The American Naturol: Museum

T H E INTEGUMENTARY, PULMONARY, AND CAR-
DIAC ilIODIFICATIONS CORRELATED WITH

INCREASED CUTANEOUS RESPIRATION I N
THE ANPHIBIA: A SOTJUTION O F THE ‘HAIRY
FROG’ PROBLEM
G. K. NOBLE
The American Museum of Naturol History
THIRTY-NIWE FIGURFS
.4UTHO&’S ABSTRACT
Astylosternus robustus has greatly reduced lungs. All Amphibia exhibiting such a
reduction have their epidermis either penetrated by capillaries or thinned to facilitate greater
cutaneous respiration. The epidermis of both sexes of A. robustus is penetrated by capil-
laries. The ‘hairs’ of the adult male are merely extensions of this vasculated epidermis to
compensate for the greater muscularity, size, and activity of this sex.
The digits of terrestrial urodeles do not s e n e a s special centers of cutaneous respiration.
Digital sinuses are present i n all urodeles. The abdominal and femoral tubercle8 of arboreal
and some terrestrial frogs may function greatly i n respiration, for their epidermis is pene-
trated by capillaries.
All urodelrs and frogs having well-developed and frequently emptied lungs possess a
functionally complete auricular septum ‘and a spiral valve. Injection experiments dernon-
strate a complete separation of arterial and venous blond i n living specimens. A reduction
of the lungs conditions a reduction of the left auricle, but disuse causes no change in she.
A great decrease of the lungs, o r even a disuse of them, conditions a fenestration of the
auricular septum and a loss of the spiral valve. The spiral valve is formed by a backward
growth of one of the synangial valves and is not homologous with the accessory valves of
dipnoans. Lungless salamanders have no left auricle and no spiral valve.
CONTENTS
Introduction ........................................................ 341
’
The structure and significance of the ‘hair of Astylosternus robustus
(Boulenger] ................................................ 342
a. Historical and critical ....................................... 342
b. The structure of the ‘hair’ .................................... 347
c. The significance of the ‘hair’ ................................... 355
The modifications of the epidermis which increase the efficiency of cutaneous
respiration in other Amphibia ...................................... 303
The nature of the digital blood sinuses in Amphibia .................... 384
The origin of lunglessness ........................................... 386
Changes in tho auricles and triincus correlated with a reduction in pulmon-
ary respimtion .................................................... 391
Summary and discussion ............................................. 404
Conclusions ......................................................... 410
1NTROI)TJ’CTION
The occurrence in a frog of long, hair-like processes cover-
ing the sides of the body and part of the thighs with a thick
341
342 G . I<. WOBLE
growth has excited the curiosity of biologists since the first

discovery of this ‘hairy frog’ nearly twenty-five years ago.
The structure of the ‘hair’ has been studied by various inves-
tigators, but its function and significance has until to-day
remained a matter of conjecture. The receipt by The Ameri-
can Xuseum of Natural History of a series of well-preserved
specimens of this ‘hairy frog,’ Astylosternus robustus (Bou-
lenger) from Dr. Thomas Barbour as an exchange with the
Museum of Comparative Zoology has led me to reexamine
the problem of the origin and significance of these ‘hairs. ’
The conclusions at which I arrived are at such total variance
with those of earlier workers, especially as regards the vas-
cular supply of these integumentary structures, that I have
supplemented my conclusions by a study of the integumentary
niotlifications of other Amphibia. Some interesting correla-
tions ha\-e come to light which not only give a satisfactory
explanation of the function of the ‘hairs,’ but also seem to
clear up a number of other long-standing problems. Thus,
I find that the fenestration of the auricular septum goes hand
in hand with certain other changes in organization. Likewise,
the presence or absence of the spiral valve is apparently
closely correlated with other factors. These correlations I
shall discuss under separate heads, as they do not aid us in
iziterpreting the significaiice of the ‘hair’ in Astylosternus.
THE STRUCTURE AND SIGNIFICANCE OF THE ‘HAIR’ O F
ASTYLOSTERNUS RORUSTUS (BOULENGER)
a. Historical aidcritical
The general form and distribution of the ‘hair’ of Astylos-
ternus robustus on the sides of the body and thighs have been
excellently figured by Roulenger (’01) and by Kukenthal
(’la). Gadow ( ’00) examined some sections of the ‘hairs’
prepared by Laidlaw and found that they consisted of a core
of connective tissue covered by a moderately thick, uncornified
epidermis. Cutaneous glands were identified in these fila-.
ments, but only small insignificant blood vessels. The ‘hairs I‘
have, of course, no structural similarity with the hair of

THE ‘HAIRY FROG’ PROBLEM 343
mammals, but the name has nevertheless remained in gen-

eral use. With the capture of additional specimens of A.
robustus, Boulenger (’01) was able to determine that the proc-
esses are found only in the male. He had previously (’00)
assumed them to be present in the female. Andersson (’05)
found that the structures were present only in the mature
male, and were entirely absent in both the young male and
old female. Kiikenthal ( W ) , who had overlooked An-
dersson’s paper, devotes considerable space to proving that
these organs are present only in the male. Kiikenthal, study-
ing the histological preparations of KornliLuser, was able to
demonstrate that Gadow, in his study of the villosities, had
overlooked a series of tactile sense cells. These were located
between a series of epidermal ‘ridges.’ I n describing the
hairs he states (’12, p. 374) : “each appendage consists of
an inner cutis papilla and an outer layer of very peculiar ap-
pearance. This outer layer is made up of many longitudinal
ridges of epidermis cells, between which are found deep
longitudinal grooves. These grooves are filled with cutis
tissue. I n transverse section (Fig. A) this condition is very
conspicuous, reminding one somewhat of the transverse sec-
tion of a developing feather.”
IGikenthal was also able to correct Gadow’s description in
one other respect. He found a stratum corneum bordering
the epidermis. The dermis and blood supply of the ‘hairs’
was, according to Kiikenthal, very much as Gadow had de-
scribed it.
Kiikenthal compared the villosities with certain low tuber-
cles which he found in the skin of the female. He concludes
that the distribution of these tubercles “over exactly the
same areas of the surface shows clearly that they are homolo-
gous with the appendages of the males.” It follows from this
purely macroscopic examination that the “hair-like append-
ages are therefore to be considered as highly developed
tubercles of the skin.” Kiikenthal had before him a rather
large collection of specimens, and as the ‘hairs’ were not all
the same length in the apparently adult specimens he further
344 G. I<. NOBLE
concluded that they appeared “only in the males during the

mating season.”
This second guess may have been based on an earlier sug-
gestion of Gadow ( ’00, p. S S S ) , who had compared the ‘hairs’
with the ‘laichpinseln’ of the male Lepidosiren, although the
blood supply in these t ~ 7 oorgans were, according to Gadow’s
description, not comparable. In spite of this extraordinary
difference in vascularization betmeen the vascular filaments
of Lepidosiren and the ‘hairs’ of A. robustus, Dean (’12)
further elaboratpl this ‘laichpinseln’ theory by publishing
a diagram showing how a male A. robustus would look if it
were covered with eggs adhering to the villosities. Dean ex-
amined the ‘hairs’ histologically, but was able to add nothing
to Iiukenthal ’s description. He concluded that the epidermal
ridges which Kiikenthal had described could permit ‘the cir-
cumference of thc hair’ t o be ‘notably dilated.’
There are a number of reasons why the conclusions of the
above investigators cannot be accepted without further data.
Gadow (’00) and Boulenger (’02) admitted that they had
no clue to the physiological significance of the hairs. Kii-
kenthal did not present any data t o prove that the hairs were
present only during the breeding season. A casual examina-
tion of any large series of males will show that, while the
longest villosities are present in those specimens having a
horny covering to the prepollex region, they are well devel-
oped in males devoid of these denticulated sheaths and hence
obviously non-breeding specimens. Kiikenthal ’s second con-
clusipi that the ‘hairs’ are homologous with the skin tuber-
cles of the female is also ambiguous, if not incorrect, for they
are certainly not homologous with any particular warts. The
villosities of the male are much more numerous than the tu-
bercles on the sides of the body of the female. Further, there
are no tubercles at all on the upper surface of the thigh in the
position of the dorsal patch of femoral villosities of the male.
Kiikenthal had not examined the structure of these tubercles
in the female, and the hairs as described by him differ re-
markably from the ordinary integumentary tubercles which
are usually purely epidermal in character. The two peculiari-

ties which Kukenthal described, namely, the sense cells and
the ridges, give us no suggestion as to the possible function
of the hairs. The sense cells are apparently not more numer-
ous in the villous appendages than in the integument from
the sides of the body of the ordinary frog (Rana). The
theories advanced by Gadow (’00) and Dean ( ’12) have like-
wise little in their support. Just how minute capillaries sep-
arated from the exterior by a thick epidermis and some con-
nective tissue could possibly aerate the eggs is left entirely
unexplained. If we compare respiratory integument such as
that in the full pouch of the marsupial frog (Gastrotheca),
or in the small pouches of the Surinam toad (Pipa pipa), or
the epithelium lining the oviduct of the gravid Salamandra
maculosa, o r that in the nursing sac of the male Rhinoderma
when carrying its young, it will be obvious that in all these
cases the epithelium is much attenuated and vasculatcd like
the epithelium of a lung. There is nothing in the description
of the hairs given by any of the above investigators to suggest
that such tissues are capable of readily transmitting gases
through their walls. There is a second equally fundamental
objection t o the ‘laichpinseln’ theory. I n no amphibian is
the general integument of the body modified to aerate eggs
which are exposed t o the air or water (excepting possibly in
Pipa, in which the egg capsules are modified into a lid for
each pouch). To be sure, a number of frogs carry their eggs
on their backs, but in these cases the parental integument is
not known to be modified. Some frogs and urodeles are said
to brood their eggs, but without any structural modification
of the integument. One brooding frog, Hemisus, was found
to be pinkish along its ventral surfaces, apparently because
of the superficial capillaries (Rles, ’01). But similar capil-
laries may occur in frogs mliich do not brood their eggs, as I
have recently seen in the case of Hyla vasta. The female
Gastrotheca possesses a special dorsal pouch for holding the
eggs. In one species recently described by Gaige (’22) the
pouch develops in the young before they leave the parent’s
346 G . K. NOBLE
back. It arises in all species from a very limited region on

the back, and when once formed is never lost. I n no am-
phibian which leaves its eggs exposed to the external media-
that is, does not carry them within a sac-is the integument
kiiowii t o be in any way specialized to facilitate an aeration
of these eggs.
The latest discussion of the ‘hairs’ of Astylosternus ro-
bustus is that given by Phisalix (’22) in her great work 011
“ Animaux veiiimeux et wniiis.” This, it appears, is a sum-
mary of an earlier study (Phisalix, ’10) on Astylosternus.
Phisalix has made numerous investigations of amphibian
integument. One would assume that she was in a better posi-
tion than any of the other writers to speak authoritatively
011 the iritegumeiit of A . robustus.
Phisalix ( ’22, p. 25) concludes (translation) : “The Iiisto-
logical study that we have been able to make, thanks t o the
generosity of Mr. G. A. Boulenger, the eminent professor of
the British hluseum, who has described Trichobatrachus, has
fully confirmed the opinion of Laidlaw. The glands are as
numerous on these hairs as on the adjacent smooth surface,
hence tlie fleece of these frogs appears to us as an organ f o r
the multiplication of the glands, and consequently as a cor-
rective for their small size.”
Phisalix ( ’22, fig.34) gives a diagrammatic figure of a cross-
section of one of the hairs. This shows very little of the
grooves that IGilrenthal and Dean stressed. The capillaries
are shown at some distance from the epidermis. Oiily two1
glands appear in the section Phisalix figures. These are the
smallest poison glands Phisalix has found in the Amphibia.
In a table (p. 62) of the poison-gland size in Amphibia Phi.
salix places these at tlie lower eiid of the list with a diameter
of oiily 0.06 to 0.09 mm.
Turning to Phisalix’s earlier paper (’10) for more details,
we find that she has repeated the old error of attributing the
liairs to both sexes. Her specimeiis were preserved in alcohol,
and we infer that they were fixed in tlie same solution. Nev-
ertheless, her stains have permitted her, she writes (Phisalix,
T H E ‘IL4IRY PBOU’ PROBLEM 347
’10, p. 347), “to differentiate clearly all the details of struc-

ture of the skin and its hairs.” In this paper she recognized
the furrows in the hair, o r rather the blocks of epidermis
between the furrows, f o r she writes (’10, p. 347; transla-
tion) : “The epidermis of the hair is provided, as that of
the skin, with a cuticle; it has as the latter an average thick-
ness of 20 p ; but its inner face shows some little swellings
(bosselures) which festoon it, and which correspond to pro-
lif eration point s. ’’
I n brief, Phisalix, believing that the ‘hairs’ are found in
both sexes, has picked out the glands as the particular defi-
ciency in the skin of A. robustus and has emphasized this
deficiency as the reason for the development of the hairs. In
all other Amphibia, when an increased secretion is needed in
the economy of the species, the glands either hypertrophy or
multiply and become grouped together into warts or folds.
Never in any other form where such a demand could be dem-
onstrated from a knowledge of the habits of the species is ‘
the skin itself thrown into prolongations of any sort-either

villi, folds, or flaps-without any development of the glands
beyond the condition found in adjacent integument. The
glands of the hairs of Astylosternus are extremely small.
Phisalix, without giving any comparative data to support her
views, contends that the integument of Astylosternus has
been thrown into these filaments in order to increase the
number of glands. It is obvious from Phisalix’s figures that
there is plenty of room for these glands to increase in num-
bers as well as in size without the formation of the hairs.
The conclusions of Phisalix leave us as much in the dark
as do those of Dean, ICiikenthal, o r Gadow.
(I. The structure of the ‘hair’
Astylosternus robustus is represented in The American
Xuseum of Natural History by six specimens, five of which
have been received in exchange from the Museum of Compara-
tive Zoology. Most of these specimens were fixed in formol.
I have studied in serial sections parts of the integument and
J O U R N A L OF MORPHOLOGY A F D P H Y S I O L O G T , VOL. 40, KO. 2
348 G. K . NOBLE
‘hairs’ of several of these formol specimens. One series of

preparations as stained in Delafield ’s haematoxylin and
eosin, a duplicate series in Xallory ’s connective-tissue stain.
A cursory examination of these sections at once demonstrated
that Gadow, Kiikenthal, Dean, and Phisalix have overlooked
entirely the chief peculiarity of the hairs, namely, their vascu-
larity. The epithelial ridges which Kukenthal describes owe
their character to the capillaries which have penetrated the
epithelium and divided it up into blocks (figs. 3 to 5). In tan-
gential section (fig. 7 ) it may be seen that these blocks do
not run the whole length of the ‘hair,’ as Kukenthal’s descrip-
tion implies, but are irregularly divided by transverse vessels,
the whole system of capillaries forming a network, the meshes
of which are elongated in the direction of the main axis of
each hair. This penetration of the epidermis by a network
of capillaries is not restricted to the ‘hairs’ of the male, it
also occurs in the integument adjacent. In figure 3 I have
ABBBEVlATlONS
A.V.VaZ., auricular-ventricular valve L u . , liver

Ba.Mbr., h s a l membrane Long.M., longitudinal muscle bundle
BLCorp., red blood corpuscle M.CZ., cardiac muscle cell
BLEp., blocks of epidermis &fez., melanophore
BZ.V., blood vessel Mbr., thick enclosing membrane of
Cap., capillary sheath to lung diverticulum
Ctl.E’p., ci!iated, non-respiratory epi- MucG‘E., mucus gland
t helium Nwc.Cap., nucleus of capillary cell
C i r X . , c i m x h r muscle bundle Nztc.Con.Tzs., nucleus of eonneetive-
C1u.C1., club cell tissue cell.
CO?L.TZS., connective tissue Suc.h‘p., nucleus of epithelial cell of
Cor., corium auricular septum
C I L ~cuticle
., Per., peritoneum
Dt.P.Gl., duct of poison gland P.GZ., poison gland
Bp., epidermis P.Dtw., posterior diverticulum of lung
Epitk., epitlielium of auricular septum B.A., right auricle
Por., sm:ill foramen in auricular sep- S.A.VnZ., sinus-auricular valve
tum Rep., auricular septum
G.La., germiiial layer S?n.V.CI., smooth-muscle ccll
Hor.La., horny layer Sp.V., spiral valve
I ’CLBr., intercellular bridges S t . , stomach
L A . , left auricle Tr.La., transitional la) er of epidermis
L ’cyte, leucocyte T’as.L., vasculated portion of lung
Lin.Cl., epithelium cell lining the inner
surface of sheath membrane
Fig. 1 Astylosternus robustus (Boulenger).

Fig. 3 Batrschophrynus microphthalmus Werner.
(Both drawn from preserved specimens.)
350 G . Xi. NOBLE
shown the appearance of one of the most dorsal hairs from

tlie side of the body as seen in a section transverse to the
body axis. I t will be noticed that the integument immediately
dorsal to the hair, namely, that from the dorsal surface of
the frog, exhibits a similar penetration of the epidermis by
B system of capillaries. It will also be gathered from this
low-magnification drawing that the capillaries tend to run
parallel t o the longitudinal axis of each hair.
Under a higher magnification (fig. 5) it may be seen that
these capillaries have penetrated the epidermis t o the horny
layer. They are thus separated from the exterior by only
two layers of greatly flattened cells. There is, to be sure,
some variation in the degree of penetration reached by these
capillaries, but the vast majority tend to reach the stratum
corneum.
In some of tlie Mallory preparations it may be seen that a
number of the capillaries have carried up with them into the
epidermis a sheath of connective tissue which surrounds the
capillary as a thin coat. This sheath may be a basal mem-
brane, but I cannot differentiate it from the subjacent con-
nective tissue. In these cases the blood corpuscles in tlie
capillary are separated from the exterior by the two attenu-
ated cells of the stratum corneum, the thin wall of the capil-
lary, and the thinner enclosing sheath of connective tissue.
I n other cases (fig. 5) I have not been able to distinguish
any sheath of connective tissue surrounding the capillary
and have assumed that it does not exist.
The blocks of epidermis which have been molded by the
capillaries have a very distinctive form. It may be seen from
figure 5 that some of the boundary cells have been flattened,
but the others retain the appearance of ordinary epidermal
cells. Well-defined intercellular bridges are visible in most
of the preparations. Some of the epidermal blocks serve for
the attachment of smooth muscle cells. The attenuated ends
of these muscle cells in a few cases are attached to the stratum
corneum, but usually to the cells of the transitional layer.
The deeper epidermal cells in these regions of attachment
itre elongated in the direction of the fibers (fig. 7 ) .
THE ‘HAIRY FROG’ PXOBLEM 351
Iiitegument of the ‘ hairy frog,’ Astylosternus robustus (Boulenger).

Fig. 3 Section transverse to thr body axis, through the longitudinal axis of
the base of one of the ‘hairs’; an adjacent ‘hair’ shown in cross-seetion. X 62.9.
Fig. 4 Section of the integument from the flanks of the female A. robustus,
showing the penetration of the capillaries into epidermis. The section is per-
pendicular t o the surface of the skin. X 225.5.
Fig. 5 A small portion of a transverse section of one of the ‘hairs,’ t o show
the relation of the capillaries to the epidermis and the attachment of the smooth
muscle cells. X .534.8.
352 G. I<. NOBLE
Cutaneous glands are numerous in the ‘hairs,’ but it will

be seen from figure 3 that these are not more numerous than
in the unmodified integument. In short, the hairs are identi-
cal in structure with the adjacent integument except that they
do not contain the deeper layers of dermal tissue. If small
areas of the integument lying dorsal to the hairs were ex-
tended into processes, and if these extensions were of such
a narrow gauge that only the more superficial parts of the
spongiose stratum of the corium were carried into them, we
would have an exact replica of the hairs we are describing.
Possibly a few differences between the hairs and the super-
ficial part of the adjacent integument may be recognized. I n
some preparations there is a greater attachment of smooth
muscle fibers to the epidermis or more capillaries may be
present. Again, the connective-tissue core of each hair is
more fibrous and contains more smooth-muscle cells. These
differences are probably of no great consequence. The hairs
may be recognized as merely finger-like extensions of a highly
vasculated epidermis into which there have been pulled a core
of connective tissue together with its smooth-muscle cells,
glands, blood vessels, and melanophores.
Sections of the integument from the sides of the body in
the female exhibit a structure practically identical to that
found in the male just dorsal to the villosities. Capillaries
penetrate the epidermis in the same way (fig. 4), but usually
do not reach the stratum corneum. I n other words, the in-
tegument from the sides of the body of male and female
Astylosternus robustus differ only in that the epidermis of
the former has been thrown into finger-like processes into
which have been carried part of the stratum spongiosum.
Kukenthal (’12, p. 373) claimed that these ‘hairs’ of the
male were homologous to tubercles scattered over the whole
back of both sexes, but “more closely crowded in the region
of the angle of the jaw.” As shown in figure 9, of a section
through one of these cheek warts in a male, the structure is
totally different from that of a lateral filament. The cheek
warts owe their character to a collection of poison glands.
Fig. 6 Dissection of the viscera of Astylosternus robustus (Boulenger), show-

ing the form of the lung in a formalin-preserved specimen. The non-respiratory
posterior diverticulum is enclosed by a tliiek sheath.
354 G. I<. KTOBLE
They are directly comparable to tlie pardoid glands of thc

toad. The capillaries which pnsh into the epidermis of the
surrounding illtegument do not occui* at all over the main
part of these warts (fig. 9), although they encroach on all
Fig. 7 Tangential section of one of the l i n i ~ vof Astylosternus robustus (Bon-

lcnger), showing tlie network of capillaries which divides the epidermis into a
series of blocks. X 225.
Fig. 8 Cross-section of the posterior clirertieulum of the lung of the niale
Astplosternus rahustus (Boulenger). X 82.2.
T H E ‘HAIILY FROG’ PROBLEM 355
sides of it. Kiikenthal’s homology of the hair-like append-

ages of the male A. robustus with warts on other parts of
its body has no basis in fact other than that both are protru-
sions of the skin.
c. l’hc si,g?i;fic.aiicc of f h e ‘hair’
It is clear from the above description that the chief pecu-
liarity of the hairs of Astylosternus robustus is their vascii-
laritp. I n the female there is also a penetration of the
epidermis by the capillaries. I n the male this epidermis is
thrown into a series of processes, thus increasing the vascu-
_-
Fig. 9 Section of one of the cheek warts in the male Astylosternus robustus
(Boulenger) ; section perpendicular t o the surface of tho wmt. X 50.
lated area. Is not, then, the function of the ‘hairs’ asso-

ciated with this vascularizationt If so, do these processes
function in facilitating a transmission of oxygen from the
frog’s body t o its eggs and larvae o r are they developed in
response to a need for a greater respiratory surface in the
adult male frog itself? In short, do these observations place
the ‘laichpinseln’ theory on a much sounder basis or do they
afford us a new and quite unsuspected explanation for the
hairs ?
I have stated above that in no amphibian which leaves its
eggs exposed to the atmosphere or the water is the parent’s
integument known to be modified to permit a greater aera-
356 G. I(. NOBLE
tion of the eggs. The breeding habits of A. robustus are

unknown, but Boulenger ('10, p. 166) has called attention to
its large eggs and adds that we may expect to find some sur-
prises in its mode of development. Egg size, alone, is not
indicative of a method of development. I n Eleutherodactylus
tlie method is direct. E. inoptatus has eggs approximately
5.5 mm. in diameter, a breeding female measures 80 mm. in
head and body length. I n E. flavescens the eggs are 4 mm.
in diameter, tlie female measures 36 mm. On the other hand,
Scaphiopus and Ascaphus pass through a larval stage. The
eggs of S. hammondii measure 2 mm., the female, 55 mm.,
while Ascaplius eggs are 4.5 mm. and the female, only 47 mm.
I have removed eggs from the lower part of the oviduct of
A. robustus and find that they measure at most only 4.5 mm.
in diameter. As the same specimen measured 102 mm. in
head and body length, it would seem that the species might
pass through a larval stage. Consistency as well as size of
the yolk would effect the method of development. (Compare
the teleost egg with the egg of Rana.) Within the Amphibia
yolk-size more or less controls the length of intracapsular
embryonic life. It is highly probable that A. robustus passes
part of its larval life outside of the egg capsules, and hence
probably as a free-swimming larva.
Whether o r not the hair-like appendages of A. robustus
play any part in the aeration of its eggs will have to await
field observation. It must be admitted that all the data are
against such a hypothesis. On the other hand, the presence
of these filaments in the male may be fully explained in a
totally different way. WTe have seen that their chief peculi-
arity is their vascularity. A similar vascularity without the
epidermal outpushiiigs is found in the female. This vascu-
larity present in both sexes would not be expected to func-
tion in the transference of oxygen from both parents' bodies
t o the outer medium, but for the reverse purpose, namely,
for securing a better oxygen supply. Such an increase in the
respiratory surfaces is correlated with, we may say condi-
tioned by, a reduction of the lungs in 9.robustus. These are
unique among frogs in being formed of a short sacculated

portion and a narrow non-alveolated diverticulum projecting
posteriorly.
The curious form of the lungs in the male is shown in fig-
ure 6. The anterior alveolated part has the appearance of
a normal anuran lung, while the narrow posterior diverticu-
lum is tightly enclosed in a sheath. On transverse section
(fig. 8) it may be seen that this sheath consists of an outer
membrane of considerable thickness bordered externally by
the peritoneum and internally by a series of much attenu-
ated cells. The bulk of the sheath is formed of connective
tissue, through which are scattered blood vessels of various
sizes. A powerful series of circular muscles encloses the
inner epithelium, while immediately adjacent to these on
their outer side may be seen a few bundles of longitudinal
muscles. The striking feature of this posterior diverticulum
is the absence of respiratory epithelium. Large tracts are
ciliated similar to the supporting trestle work in the un-
modified anterior part of the lung. These ciliated tracts
are devoid of superficial capillaries. It is obvious that the
posterior diverticulum of the lung is largely non-respiratory,
apparently serving as a kind of air sac from which the air
may he suddenly expelled by its powerful muscular equip-
ment. Comparing the lungs as a whole with those of Rana
or Bufo, it is evident that they must play a minor r6le in the
respiration of the male Astylosternus robustus.
In the female the lung is similarly divided into a broad
alveolated portion and a narrow posterior diverticulum. But
in the female the diverticulum is not enclosed by a thick
sheath. My sections show that its epithelium is largely non-
vascular, as in the case of the male.
A glance at any large series of specimens will convince
one that the male must have a much greater need for an in-
creased respiratory surface than the female. Comparing
Kiikenthal’s ( ’12, figs. 2 and 4) figures of the male and female
specimens, it may be seen that the males are enormously
more muscular, especially in the arms and shoulders. I have
358 G. K. NOBLE
examined iiiiieteen males arid eleven females, all but the six
specimens mentioned above being in the Museum of Compara-
tive Zoology. All of these nineteen males except one are
larger than any of the-females, and a few are decidedly
larger. Sexual dimorphism in A . robustus consists of a larger
size, more muscular arms, shoulders, and abdomen, pro-
riounced black combs covering the prepollex region, and prob-
ably a greater activity in the male. To compensate f o r this
greater muscularity and size increased respiratory surfaces
would be necessary. An increase in the efficiency of cutane-
ous respiration as 1%-ouldhe conditioned by a penetration of
the capillaries into the epidermis was apparently sufficient
for the needs of the female, but not for the male. An increase
in respiratory surface itself either by the formation of folds,
villi, or other processes was required. The hair-like filaments
of A. robustus represent merely an increase in the surface
area of the vasculated epidermis correlated with a demand
for greater gaseous exchange. The fact that these processes
happen to be finger-like instead of in the shape of folds or
flaps is a matter of no special significance.
That this greater need f o r respiratory surfaces in the male
is conditioned not merely by the reduction of its lungs, but
also by its increase in muscularity during the breeding season
is suggested by the change in size which the villosities undergo
during the year. Our series shows that as the black horny
‘combs’ develop in the male the arms become more muscular
and the villi longer. The males with the longest villi are the
most powerful and exhibit the best-developed ‘combs. ’ This
correlation is not always exact, as a few breeding males do
not have longer filaments than non-breeding specimens. Such
a condition may possibly be due to the retention of the combs
after the breeding season. At least no specimen with long
filaments lacks the combs.
The lungs of breeding frogs of species possessing well-
developed lungs are sometimes larger in the male sex, pos-
sibly because of a greater physiological need for respiratory
surfaces. Recently Hesse ( ’21, p. 388) has found in Bombina
“that the lungs of the female . . . . could be blown up by

far not so fully, sometimes only one-half as much as those
of the male” (translation). The respiratory part of the
lung of the femalc Astylosternus robustus is at least as large,
possibly larger than that of the male. The adult male A .
robustus with its vasculated epidermis instead of a large lung
would find itself at the beginning of the breeding season not
sufficiently equipped to oxygenate the additional musculature
developed at this time. Hence, the short integumentary
processes of the non-breeding male were produced in length
until a balance was reached.
If this explanation is correct, we naturally ask why do no
other frogs have ‘hairy growths’ to facilitate their respira-
tion? Further, why d o lungless salamanders o r other Am-
phibia of reduced lung capacity not develop these filaments?
I n regard to the first question, I have been unable to find
any frog closely related to Astylosternus robustus which pos-
sesses such strangely reduced lungs. Astylosternus oxy-
rhynchusl Nieden, as represented in The American Museum
of Natural History by a single specimen, exhibits large lungs
similar to those of Rana and possesses no villosities. Fur-
ther, Scotobleps gabonicus has a lung of usual proportions.
The type of reduced lung described above seems peculiar to
one species of the genus Astylosternus, and is not known to
occur in any other species of batrachian.
There are, to be sure, frogs not closely.related to A. ro-
bustus arid many urodeles which have a reduced lung. I n
some cases the environment is such that only a diminished
amount of gaseous exchange is required f o r life. I n other
cases the species live in more normal temperature. I n all
cases of lung reduction some compensatory change in the
integument to insure a better cutaneous respiration has oc-
curred. Some of these changes are merely a penetration of
the epidermis by capillaries, in other cases flaps or folds
develop to increase the respiratory surface. There is no rea-
son to expect that filaments similar to those of A. robustus
I use the emended spelling--see Noble, ’24.
360 G . K. NOBLE
should develop in these unrelated groups. The physiological

requirement of greater gaseous exchange through the integu-
ment is met in other ways. I n some cases these ways are very
similar t o the method adopted by A. robustus.
Every one of tliese modifications of the integument in other
Amphibia is closely correlated with the habits and habitat of
the species. Unfortunately, for a better appreciation of all
the factors involved in the production of villosities in A.
robustus we have practically no information in regard to its
habits. The species is known from only a limited region in
the Cameroun and Spanish Guinea. A few of the specimens
in the Museum of Comparative Zoology were labeled as hav-
ing been captured “ o n a grass lawn about 3 mile from the
nearest spring.” Three of the specimens in another series
contained food in their stomachs. This consisted of-two slugs,
three myriopods, one spider, one beetle, and one grasshopper.
This food suggests a terrestrial habitat. On the other hand,
the Telmatobius-like form of the species, the pronounced tar-
sal fold, suggests an aquatic or semiaquatic life. I n view of
the lack of further field observations we may conclude that
A. robustus leads a part of its life on land, but probably rc-
turns at intervals t o the water. It is important to keep this
habitat in mind when comparing the modifications of the
integument of A. robustus with that of other Amphibia.
THE MODIFICATIONS O F THE EPIDERMIS WHICH INCREASE THE

EFFICIENCY O F CUTANEOUS RESPIRATION I N OTHER AMI’HIBIA
Tlie question has been raised in the preceding discussion

as to why filaments similar to those of A. robustus do not
occur in any other amphibian. The answer that other com-
pensatory changes have occurred in the integument of those
forms having the lungs reduced or suppressed requires fur-
ther explanation, for these changes have been described in
only a few forms, and until recently no attempt was made to
correlate these changes throughout Amphibia in general.
Despax ( ’23) has described the penetration of the epidermis
by capillaries in the nearly lurigless Euproctus asper and his
THE ‘ HAI R Y FROG’ PROBLEM 361
figures of the lateral epidermis of this species comparc favor-

ably with mine of the female A. robustus. Despax has re-
viewed the recorded cases of capillary penetration of the
epidermis in Amphibia, but he has made no comparisons of
the epidermis throughout the lungless forms. His investiga-
tions were limited t o a very few species.
I have examined in sections the integument of a large series
of species. The greater majority of these were fixed in
Zenker’s. A few were in Rouin’s and several in formol. Dela-
field’s liaematoxylin with eosin or orange G were used as
stains. Attention was paid especially to the vascular supply
of the epidermis and its probable r81e in respiration. My
observations added to those in the literature give a fair sur-
vey of the modifications which the integument of the Am-
phibia has undergone to increase its respiratory efficiency.
Sections of the integuments of the f oll‘owing species were
available to me. 1 list them in phylogenetic sequence : Hyno-
bius leechii, Cryptobranchus alleganiensis, Dicamptodon
eiisatus (larva), Rhyacotriton olympicus, Amblystoma ti-
grinum (various ages), A. opacum (larvae and adults), A.
macrodactylurn, Notophthalmus torosus, Triturus viridescens
(red and green stages), Salamandrina terdigitata, Amphiuma
means, Pseudotriton ruber, Eurpcea bislineata, Stereochilus
marginatus, Plethodon cinereus, P. eschscholtzii, Ascaphus
truei (tadpoles and adults), Bombina maxima, Xenopus tropi-
calis, Scapliiopua holbrookii (tadpoles and adults), Telma-
tobius marmoratus, Batrachophrynus microphthalmus, Eleu-
therodactylus ruthae, Gastrotheca monticola, Bufo terrestris,
Hyla cinerea, H. crucifer, H. andersonii (larvae and adults),
H. dominieensis, H. vasta, Sstylosternus robustus, Rana
pipiens, R. clamitans, R. sylvatica.
The most primitive urodeles as represented by Hynobius
leechii had an integument very similar to that of Amblystoma.
The epidermis of the body varied in thickness from three to
five cells deep. There is no penetration of the capillaries
into this epidermis. The glands and dermis, which do not
concern us in the pzesent synopsis, have much the appearance
of those in Amblystoma.
362 G . K. NOBLE
The Cryptohranchidae liave evolved directly from the

Hyriobiidae and represent giant permanent larvae of an ex-
tinct form closely related to Ranodon sibiricus. Their integu-
ment differs remarkably from that of Hynobius in its greater
thickness, especially of the epidermis, and by the presence of
Iiumerous capillaries which penetrate the epidermis t o the
stratum corneum (fig. 11). This vascnlarization is most pro-
nounced oil the sides of tlie body. The loose flaps which droop
from these regions are so richly supplied with capillaries
Figs. 10 to 12 Sections of the integument, from tlir flanks of various Amphibia,

diowiiig the rc1:itioiis of tlie rapi1l:iries to the epidcrmis. All sections perpendicu-
lar to the surface.
Fig. 10 Adult male Notoplitllalnius torosus (EschsclioItz). X 300.8.
that they form veritable gills. This analogy is brought out

further by the behavior of the animal, which frequently waves
these flaps in an undulatory manner, thus assuring their con-
tinuous contact with fresh water. Both Cryptobranchus and
Megalobatrachus possess large lungs, which they fill with air
at infrequent intervals. There has been considerable differ-
ence of opinion as to the frequency with which Cryptobranchus
replenishes its luiigs with fresh air. This subject has been
recently reviewed by Willey ( '20). Under normal conditions,
Cryptobranchns iises its lungs as well as its integument iii
respiration. hregalobatrachus possesses the same thick epi-
1'HE 'HAIRY FllOG' PBOBLEX 363
dermis and superficial capillaries of Cryptobranehus (Phi-

salix, '22). Why should the epidermis of the Cryptobranchi-
dae be penetrated by numerous capillaries and not that of
Fig. 11 Adult female Cryptobranchus allegsriiensis (Daudin). X 261.8.

Fig. 12 Adnlt female Ascaphus truei Stejneger. X 260.8.
such well-known aquatic forms as the newt? It is probably

not because of the larger size of the former urodeles; other
large aquatic species do not exhibit this peculiarity. llIy oh-
servation tends to shorn much less dependence on pulmonary
SOVRAAL Or MORPHOLOOY A N D PHkSIOLO(+I, \Old. 40, LO. 2

364 G . I<. NOBLE
respiration in Cryptobranchus than in Triturus viridescens.

Willey ( '20) has shown how greatly the respiratory behavior
of Cryptobranchus may r a r p from day to day. The observa-
tions which I have made on these urodeles in miscellaneous
aquaria should be checked with careful experiments. I n the
meantime, we may conclude that Cryptobranchus does not
utilize its lungs as frequently as certain other aquatic uro-
deles which I have watched in the tanks, namely, Siren, Am-
phiuma, or the newts.
The respiration of the urodeles would not be dependent
only on the presence or absence of lungs, the size of the
cutaneous capillaries, their number and nearness to the sur-
face. The following five factors also enter into consideration :
1) Coldness of the water; 2) swiftness of the water; 3) abun-
dance of growing vegetation in habitat; 4) practice of bucco-
pharyngeal respiration in water or air ; 5) size of the animal.
In tlie following discussion we will try to keep these factors
in mind, in order that we may more clearly see how close is
the correlation between lung reduction and the penetr at'ion
of tlie epidermis by the capillaries.
The Sirenidae and the Proteidae are of uncsertain rela-
tionships. Both are permanent larvae which retain their
gills. It has been claimed that Siren loses its gills R t an
early stage, but I have shown e1sev;here (Noble, '24 b)
that these are lost only under very adverse conditions. Both
Sirenidae and Proteidae possess lungs and probably arose
from primitive salamandrids, amblystomids, or hynobiids.
The integument is thick, the epidermis consisting of a reln-
tively large number of cell layers. The number varies in
different regioiis of the body. It has been found that in all
Amphibia the epidermis from the sides of the body represents
about an average thickness. I n Necturus this epidermis con-
sists of from five t o seven layers of cells (Dawson, '20). There
is no penetration of capillaries into the epidermis of either
tlie Sireiiidae or Pro teidae. Obviously, tlie integument of
these urodeles cannot play a very great r6le in respiration.
Nor is there any great need for it so doing in forms well
equipped with both gills and lungs. To judge from the be-
havior of captive animals, pulmonary respiration is resorted
to much more frequently in Siren than in Necturus. Under
normal conditions Necturus relies chiefly on its gills.
The Amblystomidae have arisen from the Hynobiidae or
from the stock which gave rise to the Hynobiidae. Most
amblystomids pass their larval life in ponds and are equipped
with long gills and a simple integument with an epidermis
two cells thick. At about the time of metamorphosis, cell
multiplication occurs in the epidermis and the Leydig cells
begin to disappear. A t metamorphosis the skin is shed, the
underlying epidermal cells continue to divide, until many
weeks or months after metamorphosis the epidermis char-
acteristic of the adult is established. This consists of from
three to six layers of cells on the sides of the body. The
integument is practically identical with that of the less spe-
cialized hynobiids or salamandrids (fig. 10). This ontogen-
etic change in the epidermis does not proceed at the same rate
in all amblystomids. The epidermis may increase in thick-
ness during larval life. This is conspicuous in the case of
Dicamptodon ensatus. The epidermis of urodeles need not
wait until metamorphosis for an increase in thickness. Most
permanent larvae (Cryptobranchus, Siren, Necturus, and
Amphiuma) have an epidermis of several cell layers.
Among the Amblystomidae there is only one species having
greatly reduced lungs (Dunn, ’20). This form, Rhyacotriton
olympicus, lives in and along the edges of cold mountain
streams of the Olympic Mountains, Washington. Notes on
its habits have been sent me by Mr. Phillips Putnam. The
species is found most frequently out of water on rocks
soaked by the spray of some fall in the torrent. Other speci-
mens hare been captured in the water. This habitat because
of its coldness would require less respiratory activity on the
part of a salamander. The highly aerated water would be
very suitable f o r cutaneous respiration. The lungs of Rhya-
cotriton olympicus average about 5 mm. in length. Pulmon-
ary respiration must be reduced to a minimum. I have
366 C;. Ti. NOBLE
determined by a study of living specimens that there is both

aerial and aquatic buccwpliaryrigeal respiration in this form.
Under such ideal environmental conditions, it might be ex-
pected that 11o structural changes in the integument was
necessary to assure sufficient respiration. Gaige has shown
that the temperature of the water in whicli Rhyacotriton lives
arerages below 40°F. It is well known that frogs which may
be readily drowned overnight in water of 70°F. will remain
semiactive for weeks and possibly months under water that
approaches the freezing-point. Rhyacotriton is more active
than hibernating frogs and apparently in correlation with its
greater need for gaseous excliangc its integumentary capil-
laries are nearer to the surface. As shown in figure 15, the
epidermis from the sides of the body of Rhyacotriton differs
from all otlier species of amblystomids in consisting of only
two or three (rarely four) layers. The capillaries, at least
those 011 the sides of tlie body, usually push slightly into the
epidermis until there are only two layers of cells covering
tlie capillary walls. The oxygen in the water or air is sepa-
rated from the liaemoglobin of the blood by only two epider-
mal cells, ail atteriuatetl basal membrane, and the thin capil-
lary wall. The thinness of the epidermis may have been
produced by a cessation of the postmctamorphic cell multi-
plication. At least this epidermis has the same number of
cell layers that I find in a recently metamorphosed A. ti-
grinum. The capillaries of Rhyacotriton,, however, show an
incipient penetration of the epidermis which is not found in
Amblpstoma at any stage of development.
The Salamaiidridae probahly arose from some prehyno-
biid stock, for the most primitive species do not seem closely
related to Hynobius. The integument of these generalized
forms is essentially the same as in Amblystoma and in Hyno-
bins. The Salamaiidriae are of especial interest to us in this
review because they include several genera of lungless or
nearly lungless forms. The groups with reduced or absent
lungs embrace the genera Chioglossa, Salamandrina, and the
subgeiicra Ihproctus arid Rhithrotriton of Triturus. The
integument of the first and last of these groups is unknown

liistologically and may be omitted from the discussion. The
subgenus Euproctus has been recently exhaustively studied
by Despax (’23). It is important t o have his findings
before us.
Euproctus asper lives in certain mountains of Spain and
France where the environmental conditions are suited to
its particular breeding and living requirements. It frequents
clear, brook-fed ponds or the quieter pools of mountain tor-
rents, seeking the land only during the hibernation period.
Its lungs are reduced and, as clearly demonstrated by Des-
pax, play only a small part in respiration. It is the integu-
ment which plays the chief rale, and in correlation with this
has undergone changes parallel in part t o those of Astylos-
ternus robustus. The epidermis of E. asper is about as
thick as that of the lowland newts (Triturus), but in corre-
lation with the increased cutaneous respiration the capillaries
have penetrated the epidermis until they are “separated from
the stratum corneum by only a single layer of flattened cells”
(Despax, ’23, p. 116 ; translation).
I n the closely related Euproctns montanus the lungs are
lost entirely. The species frequents mountain torrents part
of the year and at other times is terrestrial. The bubbling
water of mountain cascades would be expected to carry more
oxygen than pond water. It is, perhaps, therefore not sur-
prising that Despax should have found that in aquatic speci-
mens of this species the capillaries penetrated the epidermis
as in E. asper, but to a less extent. Specimens adapted to
land life no longer show these superficial capillaries. The
whole epidermis of these land forms is thinner than in E.
asper o r the adult Triturus viridescens. Despax’s figures
indicate two o r three layers of cells below the stratum cor-
neum. This thinning is probably correlated, as we shall see
later, with cutaneous aerial respiration. Such a related form
as Triturus torosus (fig. lo), which retains its lungs, exhibits
the characteristic thick epidermis even when kept out of
water for nearly a year in the laboratory. It is therefore
368 G . K . NOBLE
apparent that within a closely related group of species we may

have, 1)a large-lunged, terrestrial or aquatic species exhibit-
ing a moderately thick epidermis, and no intra-epidermal
capillaries; 2 ) a nearly lungless species living during the
Figs. 13 to 15 Sections of the integument from the flanks of various urodeles,

made perpendicular to the surface.
Fig. 13 Triturus viridescens (Rafinesque), red Iand stage. X 307.6.
Fig. 14 Snlamnndrina terdigitata (Bonnaterre). x 307.6.
THE 'HAIRY FROG' PROBLEM 369
period of greatest activity in pools of clear, slow-moving

water, and showing an enormous penetration of the epidermis
by the capillaries, and, finally, 3 ) a torrent-living and more
terrestrial species having less penetration of capillaries, but
exhibiting a distinct thinning of the epidermis. This latter
condition would bring about the same result as a greater
epidermal penetration of the capillaries, namely, a closer
approach of the blood corpuscles to the external environment.
Salamandrina, the last salamandrid genus to be mentioned,
exhibits even a greater approach to terrestrialism than E.
montanus (Werner, '12, p. 125). Salamandrina is frequently
considered lungless. It actually possesses rudimentary lungs.
Although these are less than 2 mm. in length, Anselmi ('22)
Fig. 15 Bhyacotriton olympicus (Gaige). X 322.4.
has shown that they are functional. a s if in correlation with

the terrestrial life, the thinning of the epidermis begun in
E. montanus is carried much further in this form than in any
other salamandrid. As shown in figure 14, the epidermis of
the body consists of only one to three layers of cells. Over
many of the capillaries there is only a single epidermal cell!
The epidermis does not owe its thinness merely to the reten-
tion of juvenile characteristics. A comparison between it
and such juvenile epidermis as is found in the integument
of the red land stage of Triturus viridescens (fig. 13) will
show that a decided thinning has occurred. The difference
between the integument of Salamandrina and the red land
form of T. viridescens would seem directly correlated with
the reduction of lungs in the former species.
370 G . K. NOBLE
The Salamandridae apparently gave rise to the Amphiu-

midae, but Amphiuma is not closely allied t o any living sala-
mandrid. This genus, like Crytobranchus, is a permanent
larva, but it loses its gills very early in life. Although
aquatic, Amphiuma depends to a large extent on its pul-
monary respirations. Its lungs are large and highly vascu-
lated. Apparently pulmonary and aquatic buccopharyngeal
respiration are sufficient for the needs of Amphiuma. Its
integument is in no way\. modified for cutaneous respiration.
The epidermis consists of five to seven layers of cells. The
capillaries do not penetrate into the epidermis, although they
frequently occur between dermis and epidermis. As the inner
margin of the epidermis is somewhat undulatory, the capil-
laries occasionally appear on the crest of dermal waves, giv-
ing the appearance of an incipient penetration of the over-
lying tissue.
A second family which must have arisen from the more
primitive salamandrids is the Plethodontidae. This family
is entirely lungless and exhibits such an enormous adapta-
tion to aquatic, terrestrial, and even arboreal life that we
might expect to find considerable differences in the integu-
ment of the various species. The systematic relations be-
tween this family have been recently studied by Dunn, who
has published a number of papers in advance of the mono-
graph he has now in hand. Although I cannot agree with
Dunn as to all details (Noble, in press), the phylogeny of
the group as he conceives it is probably essentially correct.
The most primitive genera, those with the greatest number
of skull elements and the most salamandrid organization,
are found to-day along the edges of mountain streams and
cold springs of eastern United States. The genera Gyrin-
ophilus and Yseudotriton are the most primitive. Some
species of both of these groups seem at home in the small
pools of still water. This may be a secondary adaptation, for
the majority of plethodoiitids avoid such situations. Pletho-
dontids on land practice cutaneous and buccopharyngeal res-
piration (Seelye, '06) ; in the water, only the cutaneous form.
THE ' HAIRY' FROG' PI'iOBLEllI 371
M7hipple ( '06) showed that Desmognathus and Pseudotriton

ruber do not take water into their mouth when submerged,
and I have repeated these experiments with the same species.
No rhythmical movements of the throat can be found in
specimens swimming in the aquarium. Other observers have
confirmed this statement (Babik, '13). Whipple found that
both Desmognathus and Pseudotriton may be kept alive for
several days submerged in running water. I have not suc-
ceeded in keeping these same species alire in still water of
2 to 3 liters' capacity more than forty hours. P. ruber lives
a little longer than Desmognathus under these conditions. I n
correlation with this entire dependence upon cutaneous res-
piration when in the water and chief dependence (Lapicque
and Petetin, '10) on cutaneous respiration when on land,
the epidermis of all plethodontids is distinctly thinner than
in all adult salamanders of those groups which possess lungs.
Further, the capillaries frequently press slightly into the
epidermis, giving an incipient form of penetration (figs. 16
to 19). I n the more primitive forms, such as Pseudotriton
ruber (fig. E), the epidermis from the sides of the body
consists of from two to four layers of cells. The superficial
capillaries are covered by only two to three epidermal cells
and a thin basal membrane. The conditions are practically
the same in Eurycea bislineata. In the more terrestrial and
also in the more aquatic plethodontids, such as Plethodon
and Stereochilus, the epidermis is even thinner. Occasion-
ally a capillary may be covered by only a single epidermal
cell (fig. 19), and frequently the outer epidermal cells--or
cuticular layer of cells-are so attenuated that it can offer
little resistance to the passage of gases through its walls.
The march of the capillaries toward the cuticular layer doe;
not proceed regularly the more aquatic or the more terres-
trial a lungless form may become. Other factors already
suggested above may enter in to prevent the change. Further,
the limits of penetration frequently seem to be the outermost
layer of the transitional series of cells. (I follow Dawson,
'20, for my nomenclature.) F o r example, Lenrognathus has
372 G . K. SOBLE
apparently been directly evolved from Desmognathus quadra-

maculatus (Dunn, '17 ; Noble, '25). It closely resembles
tlie latter species, but differs remarkably in its more aquatic
habits (Pope, ' 2 5 ) . The integument of Leurognathus
differs only slightly from that of D. quadra-maculatus. A
glance at figure 18 of the integument of the latter species
will show how dangerous it would be to have a greater pene-
tration of the capillaries. The greatly attenuated cuticular
layer mould not be sufficient covering to the large capillaries
below them. I n short, all pletliodontids are lungless and all
have such a thin epidermis that the capillaries need penetrate
Pigs. 16 to 19 Sections oP thc integuincnt f t o m t h r fhnks of various Plctho-

t o the surface.
dontid:ir, made perp~~iidicular
Fig. 16 Pseudotriton ruber (Sonnini). X 380.1.
very slightly into their overlying tissues before they reach a

limit compatible with safety from injury to these capillaries
(compare E. asper and Astylosterrius above). The thin-
skinned plethodontids do not exhibit the striking examples of
capillary penetration of the epidermis which we have seen
Among cryptobrancliids, salamanclrids, and, to a less extent,
among amblystomids, and for the reason that the approach
of their capillaries to the exterior has been gained in another
way, namely, by a thinning of the epidermis.
There are doubtlessly integumentary adjustments other
than the epidermal penetration of capilIaries or epidermd
thiiining correlated with increased cutaneous respiration
within the Amphibia. We have tried to hold ourselves to

those which may be directly compared with conditions de-
scribed above in Astylosternus robustus. There is, however,
one other adjustment which would undoubtedly affect the
-~
17
Fig. 17 Stereocliilus niargiiintus (Hallowell). X 245.4.

Fig. 18 Desmogiiathus quddra-maculatus (Holbrook). X 252.6.
Fig. 19 Pldhodon esehseholtzii (Gray), X 219.8.
3’7-1 G. K. NOBLE
degree of capillary penetration or of epidermal thinning and

hence may be mentioned here. The increase in capillary
number correlated with different environmental conditions is
usually very striking in the urodeles. The exact distribution
of the capillaries has been easily determined from specimens
injected with India ink diluted in normal salt solution. In
figures 20 to 24 I have drawn these superficial capillaries
lying between two costal grooves of a series of specimens.
These figures, therefore, are directly comparable, even
though the width (dorsoventral) of the areas is purely awbi-
trary. It may be seen from the figures that aquatic forms of
Notophthalmus torosus and Pseudotriton ruber have more
capillaries per myotome than the less aquatic Amblystoma
tigrinum and Rhyacotriton. Further, the terrestrial Pletho-
don has fewer capillaries than the related, more aquatic Pseu-
dotriton ruber, but more than the cold-loving Rhyacotriton.
In short, terrestrial salamanders do not possess as many
superficial capillaries as the more aquatic forms, and species
living in cold regions would require fewer yet to fulfill the
demantls of cutaneous respiration. This reduction in tlie
number of capillaries does not proceed as diagrammatically
as tlic figures might indicate. I find little difference between
Desmognathus quadra-maculatus and Leurognathus. Di-
camptodon ensatus lives in the same brooks as its close
relative Rhyacotriton. I have examined the superficial
capillaries only in the larva of the former, but here
they are as numerous as in Amblystoma. It is possible that
the aquatic habits of the larva are accountable for the large
number of capillaries, and the adult will exhibit a considerable
reduction. We may at least conclude that aquatic environ-
ment demands a larger number of superficial capillaries in
tlie salamanders which live in it. Water temperature may
affect this number.
It cannot be argued that the capillary number is dependent
on the size of the cutaneous glands. I n the figures I have
indicated the position of the ducts by small circles. Com-
paring Pseudotriton ruber and Ylethodon vandykei (figs.
20 21
22 23 24
The superficial capillaries between two costal grooves of various urodeles.

Drawn from injected specimens. The grooves are indicated by a broken line at
the top and bottom of each drawing. The position of the ducts of t h e cutaneous
glands is shown by small circles or dots.
Fig. 20 Pseudotriton ruber (Sonnini).
Fig. 2 1 Plethodon vandykei Van Denburgh.
Fig. 22 Notophthalmus torosus (Eschscholtz) .
Fig. 23 Amblystoma tigrinurn (Green).
Fig. 24 Rhyacotriton olpmpicus (Gaige).
376 G . K. ROBLE
20 and 21), it will be seen how the capillary number in the

former has been increased by the addition of small connect-
ing branches which do not occur in the latter. I t will he noted
that in other forms this capillary increase may have modified,
but it has not prevented the penetration of the capillaries
into the epidermis in correlation with a demand f o r greater
cutaneous respircd t’1011.
One might ask why do we find such an exact correlation
between lung reduction and the modification of the integu-
ment? Why did the Amphibia not devise some new way of
breathing which would complicate these morphological cor-
relations? The answer is that the primitive Amphibia util-
ized all the ways possible, and the higher types gave up cer-
tain ways entirely. This would necessarily result in a demand
for increased efficiency in some of the remaining ways. The
increased efficiency in turn has meant morphological change.
Primitive Amphibia respired, 1)by gills, 2 ) by lungs, 3) by
their skin, 4) by aquatic buccopharyngeal respiration, and,
5 ) by aerial buccopharyngeal respiration. On metamorphosis,
the first method was dispensed with and the second elabo-
rated. On the reduction of the lungs the third method was
made more efficient. On complete loss of lungs, the fourth
method has been lost as well as the second. Hence, meta-
morphosed lungless salamanders have only the third and
fifth methods left. It is, therefore, no wonder that the effi-
ciency of these methods has been increased by morphological
change.
The details of respiration in Amphibia have been studied
by numerous investigators. Some urodeles encloivecl with
all five methods utilize one or two methods more than the
others. This may have resulted in morphological change as
well. We shall see that Cryptobranchus, which relies so
much on cutaneous respiration, and Necturus, on branchial,
have no mechanism for separating the arterial and venous
blood in the heart. Whether this cardiac modification is the
cause or the result of the preponderance of some non-pulmon-
ary method of respiration is unknown. The descriptive
method can demonstrate only correlations, not causes. The

changes in the integument discussed above accompany a lung
reduction. The loss of lungs is correlated with a loss of
buccopharyngeal aquatic respiration. The progressive
changes in the integument suggest an increase in the cutane-
ous respiration. Such an increase has been experimentally
demonstrated by Lapicque and Petetin ('10) and Despax
( '23). We have seen that in most urodeles a reduction of thc
lungs was correlated with external factors. In these forms
we find that such external factors as would favor cutaneous
respiration condition, or at least accompany, lung reduction,
which in turn conditions the approach of capillaries toward
the surface (by epidermal penetration or epidermal thin-
ning), and finally leads to a modification of the heart and
truncus. The latter features mentioned here for complete-
ness will be more fully discussed below. These correlations
seem so definite in the urodeles that wherever we find one
modification me may expe'ct the others.
Before turning to the Salientia it may be well to glance
at the caecilians, since they are probably not as distantly
related to the urodeles as usually conceded. No caecilians are
lungless, but one genus, Typlilonectes, unlike its relatives, is
thoroughly aquatic. Fuhrmann ( '14) has shown that in this
genus there is an enormous penetration of capillaries into
the epidermis just as we have seen above in Cryptobranchus
and Euproctus asper. Whether or not Typhlonectes, like
Cryptobranchus, can get along fairly well without the use of
its lungs is not known. It is noteworthy that the only thor-
oughly aquatic caecilian which has been studied should have
the same epidermal modifications as those species of uro-
deles which depend chiefly upon their integument f o r gaseous
exchange. I am aware that Despax ('23) has pointed out
some small differences between the capillary penetration in
Cryptobranchus and Euproctus. These differences are either
non-essential or do not hold in the many samples of Crypto-
branchus integument which I have examined in sections.
378 G. K. NOBLE
We come, at last, to the Salientia, and here at the outset

we getJ into difficulties hecause of the rarity of lung reduc-
tion. There are many cases of thoroughly aquatic forms,
but these usually have large lungs. F o r example, the lungs
of Xenopus tropicalis are enormous. I find in my sections
of the skin from the sides of the body of this species no
penetration of capillaries into the epidermis, and there is no
excessive thinniiig of epidermis beyond the variations shown
in R>ana. Rlinckotvstriim ( '94) has described a similarly
thick, non-vascular epidermis in Pipa. Bombina maxima,
which lives in colder waters and is apparently more terres-
trial, is also unmodified. The terrestrial Rufo terrestris and
Eleutherodactylus ruthae I have compared with the semi-
aquatic Rana clamitaris and R. pipiens. The descriptions of
the integument of terrestrial Saleiitia are numerous, but as
these authors have not always examined skin from the sides
of the body, I h a r e checked their results with my sections
from the terrestrial and somewhat'translucent R. sylvatica.
We may at once conclude that all terrestrial or aquatic Salien-
tia possessing well-developed lungs exhibit no especial modi-
fications of the epidermis on the sides of the body for assur-
ing cutaneous respiration.
The lungs of not all Salientia are equally developed or
equally vasculated. The terrestrial Rlytes (Boulengcr, '97)
has smaller and less vasculated lungs than the aquatic Born-
bina. The terrestrial Bufo, 011 the other hand, has highly
vasculated lungs. Bufo, as a rule, seeks drier regions than
Alytes, arid hence might be expected to demand less from its
integument. Only one species of frog other than Astyloster-
nus robustus is known to me to have greatly reduced lungs.
This is Ascaphus truei, a species now well known, especially
from the researches of Gaige ('20), to be confined to high
altitudes of northwestern United States where it can secure
its requirements of low temperature and suitable breeding
sites. At these low temperatures one might suppose that
cutaneous respiration alone (or with buccopharyngeal res-
piration) ~vonltlsuffice, a s in the case of Rana hibernating
T H E ‘HAIRY FROG’ PROBLEM 379
under the water. hscaphus remains, in fact, for considerable

periods under the water, as Mr. Phillips Putnam, who col-
lected my specimens, has assured me. Apparently its activity
in and about these cold waters (40°F.) is such as to demand
a greater cutaneous respiration than in the hibernating Rana.
Its integument is modified, as we have seen in both sala-
manders and caecilians, by a penetration of capillaries into
the epidermis (fig. 12). If we compare this integument with
that of the female Astylosternus rohustus (fig. 4), a striking
agreement will be found.
There is one other frog which I have studied not because
of any great reduction of its lungs, but because of a dermal-
fold formation along the thighs and sides of the body simu-
lating the conditions in Cryptobranchus. This frog, Batra-
chophrynus, lives at high altitudes in Peru and is purely
aquatic (Barbour and Noble, ’20, p. 408). The waters of the
lakes in which it lives are very cold. It is perhaps therefore
not surprising that its lungs should be shorter and decidedly
less vascular than in its relative, Leptodactylus pentadac-
tylus, which attains about the same size. These lungs are,
however, by no means rudimentary. Allen (’22, p. 52) has
studied the habits of the closely related Telmatobius culeus,
which agrees with Batrachophrynus in form and habits.
allen states that in Lake Titicaca T. culeus “was never ob-
served t o emerge from the water; was never found out of
water; was never seen rising to the surface to breathe, and
never seen swimming more than a few inches from the
bottom. ’’
The only specimens of Batrachophrynus microphthalmus
available to me were fixed in wood alcohol and are almost
worthless histologically. Sections of the folds from the sides
of the body reveal a grouping of the epidermal cells which I
interpret as due to a penetration of capillaries into the epi-
dermis. I n short, better-fixed material will very probably
sliow that in this completely aquatic frog, just as in Crypto-
branchus, the skin has assumed the major r61e in respiration.
In order to secure a better cutaneous respiration, greater
380 G . H. NOBLE
surface area has been obtained by the formation of loose folds

or flaps. 9comparison between the folds of Cryptobranchus
and the ‘hairs’ of Astylosternus has been made above. A
further comparison of the ‘hairs’ with the folds of Batra-
choplirynus is at once suggested. Batrachophrynus has pro-
portionately larger lungs than Astylosternus, but it does not
depend very much on them for respiration. I n frogs, as in
urodeles, a great reduction or functional loss of the lungs
has resulted in an increased cutaneous respiration. Urodeles
secured a greater efliciency in cutaneous respiration by either
the penetration of capillaries into the epidermis o r by the
thinning of the whole epidermis over the superficial capil-
laries. 111 the Snlientia only the first of these two methods
was adopted.
In this series of observations we have compared skin from
the sides of the body of all forms chiefly because this repre-
sented an average type of integument, but also because the
‘hairs’ of Astylosternus are especially well developed on the
flanks. I n conclusion it may be well to point out that there are
regions other than the sides of the body which function in
cutaneous respiration. I n other Salientia some of these
regions may serve to a better advantage than the integument
from the flanks.
We have seen in the first part of this paper that Kukenthal
was mistaken ill comparing the hair-like appendages of Asty-
losternus robustus with the tubercles from the sides of the
head and the dorsal surface of the body. They are in no way
comparable, for the first is primarily a respiratory organ
and the latter owes its tubercular character to an aggregation
of integumentary glands in the underlying derm. There is
another kind of tubercle scarcely developed in Astylosternus,
but pronounced in arboreal frogs. Kiikenthal made no men-
tion of these.
Arboreal frogs differ from terrestrial ones in having their
abdomens and ventral surfaces of the thighs covered with a
pavement of large, flat tubercles. Familiar examples occur
among Hyla, Hylambates, and Rhacophorus. This correla-
T H E ‘ H A I R Y FROG’ PROBLEM 381
tion of ventral tubercles with arboreal life is very close.

Within a single genus arboreal forms will possess these struc-
tures, while terrestrial or aquatic forms will exhibit smooth
surfaces. I have recently studied the habits of various species
of Eleutherodactylus in Santo Domingo. E. inoptatus, E.
auriculatoides, and E. ruthae frequent plants, bushes, or trees.
They all possess ventral tubercles. E. weinlandi and E.
schmidti are terrestrial and lack these structures. Similarly,
Dr. E. R. Dunn has very recently found in Cuba that the
arboreal forms of Eleutherodactplus all possess ventral warts
while the terrestrial species arc smooth. What is the func-
tion of these tubercles? To insure greater adhesion to the
trees? Sections show that there is no aggregation of glands
in these warts. They owe their form t o dermal papillae. It
is possible that they function by increasing the friction. The
ventral surfaces of arboreal frogs tend to adhere to an up-
right support.
It is possible that in some forms these warts have another
function as well. In Santo Domingo there is found a large
tree-frog, Hyla vasta, that spends the daylight hours high
in the trees and the evenings along mountain streams. On
several occasions we traced the frogs by their voice as they
approached the stream beds at dusk. Why did they come
to these streams? The breeding season was past, and while
some males were calling, we never found any pairs in embrace.
The chief features of these rocky ravines were their dampness
and their coolness. Nearly fifty specimens of Hyla vasta
were captured on rocks overhanging the current. The ven-
tral surfaces of all these frogs were highly vasculated, the
abdomen, thighs, and digits appearing pink to the unaided
eye. When one of these specimens was injected with India
ink a large part of the abdomen and thighs blackened. This
darkening was due to the superficial capillaries covering the
warts and adjoining regions (fig. 29). On sectioning, it W R S
found that the capillaries actually penetrated into the epi-
dermis of the warts. Could the function of these warts be
similar to the hairs of A. robustus?
382 G . I<. NOBLE
In Saiito Doming0 there is another tree-frog, Hyla domini-

censis, which has not such a restricted habitat; it occurs in
almost any wooded region. This frog was frequently dis-
covered during the day on the ground under piles of vegetable
debris. On injection, it was found that the superficial capil-
laries, although as numerous in each wart (fig. 28), did not
blacken so great a part of the ventral surface as in H. vasta.
Further, they were not quite so superficial in any wart. I n
the American tree-frog, H. cinerea, a somewhat similar pene-
tration was found, but in the diminutive H. crucifer the pene-
Figs. 2 5 to 29 A coinpiirisoil of thc vaseularizatiori of the integument of the

chest anti ventral tubercles in terwstri;il arid :~rhore:tl frogs. #&ions perpen-
dicular to the surfnre of t h e body.
Fig. 2.5 Iiitegiimeiit from the chest of H:iii:~ sy1vstiv:t Lo Conte. X 293.
tration was slight. The number of layers of cells in the

epidermis of the larger species of Hyla does not vary greatly.
I can think of no reason for the penetration of capillaries
into these ventral tubercles other than to increase the respira-
tory efficiency of this integument. It is possible that these
surfaces pressed against the ground have greater need for
an oxygen supply than the integument of the back. But in
the crouching position other parts of the body integument
are not exposed to the air, as, for example, that between
thigh and body wall. Why are these surfaces not as highly
vasculated as the ventral papillae? Comparing the integu-
ment from the ventral surface of the thigh of any of these
29
Fig. 26 Section of part of one of the tubercles from the pubic region of Rana
sylvatica. Le Conte. x 203.
Fig. 27 Section of part of oiie of the femoral tubercles of HyIn domini-
censis (Tschudi). X 293.
Fig. 28 Superficial capillaries of one of the femoral tubercles of I-Iyla domini-
censis (Tschudi), injected specimen.
Fig. 29 Superficial capillaries of one of the femoral tubercles of Hyla vasta
Cope, injected specimen,
384 G. K. NOBLE
large hylas with the integument from the same region in the
fossorial Scaphiopus holbrookii, a marked difference will be
fourid, f o r not only are the tubercles lacking, but there is no
penetration of capillaries into the epidermis. I n such a ter-
restrial form as Rana sylvatica tubercles similar to those of
Hyla, hut smaller, arc found on the pubic and femoral regions,
but lacking from the abdomen. On sectioning, the tubercles
from these regions are found t o have capillaries penetrating
into the epidermis.
It would therefore seem that arboreal frogs which are in
danger of drying their skins sufficiently to hinder cutaneous
respiration, and even terrestrial frogs which are at home
among the dry leaves of the forest floor, have that portion
of their integument most apt to be moist under these condi-
tions richly supplied with capillaries penetrating into the epi-
dermis, apparently serving as a center f o r cutaneous respira-
tion. This docs not apply to the ventral surfaces of the feet
which frequently possess a thickened epidermis. It may be
seen from figures 25 and 26 how different is the appearance
of the integument of the pubic region and from the chest of
Rana sylvatica. The number of capillaries to each tubercle
may be very numerous in the larger hylas. The capillaries
are apparently of a greater caliber in Hyla vasta than in H.
dominicensis. It would seem from the greater extent of this
superficially vasculated area in H. vasta that it depended
more upon cutqieous respiration than did H. dominicensis.
.r-
THE NATUltE OF THE DIGITAL BLOOD SINUSES IN AYPHIBlA
If the abdominal and femoral tubercles of Salientia serve

as special centers of cutaneous respiration, we might expect
that other integument brought in contact with the substratum
would similarly function. In other words, the palms and soles
might he expected to facilitate cutaneous respiration in ter-
restrial or arboreal Amphibia. Some years ago, Ritter and
Miller (’99, p. 695), impressed by the blood sinuses, or better,
rete, which were plainly visible on the tips of the digits in the
semiarborcal Aneides lugubris, went so far as to say: “The
toes, in fact, may be considered to have assumed in a measure

the function of external gills.” Ritter and Miller found simi-
lar blood sinuses in the digits of two species of Plethodon
having habits similar to Aneides, “while in Diemyctylus toro-
sus, the habits of which are quite different, and in which
lungs are present, no unusual degree of vascularity is found
in its members.’’ Digital sinuses similar t o those of Aneides
lugubris may be seen in nearly every species of Plethodon.
I have studied them in P. eschscholtzii, P. vandykei and P.
cinereus. They are well marked in P. glutinosus, but,
strangely enough, cannot be seen without sectioning in the
closely related P. metcalfi. The question arises as to whether
similar rete or sinuses are not present in all salamanders,
although obscured from view by the overlying pigment in
many forms. By means of India-ink injections of a series of
forms, I have been able to determine that sinuses of a greater
or smaller size are actually present in all species, whether
these be aquatic or terrestrial. I have examined in addition
to the plethodons mentioned, Eurycea bislineata, Stereochilns
marginata, Rhyacotriton olympicus, Amblystoma macrodac-
tylum, A. opacum, and Dicamptodon ensatus. I n some cases
the injected appendages had to be cleared before the exact
extent of these sinuses could be determined. As shown in
figure 31, A and D, the sinuses are possibly slightly larger in
the terrestrial Plethodon eschscholtzii o r P. cinereus. They are
present, however, in the aquatic Stereochilus and even in the
larva of Dicamptodon ensatus. The latter species has horny
coverings to its digits, making it practically impossible for its
digital rete to assist in cutaneous respiration.
When sections are made of the digits of‘ P. eschscholtzii,
the form having the largest sinuses, it is found that the epi-
dermis covering the blood sinuses is very thick as compared
with that from the sides of the body (fig. 30). Since, then,
the sinuses are found in all urodeles, whether purely aquatic
o r terrestrial, and are fairly well developed even in those
aquatic larvae that have the digits covered with a thick, horny
sheath, it does not seem possible that these sinuses could be
386 G . I<. NOBLE
correlated with-we may say called out by-a great demand

for cutaneous respiration in the region of the digits.
Is there, however, any other explanation f o r the digital
sinuses ? I n the early larva, at least in Desmognathus quadra-
maculatus, the only form I have examined f o r this peculiarity,
a single capillary runs completely around the periphery of
each digit. As development continues, other capillaries de-
velop. There would result from this process a point near
the end of the toes where the capillary before doubling back
on itself joined with some of its neighbors to form a rete. As
the capillaries in the lungless P. cinerea are proportionately
of B greater diameter than in Amblystoma, we would seem to
have a larger rete in Plethodon than in Amblystoma. Fur-
ther, the number of capillaries would be dependent on the
size of the digit and capillaries. This may be made clearer by
an examination of the figures (fig. 31). Such an explanation
would not acconn t for the difference between P. eschscholtzii
and Amblystoma. Undoubtedly, other factors enter into con-
sideration. Tt seems very unlikely that these slight differ-
ences could be due to a greater function in cutaneous respira-
tion. In urodeles the epidermis from the sides of the body
is histologically better suited for cutaneous respiration than
that from the digits. It apparently plays a much greater
rBle. I n arboreal and terrestrial frogs with well-developed
lungs the abdominal and femoral tubercles may serve as great
or a greater part in cutaneous respiration than the integu-
ment from the sides of the body.
THE ORIGIN 0)’ LUNQLESSNESS
It has been pointed out in the first part of this paper that
the method of lung reductioii in Astylosternus robustus is
unique among the Amphibia. Lung reduction in other forms,
both frogs and urodeles, proceeds on a different plan and is
usually correlated with certain environmental factors. Almost
notliing is known of the habits of Astylosternus, but it may
be safely assumed that these environmental factors have not
been operative here.
THE 'HAIRY FROG' PROBLEM 38'7
As recently pointed out by Wilder and Dnnn ('20, p. 63),

most salamanders with the lungs reduced or lacking either
live to-day in the vicinity of mountain brooks or have origi-
nated from species which lived in this habitat. Wilder and
30
I
A D
t C
3 1
The digital sinuses of urodeles.
Fig. 30 Longitudinal section (perpendicular to the surface) of the integument
from ventral surface of the digit tip of Plethodon esc,hscholtzii (Gray). X 211.
Fig. 31 A comparison of t h e digital sinuses of: A, Plethodon eschscholtzii
(Gray) ; B, Dicamptodon ensatus (Eschsclioltz) ; C, Amblystoma maerodaetylum
Bairn ; D, Plethodon cinereus (Green).
388 G . Ti. KOBLE
Dunn are inclined to think that this reduction may be corre-

lated with the swift current of these streams, forms having
well-developed lungs would he swept t o their destruction be-
cause of the hydrostatic nature of their lungs. They point
to the fact that a lungless form sinks to the bottom of such
streams aiid crawls, while the adults and larvae of newts
(Triturus) which they placed in such a stream could not
maintain their way against the current. There can he little
doubt that tlie current v-ould prevent the iiewts from invading
tlie mountain-brook habitat. It is, however, to be doubted
tliat natural selection working in this brutal way has been
the only factor fostering the development of lnngless forms
in the mountain-brook habitat.
In the first place, all mountain-brook salamanders may be
divided into two types : those that live primarily in the water
aiid those that live primarily along the margins of the brook.
The first group comprises Ranidens sibiricus, Amblystoma
altamirani, and the recently derived Leurognathus. The first
two genera, in direct contradistinction to the hypothesis of
Wilder and Dunii, possess lungs. There was some doubt in
D L ~ ~original
s ’ description as to the habitat of A. altamirani,
but Gadow (’08, p. 16, footiiote) has shown that the meta-
morphosed adult is purely aquatic. Both A. altamirani and
R. sibiricus are high mountain forms. The cold tempera-
tures of their habitats map facilitate their respiration under
water, but the current has not been detrimental to their pro-
gression in these streams.
The second category of mountain-brook salamanders would
come during adult life under the influence of this current
factor only at such intervals as when seeking to avoid their
enemies or in some cases when laying their eggs. The genera
of this second category hare the lungs either partly or entirely
reduced.
Aiiotlier reason for our seeking the coritrolliiig factor not
in the water, but near tlie water, is that two such closely re-
lated genera as Dieamptodon and Rhracotriton live side by
side in the mountain brooks, and yet the former has pro-
portionately larger lungs that the latter. The former genus

upon metamorphosis leaves the vicinity of the torrents where
it passes its early life t o take up a terrestrial abode. The
latter, however, remains in the vicinity of the streams and
seems at ease both in and out of the cold waters. It is there-
fore apparent that Boulenger (’17,p. 802) has pointed out
the more important factor when he writes (translation) :
“The greater part of the species in which the absence o r
regression of the lungs has been determined live in obscurity,
or more or less shaded from the active light, a mode of life
which tends to render the gaseous exchanges of respiration
less active.”
Now it is difficult t o imagine a locality offering greater
opportunities for cutaneous respiration than the immediate
vicinity of a cold mountain brook. Such water, due to the
many falls, is highly aerated and, due to the cold, must contain
much oxygen. How much greater the oxygen content of this
cold water must be over that of a pond may be realized from
scanning the Smithsonian Tables of Physical Constants show-
ing the solubility of gases in water. This table, kindly called
to my attention by Prof. F. H. Pike, shows that only 0.0368
gram of oxygen is absorbed in 1000 grams of water at 30°C.;
0.0443 gram at 20°C. ; 0.0551 gram at IOOC., and 0.0705 gram
at 0°C. Cold, highly aerated water contains, therefore, nearly
half again as much oxygen as pond water. This habitat, it
would seem, should demand less from the lungs during larval
life and possibly hinder their development. After metamor-
phosis the salamanders find themselves in an ideal spot f o r
aerial cutaneous respiration, namely, the cold, damp crevices
between the rocks near water.
It is important to emphasize this cold factor, for it is this
which seems to have been chiefly operative in the case of the
Salientia. Rana hibernating under water does not use its
lungs. The nearly lungless Ascaphus very soon dies if ex-
posed to the air at ordinary temperature. I have kept a large
series of Ascaphus alive on ice for over a year! During this
time they were quite active, but refused to feed. The tadpole
390 CX. I<. NOBLE
of Ascaplius lives in icy brooks and lacks all trace of lungs

at the time the hind-limb buds appear. The tadpole of Hyla
heilprini lives in equally swift torrents in Santo Domingo,
but here the water runs from 74" to 78"F., and this species has
well-developed lungs at exactly the same stage. Batra-
chophrynus, which we have mentioned as living in thc cold
lakes of the Peruvian highlands, has reduced and poorly vas-
culatcd lungs.
There can be little doubt that the plethodontids arose in a
mountain-brook habitat, but not all lungless salamanders.
M7e have emphasized the cold factor in the case of Eatra-
clioplirynus a i d also for Ascaplius. The current factor might,
however, be equally well employed in the case of the latter.
Undoubtedly, the mountain-brook habitat-current, cold, and
conditions along the edge of the stream-has been the spot
which has fostered lunglessness in hynobiids, amblystomids,
salamandrids, and plethodontids. There is, however, some
evidence that lunglessness may have arisen in at least one
salamandrid under other conditions. Salamandrina we have
compared above to the red land stage of Triturus viridescens.
The typo of integument found in the former may have been
directly derived from that of the latter. In another paper
I have brought forth considerable evidence to show that life-
history is a much better indication of relationships than
usually conceded (Noble, '25). Now, the eggs and larvae
of Salamandrina approach more nearly t o those of Triturus
or Notophthalmus torosus than they do to Euproctus. From
this life-history data it would seem that Salamandrina may
have arisen directly from one or the other of these genera,
without ever having occupied the mountain-brook habitat.
The reduction and loss of lungs we have seen above to be
directly correlated with an increase in cutaneous respiration.
No integumentary change toward assuring a greater gaseous
exchange occurs usually until after metamorphosis. All Am-
phibia destined to live an adult life without lungs (or very
reduced ones) either fail to develop a many-layered epidermis
o r push the superficial capillaries into such a covering. In
short, even the most ideal environmental conditions are not

good enough for Amphibia to live by only cutaneous respira-
tion through such a thick epidermis as is found in the more
primitive forms. The mountain-brook region seems to have
been the habitat in which most lunglessness arose. Several
factors seem to be operative in such a habitat fostering lung-
lessness. Wilder and Dunn ('20) have emphasized the cur-
rent factor, Boulenger ( '17), the darkness and dampness
factor, while I have stressed the greater oxygen supply in
cold and in running water. It is probable that all these fac-
tors are operative, tending to produce lunglessness in
Amphibia.
The lung reduction of Astylosternus is not correlated with
a mountain-brook habitat. It is possibly not correlated with
any environmental factors. Nevertheless, compensatory
changes in the integument have proceeded in Astylosternus
along one of the two methods adopted by all Amphibia. The
reduced lungs of Astylosternus must have considerable effect
on its behavior. It remains for the field naturalist to deter-
mine the extent of these changes in habits.
CHANGES I N T H E AURICLES AND TXUNCLJS CORRELATED WITH A

REYUCTIOX I N PULMONARY RESPIRATION
It might be assumed that with a reduction of the lungs o r

an enormous increase in the cutaneous respiration the heart
would necessarily undergo certain changes. A study of the
literature does not give us a clear picture of such modifica-
tions. Iiopkins ('96) thought there was a reduction of the
left auricle in lungless salamanders and announced the dis-
covery of a rudimentary auricular septum in these forms.
Bruner ('00) showed that Hopkins had confused the sinus-
auricular valve with a rudimentary septum. He showed that
there was no remnant of the left auricle in lungless salaman-
ders. But instead of assuming that the left auricle has be-
come reduced until it has finally disappeared, Bruner tells us
(p. 330) that the shifting of the position of the sinus-auricular
valve "is t o be accounted for by the disappearance of the
392 G. R. NOBLE
septum atriorum. ” Bruner gives n o evidence f o r this view, and

it is very difficult to imagine how the sinus-auricular valve left
stranded between the two auricles could have gained a new
attachment to the left wall of the now confluent auricles. We
might expect that any series of urodeles showing a gradual
reduction of the lungs would illustrate various stages in the
reduction of the left auricle or, if Bruner is right, in the
reduction of the auricular septum and migration of the valve.
Such a series of urodeles is found within the genus Euproctus.
Dehaut (’ll), the only investigator t o study the hearts of
these forms, failed to examine the auricular septums, and his
conclusions based on the external anatomy of these hearts
must he taken with considerable reserve, because usually in
all Amphibia there is no external indication of the position
of the septum. I have examined the internal structure of the
hearts of a large series of Amphibia and have attempted to
correlate the changes in auricles, in septum, and in truncus
with functional changes. These correlations clear up con-
siderable misunderstanding prevalent in regard to the separa-
tion of arterial and venous blood in the vascular system of
the Amphibia.
I t is generally believed that the auricular septum of uro-
deles is greatly perforated, permitting a mixture of arterial
and venous blood (Kerr, ’19, p. 390). Long ago Langerhans
(’73) described the auricular septum of Salamandra rnacu-
losa as a mere trestle work. Langerhans’ figure is rather
diagrammatic, but shows clearly that he regarded the upper
two-thirds of the septum as greatly fenestrated. Some va-
riation was to be found as to the extent of this perforated
zone, but Langerhans ( ’73, p. 458, translation) concludes :
“never have I missed the areolar structure of the upper part
in about 20 individuals. ” Later, Boas ( ’82, p. 183) confirmed
the observations of Langerhans on the auricular septum of
Salamandra, but adds that he has never seen so many per-
forations as Langerhans described. I have examined the
hearts of only four specimens of Salamandra maculosa, but
these mere especially fixed and stained to demonstrate the
auricular septum. The blood was first washed from the living
heart with normal salt solution, the beating gradually stopped
with chloretone, a ligature applied to the moderately dis-
tended heart, and the preparation immersed in fixing fluid.
Of the variety of fixing fluids used on these and other hearts
(Carnoy’s, Lovdowsky’s Zenker ’5, and Bouin’s), Zenker ’s
proved to be the most satisfactory. I have represented in
figure 32 a large part of the upper two-thirds of the auricular
septum of Salamandra maculosa. It will be noted that there
is only a single small perforation. Some specimens show
over a dozen of these minute holes which never approach the
condition shown by Langerhans.
I have studied by this same method the auricular septum
of Amblystoma opacum, a.macrodactylurn, A. maculatum,
A. paroticum, A. tigrinurn, Dicamptodon ensatus, Notoph-
thalmus torosus, Triturus viridescens, Pleurodeles waltl, Am-
phiuma means, Siren lacertina, Rhyacotriton olympicus, and
Cryptobranchus alleganiensis. I n several cases larvae have
also been available to me. It is well k i i o ~ ~that
i i the auricu-
lar septum of the larval salamander is complete (Kerr, ’19).
I have found it complete in the larvae of Amblystoma p r o -
ticum, Dicamptodon ensatus, and also in the recently meta-
morphosed Amblystoma tigrinurn. Shortly after metamor-
phosis in Amblystoma tigrinurn the muscular fibers in the
septum appear to group into bundles. I n the interspaces
between the bundles the septum is formed of merely two
sheets of thinned epithelium separated here and there by
connective-tissue cells. In the center of those interspaces
which apparently receive the greatest strain small perfora-
tions occur of exactly the same character as in Salamandra.
In Triturus, and to a large extent in Salamandra, the bundles
of muscle cells are more pronounced and the interspaces
wider. I n the adult Notophthalmus torosus and Pleurodeles
waltl the perforations are more numerous than in the adult
Amblystoma opacum. These perforations vary in every indi-
vidual, never occurring in exactly the same position twice.
They are always small, never forming a meshwork such as
394 G . I<. NOBLE
Langerhans described for botli Salamandra and Triturus.

The auricular septum of Rmphiuma and Siren is very simi-
lar to that of Amblystoma. I n none of these forms of Am-
blystoma, Dicamptodon, Notoplithalmus, Triturus, Pleuro-
deles, Siren, and Ampliiuma could any extensive exchange of
arterial and venous hlood occur between heart beats. I have
injected with a micro-injector a solution of India ink in nor-
mal salt into the left auricle of tlie beating heart of Notoph-
thalmus torosus and Amblystoma opacum. These hearts are
fairly translucent, but I could never see under the binocular
any of the dark solution working its way through the auricu-
lar septum into the right auricle.
I have repeated this experiment with Rhyacotriton olym-
picus. In this form the lungs vary from 2 to 7 mm. in length
and average approximately 5 mm. in adult specimens meas-
uring from 79 to 105 mm. total length, 48 to 58 mm. head
and body length. When the heating heart was washed free
from blood the auricular septum was plainly visible. Its
relative position (figs. 34) showed that the left auricle of
Rhyacotriton had been considerably reduced in size. Hence,
in Rhyacotriton R reduction of the left auricle had accom-
panied a reduction of lung capacity. Injections of India ink
in normal salt were then made into tlie pulmonary vein by
means of a micro-injecting apparatus similar to that described
by Brown ( '23). The lieart was beating normally and pumped
the injection mass into the left auricle. This ink diffused
through the auricular septum. Total preparations of the
distended heart made similar to those of the above urodeles
showed that the auricular septum in Rhyacotriton is greatly
fenestrated. The muscular bundles seen in the lunged sala-
manders were in this form proportionately larger ; the epi-
thelium, which ii: the other forms covered the interspaces
like a thin cloth over a lattice-work, was in Rhyacotriton re-
duced to little patches which here and there still retained
their original arid probably larval position, but in the major-
ity of cases was merely wrapped around the muscular bundles
permitting the coiltents of one auricle to flow freely into the
The auricultrr septum of urodeles
Fig. 32 The central portion of tlie aiiricu1:tr septum of Salamandrn maculosa
(Laurenti), approximatel? half of the entire septum.
Fig. 33 The auricillar septum of R h p e o t r i t o n olympicus (Gnigc) as seen
from the right a f t e r the removal of the riglit auricle.
Fig. 34 Diagram of the auricles of Rhyncotriton olympicus (Gaige), showiug
the disproportion in size of the auricles :In? tlie position of tlie septum.
39.5
J O U R N A L OF MORI’HOlrOHY A h 0 I’HYBTOLOCY, VOL. 40. NO. 2
396 G. K. NOBLE
other. This, enormous fenestration of the auricular septum

(fig. 33) is not due to faulty technique as in the case of Lan-
gerhans ’ preparations of Salamandra. I have prepared the
hearts of A. macrodactylum of practically the same size as
those of Rhyacotriton by the same method and have secured
very different results. The hearts of ten specimens of Rhyaco-
triton injected with normal salt and fixed in Zenker exhibited
a fenestration similar to that described.
As Rhyacotriton olympicus is the only available urodele
having greatly reduced lungs, we may assume that it rep-
resents an intermediate stage between the lunged and the
lungless salamanders. It is therefore apparent that a reduc-
tion of the lungs and, hence, reduction of the volume of blood
returned t o the lieart, brought about a reduction in the size
of the left auricle. At a certain stage some other factor en-
tered in to cause a fenestration of the auricular septum, which
in turn permitted a mingling of the arterial and venous blood.
Is there any evidence as to the nature of this second factor?
In striking contrast to the lunged forms described above,
the auricular septum of Cryptobranchus alleganiensis and,
to judge from the published descriptions, those of Megalo-
batrachus, of Proteus, and of Necturus, are represented by
only a series of muscular strands. It would seem that a great
part of the interspaces between the muscle bundles found in
Amblystoma had in these forms disappeared. The arterial
and venous blood must mix to a certain extent in the auricles
of the Proteiidae and Cryptobranchidae, while in all other
adult salamanders which possess well-developed lungs this
mixture must be very slight, if any.
It will be noticed at once that outside of the lungless forms
it is just these families, the Cryptobranchidae and Proteiidae,
in which methods of respiration other than pulmonary have
gained an ascendancy. We have seen that cutaneous respira-
tion was the chief method of Cryptobranchus and branchial
in Necturus. In urodeles, therefore, in which the lungs are
well developed, hut play only a small part in respiration,
the auricular septum has degenerated so far that it no longer
serves to separate arterial from venous blood. This suggests

at once that the fenestration of the auricular septum of Rhya-
cotriton was caused by disuse of the lungs in respiration. It
is apparent that small lungs cannot play a very large part
in the respiration of the animal. Lungs that are not contract-
ing and expanding would be subject to fewer kinds of pressure
than those which do. It is possible that the current in the
blood vessels of the urodeles which do not frequently empty
their lungs is less than in the pulmonary vessels of the other
group. Experiments could be devised to demonstrate if the
factor determining the fenestration of the auricular septum
is the slow rate of blood flow. The present observations dem-
onstrate only the following facts:
1. A reduction in size of the left auricle occurs in urodeles
having reduced lungs, and no reduction occurs if well-devcl-
oped lungs are maintained whether or not these be frequently
used in respiration.
2. All urodeles possessing lungs which play a large part
in respiration have a functionally complete auricular septum,
while all those in which either the gills, the skin, or the bucco-
pharyngeal surfaces have assumed the major r61e in the res-
piration of the adult exhibit a greatly fenestrated septum.
This is a secondary degeneration, for the larvae of all lunged
urodeles possess a complete septum.
Turning to the Salientia, we find a very close parallel.
Ascaphus has reduced lungs and its left auricle is relatively
much smaller than that of other frogs (as Rana). The lungs
are proportionately larger than in Rhyacotriton. Its auricu-
lar septum is complete. The septum of Astylosternus cannot
be studied critically without live material (or better-fixed
specimens). I doubt, however, that its auricular septum will
be found to be perforated because, as we shall see below, the
structure of its truncus excludes such a possibility. More-
over, the vascular part of its lungs is proportionately greater
than in Rhyacotriton.
The functional completeness of the auricular septum of all
hmphibia, both urodeles and frogs, having well-developed
398 0. I<. NOBLE
liuigs playing a large part in respiration suggests that in

these forms there may be a fairly complete separation of
arterial and venous blood throughout the body. Numerous
physiologists have studied the separation of arterial and
venous blood in the heart of Rana. A convenieiit summary
of their observations is given by Gaupp ( ’99, pp. 281-284). ‘
He (’99, p. 384) concludes that the separation is not complete,
but that “the vessels of the respiratory circuit contain the
highest venous, the liead vessels the greatest arterial blood”
(translation). A similar view is adopted by most recent text-
books of physiology (as, €or example, Burton-Opitz, ’20,
p. 257). The proof of even this amount of separation of
arterial and venous blood does riot rest upon a very sound
evidence. As recently as 1914, Pahlman (p. 130) dogmatically
states: “there is no proof of a segregation of arterial and
venous blood throughout the vertebrate scale excepting in
the post-foetal bird a i d mammal and possibly in the crocodile
family. ’’
Fortunately, there is a very simple way by which this ques-
tion may be settled. With the micro-injectilig apparatus
mentioned above it is possible to pass a stream of India ink
in normal salt solution into the pulmonary vein of even the
smallest specimens. If small, translucent specimens are used,
the course of tlie India ink through the heart and truncus
may be studied for several heart beats, that is, until the
ventricle becomes so choked with ink that there is no longer
a visible distinctioii between arterial and venous streams.
The success of this demonstration is largely dependent on
the normal pumping of the heart arid the utilization of such
a small stream of ink that tlie blood flow, both arterial and
venous, proceeds iiormally. The glass canula should be so
small that wheii inserted at an angle into tlie pulmonary vein
it does not materially obstruct the flow of blood in this vessel,
1 have made successful demonstratioils oii the following
species : Notophthalmus torosus (2), Triturus viridesceiis
(6), Amblptoma maculatum (I),A. opacum (2), Scaphiopus
holbrookii (1), Hyla crucifer ( 3 ) , acris gryllus ( a ) , Rana
T H E ‘ H A I R Y FItOG’ PRORLEM 399
clamitans juv. (1). In all of these species the India ink dur-
ing the first four o r five beats, that is, until clouding the
ventricle entirely, was distributed t o the first a i d second
aortic arches, never to the third or fourth (of salamanders).
I n the salamanders the ink was distributed approximately
equally to the first and second arches, while in the frogs the
posterior half of the second arch usually remained red as the
black blotch swept domi the first and anterior part of the
second arches. I n no case where the heart flow was normal
and the needle correctly inserted was there any exception
to this rule.
I n contrast to the results obtained above, I never sue-
ceeded in obtaining a segregation of the ink in Rhyacotriton
nor in Cryptobranchus. The latter is so large and its aortic
arches so opaque that the demonstration is not very exact.
Rhyacotriton, on the other hand, has these structures so
translucent that there can be no doubt that in that genus a
separation between arterial and venous Mood is not main-
tained in the truncus.
Very recently, Ozorio de Almeida ( ’23) has shown that in
a frog (Leptodactylus) the arterial and venous blood remain
distinct during their passage through auricles, ventricle, and
truncus. The technique employed by this investigator seems
simple and apparently as efficient as that which I have util-
ized. Ozorio de Almeida notes that any interference with the
movements of the auricles, as, f o r example, that produced by
the application of ice, brings about a mixture of the arterial
and venous blood in the rentricle. I have noticed the same
mixture of my injection mass when the diastole of the auricles
mas mechanically hindered. The separation of arterial and
veiious blood is maintained in the auricles of the Salientia by
the septum. It has been assumed by earlier workers that the
spongiose tissue of the ventricles continued this separation,
and I have not evidence to disprove this view. There is, how-
ever, little agreement in the literature as to how the two
kinds of blood emerging from the rentricle are kept distinct.
In general it is belieded that the pulmonary arch would o f e r
38
39
400
legs resistance than the other arches, and the first blood, the
venous, emerging from the ventricle would flow through this
outlet, leaving the other channels for the arterial blood. I n
frogs the spiral valve is believed to assist this separation of
blood (Gaupp). Pohlman ( ’14) claims that the structure of
the valve precludes such a possibility. Bruner (’00) thinks
that in salamanders the function of the spiral valve is to pre-
vent the collapse of the conus. In support of this view, he
claims (p. 329) that : <‘aspiral valve is distinctly recogniz-
able in lungless forms. ” Rruner worked with Salamandrina,
Plethodon, Desmognathus, and Hydromantes. Recently
Cords (’24) has failed to find any spiral valve in Sala-
mandrina.
I have examined the truncus of a large series of Amphibia
and have found that the spiral valve ( o r a functionally simi-
lar structure) is always present in those species in which the
arterial and venous blood streams retain their identity, and
is always absent in those species in which the blood streams
are mixed. There is no spiral valve in any lungless sala-
mander. The truncus of all plethodontids is essentially the
same and similar to that of Plethodon glutinosus (fig. 39),
which I have figured as split open along its left side. I have
examined the truncus of several specimens of Pseudotriton
ruber, P. montanus, Desmognathus yuadra-maculatus, Pleth-
odon metcalfi, and P. glutinosus. Further, the urodeles which
have a rudimentary lung or well-developed one not frequently
used in respiration possess no spiral valve. I find that it is
absent in Rhyacotriton (fig. 37) and also in Cryptobranchus
(fig. 38). According to Boas (%a), Necturus and Proteus
both lack this structure. On the other hand, all Amphibia
Figs. 35 to 39 The truncus of various urodeles, opened along the left side and
turned back to show the valves.
Fig. 35 Amblystoma maculatum (Shaw) .
Fig. 36 Amblystomn. opacum (Gravenhorst).
Fig. 37 Rhyacotriton olympicus (Gaige).
Fig. 38 Cryptobranchus alleganiensis (Daudin) .
Fig. 39 Plethodon glutinosus (Green).
The aortic arches are iiumbered according to the usually accepted system.
402 0. I(. NOBLE
having a fmictionally complete septum possess a spiral valve.

T liave found it pi-eseiit in Siren lacertina, Ampliiuma means,
Bmblysioma opacum, A. macnlatnm, Notophthalmus torosus,
a i d Triturus viridesceiis, besides all Salientia studied.
I t will be noted that tlie spiral valve in Amblystoma macu-
latum (fig. 3 5 ) is loiiger tliaii that of A. opacum, dthougli tlie
auricular septum of both are functionallp complete. The
lungs of tlie latter species are distiiictly shorter tliaii those
of the former. A. maculatum, A. opacum, and Rh~-acotritoii
illustrate tlirce stages ill the rctluction of tlie lungs. They
also represent three steps iii the reduction of tlie spirgl vdve.
Thie series mn11d suggest that a reduction of the spiral valve
accompanies luiig rednctioii and precedes the fenestration of
the auricular septum mliicli oiily occurs when the lmigs have
reached a certain degree of diminished usefulness in res-
pir a t'1011.
I shall not at this time attempt to coiisider the detailed
movements of the spiral valve. Small translucent spccimeiis
when injected with ink show under the binocular not only the
exact course of the arterial hloocl, 1)ut also the movemcnts
which divert the arterial blood away from the venous. There
can be 110 doubt that the spiral valve functions in the separa-
tion of the two blood streams. 'l'hc exact part p1a;ved by the
valve arid tlie part by the different rc+htances in the rcspec-
tive arches can be determined only by more exact methods
tliaii are available t o me a t this time. I have demonstrated
a mnch more complete separation of arterial and venous blood
tliaii Qaupp supposed. I have also shown that the presence
of the spiral valve may be taken as an indicator of such a
separation.
From the above observations Tve may conclude :
1.A spiral valve a i d a functionally complete auricular sep-
tum were characteristic of primitive' Amphibia.
2 . As tlie lungs of certain iirodeles became reduced, tlie
spiral valve decreased in length.
3. With further reduction of tlie lnngs the left auricle be-
came noticeably smaller, the auricular septum fenestrated,
and the spiral valve was lost.
THE ‘HAIRY FROG’ PROBLEN 403
4. Luiigless salamanders have no left auricle (except pos-

sibly a small part which has coalesced with the right auricle),
no auricular septum, and no spiral valve.
5. I n adult urodeles in which cutaneous or hraiichial res-
piration pretlominated, hut the lungs were retained, the
auricular septum degenerated without a reduction in size of
the left auricle. With the mixture of arterial and venous
blood witliin the auricles the spiral valve of tlie truncus clis-
appeared.
There is only :I single exception to these coiiclusions, and
it is possible to account for this in another way. A small
group of European newts (Triturus) are said t o lack the
spiral valve. I have examined the spiral ralve of two speci-
mens of one of these, Triturus cristatus, aiid find that Boas
(’82) is correct in stating that tlie spiral valve is ahsent.
However, the spiral valve is certainly not represented by
the row of accessory valves, as Boas suggests (’82, p. 493).
These accessory valves as well as a spiral valve are present in
the closely related Notophtlialmus torosus. As my figures
indicate, the spiral valve is one of the synangial valves greatly
elongated and has nothing to do with the accessory valves
or, better, knots of tissue found between spmngium and py-
langium, nor mrith similar structures found in dipnoans. The
synangial valves of ‘I’riturus cristatus are unique among
urodeles in that two of these are large and of the same size,
while one is small. It occurred to me that these large valves
might act in the way that a spiral valve is said to do by forcing
the arterial blood which enters the truncus last in the tlirec-
tion of the small valve. On the first part of the ventricular
systole the truncus would fill with blood and all three valves
be opened. I t should be noted that the small valve in the
truncus when normally bent lies directly opposite the open-
ings of the first arid sccond aortic arches. T o test out this
possibilit,y I injected one of my specimens with India ink
in the maiiiier indicated above. The ink was carried to the
first and second aortic arches exactly as in those species
which possess a spiral valve. We may, therefore, conclude
404 G . I<. NOBLE
that the synangial valves of Triturus cristatus function in the

same manner as the spiral valve, even though the structures
have a diff ereiit form.
We might expect from the above discussion that Salientia
with reduced lungs would show a degeneration of the spiral
valve. Such a change is not pronounced in either Astyloster-
nus, Ascaphus, or Batrachophrynus. Is it that in these forms
the reduction of the lungs has not proceeded far enough?
The spiral valve varies greatly in the different genera of
frogs and toads (Oliver, 'lo), and it is possible that some
such correlations between lung size and valve size m7ill be
found in these forms. This work to be accurate as to details
demands especially fixed material. Such is not available to
me at the present time. It would nevertheless seem highly
probable that if lungless frogs existed they would lack both
the left auricle, the auricular septum, and the spiral valve.
SUMMARY AND DISCUSSION
The hair-like growths on the sides of the body and part

of the thighs of the male ,4stylosternus robustus are found
only in that species and do not occur in other species of the
genus or in closely related genera. These structures have
been inadeqnatelv described by Gadow ( '00) , Phisalix ( '10,
'22), Kiikenthal ('12)' and Dean ( '12). Their chief pecu-
liarity is their enormous vascularity, the superficial capillaries
penetrating into the epidermis and forming a network di-
rectly beneath the stratum corneum. The 'laichpinseln'
theory suggested by Gadow and advanced by Dean to account
for these hair-like appendages cannot be accepted, f o r in no
amphibian in which the eggs are clxposed t o external media
is the parental tissue known to be modified to oxygenate the
eggs or larvae. The sensory-appendage theory developed
by Kiikenthal has little in its support, for the sense cells in
these appendages are no more numerous than in the integu-
ment of other Salientia. The poison-gland hypothesis of
Phisalix is also discarded because the poison glands are no
more numerous in the 'hairs' than in the adjacent integument.
I n all Amphibia other than Astylosternus the poison glands

increase in effectiveness by an enlargement of the glands or
by a multiplication in number per unit of integument. Phi-
Salk makes no attempt to explain why the integument of
Astylosternus should be produced into processes without
changes in the size o r number of tlie poison glands of these
appendages.
The vascularity of the epidermis of Astylosternus robustus
is directly correlated with the reduction of its lungs. Both
males and females exhibit a constriction of the posterior half
of the lungs, but in the male the narrow portion is encircled
by a thick sheath of connective tissue and muscles. The lung
capacity is possibly smaller in the male than in the female.
Females have the skin from the sides of the body highly
vasculated, the capillaries penetrating into the epidermis. I n
non-breeding adult males the epidermis on the sides of the
body and part of the thigh is thrown into a series of finger-
like processes, carrying with it a part of the corium lying
directly beneath. I n breeding males these processes are ex-
tended in length. This sexual difference in the development
and extension of the finger- or hair-like processes is directly
correlated with a difference in size, muscularity, and prob-
ably activity of the sexes. It may be readily assumed that
the breeding male has a greater need for gaseous exchange
than its smaller and less active female. This is further sug-
gested by the larger lungs in the male of other frogs (Boulen-
ger, ’97) ; the hair-like processes of A. robustus may be com-
pared with the loose folds of Cryptobranchus and Batra-
chophrynus microphthalmus, which are produced for the same
purpose and exhibit a similar penetration of capillaries into
the epidermis.
Lung reduction in Amphibia cannot be traced to a single
cause. I n the urodeles, species which live near but not in
mountain brooks and pass their larval life in the current,
almost invariably show a reduction, frequently a complete
loss, of the lungs. This may be due in part to the fact that
lungs acting as hydrostatic organs would be a hindrance to
406 (1. R. NOBLE
these larva2c (Tl'ilder and Dann). The coltlness of water and

its aeration permitting a grcatcr oxygen coiiterit would foster
cutaiieous respiratioii iii these forms. Further, the cool, damp
recesses near the water make suitable localities for cutaneous
respiration ill adult life. Species ~ - h i c hlive througliont life
in the stream retain their luiigs to a greater cxteiit, uiiless,
as in tlie case of Lenrognathus, they be derived from a lnng-
less form. Most lungless salamanders which live away from
the mountain-brook habitat 1ia.c.e been derived from species
which occnpicd that habitat. This does iiot applv to one
gains, Salamantlriiia, that was probably directly derived
from a pond-breeding species.
In the Salientia Imig reduction may be correlated with a
mouiitaiii-brooli habitat in the case of Ascaphus, but not in
Ratrachophrynus. As many frogs live near mountain streams
~vitlioutcxliihitirig a reduction of the lungs, it is more prob-
able that the temperature arid iiot tlie current factor mas
operative in the case of Ascaphus. Cold temperatures would
'
permit cutaneous respiration to suffice iii much the same way
as in frogs hibernating under tlie water. No correlation he-
t\t-eeii the lung reduction of A stylosternus robustus and ex-
ternal factors are knowii.
No matter how favorahle map have been the environment,
a reduction of tlie lungs in all Amphibia has brought with it
clianges in the integument which would increase the efficiency
of cutaiieous respiration. I n urodeles these integumentary
changes have been one of two types: either a penetration of
capillaries into the epidermis or the thinning of tlie mliole
epidermis over the superficial capillaries. In the Salientia
only the first of these two methods has been adopted.
Secoritlary clianges t o further increase the efficiency of cu-
taneous respiration in both urodelos and frogs have occurred.
These include the increase of the surface area by the forma-
tion of folds or filaments o r the increase of the number of
capillaries per unit of integument.
Two special methods of cutaiieons respiration deserve men-
tion, although neither are correlated with definite chaiiges in
the lungs. Ritter and Miller (’99) claimed that the digits of
certain terrestrial and semiarboreal salamanders were
equipped with subcutaneous sinuses which assisted materially
in the respiration of these forms. I have shown that similar
sinuses are present in all salamanders whether these are
aquatic or terrestrial forms o r whether the tips of the digits
are covered by a horny cap which would effectively hinder
respiration. Further, in the species which have the largest
sinuses the epidermis of the digits is considerably thicker
than that from other parts of the body. Ritter and Xiller
were therefore mistaken in calling these special centers of
respiration. On the other hand, arboreal frogs have the ven-
tral surfaces of abdomen and thighs covered by a pavement
of flat warts which apparently function by increasing the
friction of these surfaces during movements of the frogs.
The epidermis of these warts is penetrated by capillaries. It
is probable that such warts are especially effective in cutane-
ous respiration. Terrestrial frogs usually exhibit a few
papillae in the pubic arid femoral regions. Such papillae are
likewise penetrated by epidermal capillaries and apparently
aid in respiration. The surfaces of arboreal or terrestrial
frogs which are brought in frequent contact with the damp
substratum are therefore especially equipped for cutaneous
respiration. This does not apply to the feet, which would
be subject to greater stresses and strains.
Primitive Amphibia, both nrodeles and frogs, were en-
dowed with five methods of respiration: 1) pulmonary, 2)
cutaneous, 3) aquatic buccopharyngcal, 4) aerial bucco-
pharyngeal, and during larval life with, 5 ) branchial. At
metamorphosis the last method was lost. With the complete
loss of the first method the third method was also destroyed.
No primitive amphibian can live for a long period at normal
temperatures with one method alone, and most use all of the
first four methods. It is not surprising, therefore, that a
reduction of lungs should have brought about compensatory
changes in the integument to increase the efficiency of cu-
taneous respiration. Changes in the pharynx and oesoph-
408 G . Ii. NOBLE
agus have been described by previous workers, but these are

not marked (Kiinigstein, '03) ; at least, no striking differences
in the histology of this region in various salamanders have
been found.
With the reduction of the lungs and a diminution of the
oxygenated blood received from the pulmonary vein certain
definite changes have occurred in the heart and truncns. 1
have proved by means of micro-injections into the beating
heart that the arterial and venous blood streams are not
mixed in the heart of urodeles having well-developed and
fuiictional lungs. The fenestration which Langerhans ( '73)
figured are caused by faulty technique in preparation. I
have also shown the complete separation of arterial and ven-
ous blood in various Salientia, and hence can coilfirm the
conclusions of Ozorio de Almeida ( '23)' though reached in a
different way. The spiral valve insures a separation of the
two blood streams in the truncus, although this has been
denied on insufficient grounds by some, such as Pohlman ( '14)
and Brnner ( '00). The action of the spiral valve may be
watched in small translucent specimens during the injections
described above. A reduction of the spiral valve accom-
panies a reduction of the lungs. The spiral valve is lost in
all lungless forms, and it is difficult to understand how Bru-
ner ('00) could have described it as present. The spiral
valve is formed by the increase in length of one of the synan-
gial valves. Boas ('82) was wrong in homologizing the row
of knots found in the conus wall of Triton cristatus with an
incipient spiral valve. Such knots as well as a spiral valve
are found side by side in the more primitive Notophthalmus
torosus. It follows that the comparisons which Boas ('82)
made between dipnoans and urodeles does not rest on a sound
basis.
With a reduction in size of the lungs the left auricle de-
creases in size. Tt is possibly lost entirely in lungless forms,
although this would be more or less a matter of definition.
With the reduction of the left auricle the auricular septum
becomes greatly fenestrated, allowing a mixture of arterial
and venous blood within the auricles. Bruner (’00) claims

that in the lungless forms the sinus-auricular valve has
shifted to the left wall of the now confluent auricles. It might
be readily assumed that the left mall shifted to the position
of the sinus-auricular valve on the complete reduction of
the left auricle.
In urodeles in which the lungs are not reduced but are not
frequently used in respiration, the left auricle is not reduced
in size, but the auricular septum becomes greatly fenestrated.
I n correlation with this mixing of arterial and venous blood
the spiral valve has disappeared. We have established a
definite correlation between the distinctness of arterial and
venous streams, the functional completeness of the auricular
septum and the occurrence of a spiral valve. If one of these
features is lacking the other two cannot be present. These
correlations seem to hold for all urodeles which have been
studied. It would be interesting to know if they did not apply
to the only large group which has not been examined, the
Hynobiidae.
I n none of the Salientia have the lungs become reduced to
under 7 mm. in length when distended. In none has the
spiral valve been lost nor the auricular septum perforated.
Some forms as A stylosternus robustus and Batrachophrynus
microphthalmus must hare a very extensive cutaneous res-
piration, but both have more vasculated lungs than Ascaphus,
the only species of reduced lung capacity available to me in
the living state. I n Ascaphus the left auricle is reduced, but
the auricular septum is complete. We may therefore assume
that in all Salientia, no matter how extensive the cutaneous
respiration may be, the reduction of the lungs has not pro-
ceeded so f a r as to produce those cardiac modifications which
we have seen in urodeles of greatly reduced lung capacity.
The correlations which we have found between the environ-
ment, the lung capacity, the modifications of the integument
to facilitate cutaneous respiration, the reduction of the spiral
valve, the diminution of the left auricle, and the fenestration
of the auricular septum, apply to all Amphibia. Some cor-
410 G. 1<. KOULE
relatioils such as that tlemandiiig a modification of the integu-

meiit 011 the reduction of the lungs o r the loss of the spiral
valve oil the fciiestratioii of the auricular septum are much
more coiistaiit than those between hahitat aiid lung reiiuction.
'J'liis suggests that lung reduction may be coiiditioned by sev-
eral factors, hut that any factor causing a fenestration of
the aui*icular septum would automatically bring about a re-
clnctioii of the spiral valve.
CONCLURJO?\'S
1. The hair-like appendages of A stylosternus robustus are

respiratory filaments produced by exteiisioiis of a highly
vasculated epidermis arid a part of tlie dermal tissue lying
directly beneath it.
2. The vascularization of the epidermis of A . robustus is
conditioned by a reductioii of the luiigs in both sexes, the
production of the filaments in the male, by the greater vas
cnlarity, size, a i d , probably, activity of this sex.
3. All Ampliibia which undergo a reductioii of the lungs,
110 matter what the eiivivonmental coiiditions may be, either
oxliibit a peiietration of their superficial capillaries into the
epidermis or the epidermis is greatly tliiiiiied over the super-
ficial capillarics, thus iiisuriiig greater efficiency of the cu-
taneous respiration.
4.Arboreal frogs with large lungs have the ventral surfaces
of their thighs a i d ahdomeiis covered with a pavement of
tubercles wliich possess a vasculated epidermis similar in
most respects to the vasculated epidermis of the female Asty-
losteriius. I t is assumed that these regions are special cen-
ters of cutaneous respiration. A much more restricted
vasculated regioii is found 011 the ventral surfaces of terres-
trial frogs aiid none on aquatic or fossorial frogs having
large Iuiigs.
5. The blood siiiuses fouiid at the eiids of the digits in
Aneides aiid Plethotloii are found more or less developed in
all urodeles. They do not serve as special centers of res-
piratory activity.
6. The causes of lung reduction in Amphiloia are complex;

the factors correlated with lung reduction in one group do
not maintain in another. The chief factors seem t o have
been swift and highly aerated w-ater during larval life, cold
temperatures throughout life, and damp, dark retreats during
adult life.
7. A reduction of the lungs in all Amphibia is correlated
with a reduction of the left auricle.
8. An extensive reduction of the lungs such as that found
only in urodeles leads to a fenestration of the auricular
septum and a loss of the spiral valve.
9. A disuse, or only occasional use, of the lungs in respira-
tion conditions it fenestration of the auricular septum with-
out the reduction in size of the left auricle, but with a com-
plete loss of the spiral valve.
10. The spiral ralve is formed by a backward growth of
one of the syiiaiigial valves and has no relation to the knots
of tissue found in the conus of the specialized Triturus
cristatus.
11. All Amphibia having well-developed and frequently
used lungs possess a fiinctionally complete auricular septum
and a spiral valve. I n these forms injections of small quan-
tities of India ink into the pulmonary vein of the beating heart
has demonstrated a complete separation of arterial and ven-
ous blood. No ink was ever distributed to other than the
first and second aortic arches.
12. All Amphibia liaring a fenestrated auricular septum
lack the spiral valve and the ink injected into the pulmonary
vein was divided at random ampng the aortic arches.
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T H E INTEGUMENTARY, PULMONARY, AND CAR-

DIAC ilIODIFICATIONS CORRELATED WITH

growth has excited the curiosity of biologists since the first

have, of course, no structural similarity with the hair of

mammals, but the name has nevertheless remained in gen-

concluded that they appeared “only in the males during the

are usually purely epidermal in character. The two peculiari-

back. It arises in all species from a very limited region on

’10, p. 347), “to differentiate clearly all the details of struc-

the skin itself thrown into prolongations of any sort-either

‘hairs’ of several of these formol specimens. One series of

A.V.VaZ., auricular-ventricular valve L u . , liver

Fig. 1 Astylosternus robustus (Boulenger).

shown the appearance of one of the most dorsal hairs from

Iiitegument of the ‘ hairy frog,’ Astylosternus robustus (Boulenger).

Cutaneous glands are numerous in the ‘hairs,’ but it will

Fig. 6 Dissection of the viscera of Astylosternus robustus (Boulenger), show-

They are directly comparable to tlie pardoid glands of thc

Fig. 7 Tangential section of one of the l i n i ~ vof Astylosternus robustus (Bon-

sides of it. Kiikenthal’s homology of the hair-like append-

lated area. Is not, then, the function of the ‘hairs’ asso-

tion of the eggs. The breeding habits of A. robustus are

unique among frogs in being formed of a short sacculated

“that the lungs of the female . . . . could be blown up by

should develop in these unrelated groups. The physiological

THE MODIFICATIONS O F THE EPIDERMIS WHICH INCREASE THE

Tlie question has been raised in the preceding discussion

figures of the lateral epidermis of this species comparc favor-

The Cryptohranchidae liave evolved directly from the

Figs. 10 to 12 Sections of the integument, from tlir flanks of various Amphibia,

that they form veritable gills. This analogy is brought out

dermis and superficial capillaries of Cryptobranehus (Phi-

Fig. 11 Adult female Cryptobranchus allegsriiensis (Daudin). X 261.8.

such well-known aquatic forms as the newt? It is probably

SOVRAAL Or MORPHOLOOY A N D PHkSIOLO(+I, \Old. 40, LO. 2

respiration in Cryptobranchus than in Triturus viridescens.

determined by a study of living specimens that there is both

integument of the first and last of these groups is unknown

apparent that within a closely related group of species we may

Figs. 13 to 15 Sections of the integument from the flanks of various urodeles,

period of greatest activity in pools of clear, slow-moving

Fig. 15 Bhyacotriton olympicus (Gaige). X 322.4.

has shown that they are functional. a s if in correlation with

The Salamandridae apparently gave rise to the Amphiu-

M7hipple ( '06) showed that Desmognathus and Pseudotriton

apparently been directly evolved from Desmognathus quadra-

Pigs. 16 to 19 Sections oP thc integuincnt f t o m t h r fhnks of various Plctho-

very slightly into their overlying tissues before they reach a

within the Amphibia. We have tried to hold ourselves to

Fig. 17 Stereocliilus niargiiintus (Hallowell). X 245.4.

degree of capillary penetration or of epidermal thinning and

The superficial capillaries between two costal grooves of various urodeles.

20 and 21), it will be seen how the capillary number in the

method can demonstrate only correlations, not causes. The

We come, at last, to the Salientia, and here at the outset

under the water. hscaphus remains, in fact, for considerable

surface area has been obtained by the formation of loose folds

tion of ventral tubercles with arboreal life is very close.

In Saiito Doming0 there is another tree-frog, Hyla domini-

Figs. 2 5 to 29 A coinpiirisoil of thc vaseularizatiori of the integument of the

tration was slight. The number of layers of cells in the

If the abdominal and femoral tubercles of Salientia serve

toes, in fact, may be considered to have assumed in a measure