical
temperature.
The ecological benefit of huddling is
that emperors can go without food for
very long periods. When kept in a
fenced area during the winter?pro
moting decreased activity, but elim
inating the possibility of huddling?a
35-kg emperor weighed 20 kg after
only 60 days of food deprivation (Le
-. 1974a. Observations ?cologiques ? la
Maho et al. 1976). A body mass of 20
kg is below the "critical body mass" of
the adult?i.e. the body mass at
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which lipid reserves are no longer
available (Le Maho et al. 1976; Gros
colas and Cl?ment 1976). It seems
probable that huddling roughly dou
bles their endurance?the male em
peror's winter fast is about 115 days?
and thus makes winter breeding
possible so far from the open sea. The
fact that emperor penguins do not
stake out an incubating territory is
the adaptative basis for huddling?
the vital behavioral strategy that al
lows the bird to live and breed in the
Antarctic cold.
More studies are necessary to com
plete our meager knowledge of this
unique and fascinating creature.
Fields of research full of promise in
clude endocrinology, heat conduction
and radiation, and morphological and
physiological adaptations to marine
life. However, even with the biological
data currently available, we can un
derstand many of the important
characteristics of the emperor pen
guin's strategy to live and breed in the
cold, a strategy that involves ex
traordinary specialization in limiting
energy expenditure.
References
Aschoff, J., . G?nther, and K. Kramer. 1971.
Energiehaushalt und Temperaturregulation.
M?nchen: Urban and Schwarzenberg.
Aschoff, J., and H. Pohl. 1970. Der Ruheumsatz
von V?geln als Funktion der Tageszeit und
der K?rpergr?sse. J. Ornithol. 111:38-47.
Aschoff, J., and R. Wever. 1959. W?rmeaus
tausch mit hilfe des kreislaufes. Deutsche
Medizinische Wochenschrift 84:1509-17.
Baker, . A., and J. N. Hayward. 1968. The
influence of the nasal mucosa and the carotid
rete upon hypothalamic temperature in
sheep. J. PhysioL, Lond. 198:561-79.
Bakken, G. S. 1976. A heat transfer analysis of
animals: Unifying concepts and the appli
cation of metabolism chamber data to field
ecology. J. Theor. Biol. 60:337-84.
Barrat, A. 1976. Quelque aspect de la biologie
et de l'?cologie du Manchot royal (Apteno
dytes patagonicus) des ?les Crozet, Com.
nat. fr. Rech, antart. 40:9-52.
Bartlett, P. N., and D. M. Gates. 1967. The
energy budget of a lizard on a tree trunk.
Ecol. 48:315-22.
Birkebak, R. C. 1966. Heat transfer in biologi
cal systems. Int. Rev. General and Exptl.
Zool. 2:269-344.
Birr, G. 1968. Observations ?tho-?cologiques
? la colonie de Manchots empereurs de
Pointe G?ologie en 1966. L'oiseau et la
R.F.O. 38:53-88.
Bougaeff, S. 1972. Notes pr?liminaires sur
quelques donn?es physiologiques enre
gistr?es chez le Manchot empereur. L'oiseau
et la R.F.O. 42:131-45.
colonie de Manchots empereurs de Pointe
G?ologie (Terre Ad?lie) en 1970. Corn. nat.
fr. Rech, antarct. 33:89-98.
--. 1974b. Etude comparative de quelques
param?tres physiologiques chez deux esp?
ces de Manchots antarctiques, le Manchot
empereur et le Manchot ad?lie. Com. nat. fr.
Rech, antarct. 33:99-110.
Boyd, J. C, and J. L. Sladen. 1971. Telemetry
-.
studies of the internal body temperature of
Ad?lie and emperor penguins at Cape Cro
zier, Ross Island, Antarctica. The Auk 88:
366-80.
Budd, G. M. 1962. Population studies in
rookeries of the emperor penguin. Proc. Zool.
Soc, Lond. 139:365-88.
-. 1975. The king penguin Aptenodytes
patag?nica at Heard Island. In The Biology
of Penguins, ed . Stonehouse, pp. 337-52.
Macmillan.
*
Conroy, J. W. 1975. Recent
guin population in Antarctica
Antarctic. In The Biology
. Stonehouse, pp. 321-36.
millan Press.
Conroy, J. W., and M. G. White. 1973. The
breeding status of the king penguin, Ap
tenodytes patag?nica. Bull. Brit. Antarctic
Survey 32:31-40.
Drent, R. H., and B. Stonehouse. 1971. Ther
moregulatory responses of the Peruvian
penguin, Spheniscus humboldti. Comp.
Biochem. Physiol. 40A:689-710.
Filhol, M. H. 1885. Observations relatives ?
Panatomie de diverses esp?ces de Manchots.
In Recherches Zoologiques, Botaniques et
G?ologiques Faites ? l'Ile Campbell et en
Nouvelle Z?lande 3:65-339. Paris: Gau
thier-Villars.
Frost, P. G. H., W. R. Siegfried, and P. J.
Greenwood. 1975. Arterio-venous heat ex
change systems in the jackass penguin,
Spheniscus demersus. J. Zool. London
175:231-41.
Gates, D. M. 1962. Energy Exchange in the
Biosphere. Harper and Row.
Goldsmith, R., and J. L. Sladen. 1961. Tem
perature regulation of some Antarctic pen
guins. J. Physiol., Lond. 157:251-62.
Grande, F. 1964. Man under caloric deficiency.
In Handbook of Physiology 4: Adaptation
to the Environment, pp. 911-37. Washing
ton, DC: Am. Physiol. Soc.
Groscolas, R., and C. Cl?ment. 1976. Utilisation
des r?serves ?nerg?tiques au cours du je?ne
de la reproduction chez le Manchot emper
eur, Aptenodytes forsteri. C.R. Acad. Sci.,
Paris 282:297-300.
Harrington, H. J. 1959. Narrative of a visit to
the newly discovered emperor penguin roo
kery at Coulman Island, Ross Sea, Antarc
tica. Notornis 8:127-32.
Hoshiai, T., and K. Chujo. 1976. New emperor
penguin rookery of Riiser-Larsen peninsula,
east Antarctica. Antarc. Ree. 57:73-79.
Isenmann, P. 1971. Contribution ? l'?thologie
et ? l'?cologie du Manchot empereur (Ap
tenodytes forsteri Gray) ? la colonie de
Pointe G?ologie (Terre Ad?lie). L'oiseau et
la R.F.O. 41:9-64.
Isenmann, P., and E. P. Jouventin. 1970. Eco
?thologie du Manchot empereur {Apteno
dytes forsteri) et comparaison avec le
Manchot Ad?lie (Pygoscelis adeliae) et le
Manchot royal (Aptenodytes patag?nica).
L'oiseau et la R.F.O. 40:136-59.
Jarman, M. 1973. Experiments on the emperor
penguin in various thermal environments.
Bull Brit. Antarctic. Survey 33, 34:57-63.
Jonkel, G. M., and G. A. Llano. 1975. Emperor
200.145.52.210 on Fri, 26 May 2023 19:04:19 +00:00
penguins nesting on Inaccessible Island.
Antarc. J. of the U.S. 9:93-95.
Jouventin, P. 1971a. L'incubation et l'?levage
itin?rants chez le Manchot empereur de
Pointe G?ologie. Revue du comportement
animal 5:189-206.
1971b. Comportement et structure
sociale chez le Manchot empereur. La terre
et la vie 25:510-86.
-. 1972a. Note sur l'existence et la signi
fication d'une rythmicit? des parades mut
uelles. Alauda XL:56-62.
-. 1972b. Un nouveau syst?me de recon
naissance acoustique chez les oiseaux. Be
haviour 43:176-85.
?-. 1975. Mortality parameters in emperor
penguins, Aptenodytes fosteri. In The
increases
Biology of Penguins, ed.in pen pp.
. Stonehouse,
435-46. Macmillan.
and the sub
of D.Penguins,
Kilgore, L., M. H. Bernstein,ed.and D. M.
London: Mac in birds.
Hudson. 1976. Brain temperature
J. Comp. Physiol. 110:209-15.
King, J. R., and D. S. Farner. 1961. Energy -.
metabolism, thermor?gulation and body
temperature. In Biology and Comparative
Physiology of Birds, Vol. 2, pp. 215-88, ed.
A. J. Marshall. Pergamon.
Kooyman, G. L., C. M. Drabek, R. Eisner, and
W. B. Campbell. 1971. Diving behavior of the
emperor penguin, Aptenodytes forsteri. The
Auk 88:775-95.
Lasiewski, R. C, and W. R. Dawson. 1967. A
re-examination of the relation between
standard metabolic rate and body weight in
birds. Condor 69:13-23.
Le Maho, Y., P. Delclitte, and J. Chatonnet.
1976. Thermor?gulation in fasting emperor
penguins under natural conditions. Am. J.
Physiol. 231:913-22.
Le Maho, Y., and B. Despin. 1976. R?duction
de la d?pense ?nerg?tique au cours du je?ne
chez le Manchot royal. CR. Acad. Sci., Paris
283:979-82.
Mougin, J. L. 1966. Observations ?cologiques
? la colonie de Pointe G?ologie (Terre Ad?l
ie) en 1964. L'oiseau et la R.F.O. 36:166
26.
Murrish, D. E. 1973. Respiratory heat and
water exchange in penguins. Respir. Physiol.
19:262-70.
Odum, E. P., D. T. Rogers, and D. L. Hicks.
1964. Homeostasis of the nonfat components
of migrating birds. Science 143:1037-39.e
Pinshow, B., M. A. Fedak, D. R. Battles, and K. -.
Schmidt-Nielsen. 1976. Energy expenditure
for thermor?gulation and locomotion in
emperor penguins. Am. J. Physiol. 231: -. 1969. Environmental temperatures of
903-12.
Pohl, H. 1969. Some factors influencing the Taylor, C. R., and C. P. Lyman. 1972. Heat
metabolic response to cold in birds. Fed.
Proc. 28:1059-64.
Porter, W. P., and D. M. Gates. 1969. Ther
modynamic equilibria of animals with en Trawa, G. 1970. Note pr?liminaire sur la vas
vironment. Ecol. Monogr. 39:227-44.
Pr?vost, J. 1961. Ecologie du Manchot em
pereur Aptenodytes forsteri Gray. Paris: Van Zinderen Bakker, E. M., Jr. 1971. Com
Hermann.
-. 1963. Influence des facteurs biocli
matiques sur le nomadisme des Manchots
empereurs ? la colonie de Pointe G?ologie.
L'oiseau et la R.F.O. 33:90-101.
Pr?vost, J., and J. L. Mougin. 1970. In Guide
des Oiseaux et Mammif?res des Terres
Australes et Antarctiques Fran?aises, ed.
Delachaux and Niestl?. Neuch?tel, Swit
zerland.
Pr?vost, J., and J. Sapin-Jaloustre. 1964. A
propos des premi?res mesures de topogra
This content downloaded from
All use subject to https://about.jstor.org/terms
phie thermique chez les Sph?niscid?s de la
Terre Ad?lie. L'oiseau et la R.F.O. 34:52
90.
Prvost, J., and V. Vilter. 1963. Histologie de la
s?cr?tion oesophagienne du Manchot em
pereur. Proc. Inter. Ornithol. Congr., pp.
1085-94.
Pycraft, W. P. 1907. On some points in the
anatomy of the emperor and Ad?lie pen
guins. Brit. Nat. Antarct. Exp. Rep. 1901
1904. Zoology 2:1-21.
Saint Romas, G., and Y. Le Maho. 1976. D?
croissance pond?rale au cours des premiers
jours de je?ne chez le Manchot empereur.
CR. Acad. Sci., Paris 283:1097-99.
Sapin-Jaloustre, J. 1952. D?couverte et de
scription de la rookerie de Manchots em
pereurs de Pointe G?ologie (Terre Ad?lie).
L'oiseau et la R.F.O. 22:143-260.
Schmidt-Nielsen, . 1972. How Animals Work.
Cambridge Univ. Press.
1975. Animal Physiology, Adaptation
and Environment. Cambridge Univ.
Press.
Scholander, P. F., R. Hock, V. Walters, F.
Johnson, and L. Irving. 1950. Heat regula
tion in some arctic and tropical mammals
and birds. Biol. Bull. 99:237-58.
Scholander, P. F., and J. Krog. 1957. Coun
tercurrent heat exchange and vascular
bundles in sloths. J. Appi. Physiol. 10:
405-11.
Scholander, P. F., and W. E. Schevill. 1955.
Countercurrent vascular heat exchange in
the fins of whales. J. Appi. Physiol. 8:279
82.
Simpson, G. G. 1946. Fossil penguins. Bull. Am.
Mus. Nat. Hist. 87:9-99.
-. 1975. Fossil penguins. In The Biology
of Penguins, ed . Stonehouse, pp. 19-41.
Macmillan.
-. 1976. Penguins, Past and Present,
Here and There. Yale Univ. Press.
Stonehouse, B. 1953. The emperor penguin
Aptenodytes forsteri Gray. I. Breeding be
haviour and development. Scient. Rep.
Falkld. Isl. Depend. Surv. 6:1-33.
-. 1960. The king penguin Aptenodytes
patag?nica of South Georgia. I. Breeding
behaviour and development. Scient. Rep.
Falkld. Isl. Depend. Surv. 23:1-81.
1967. The general biology and thermal
balance of penguins. Adv. Ecol. Res. 4:
131-96.
tertiary penguins. Science 163:673-75.
storage in running antelopes: Independence
of brain and body temperatures. Am. J.
Physiol. 222:114-17.
cularisation des membres des Sph?niscid?s.
L'oiseau et la R.F.O. 40:142-56.
parative avian ecology. In Marion and
Prince Edward Islands, pp. 161-72. Cape
town: A. A. Balkema.
Watson, G. E. 1975. Birds of the Antarctic and
Subantarctic. Washington: Am. Geophys.
Union.
Watson, M. 1883. Report on the anatomy of the
Spheniscidae. Rep. on the sc. res. of the
voyage of H.M.S. Challenger during the
years 1873-76. London, Zoology 7:1-242.
Wilson, E. A. 1907. Aves. Brit. Nat. Antarct.
Exp. Rep. 1901-1904. Zoology 2:1-121.
1977 November-December 693