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=Chapter III The Alimentary Canal=
=Chapter III The Alimentary Canal=
CHAP'l_‘l+3R III
THE ALIMENTARY CANAL
THE alimentary canal or enteron‘ of the V crtebratc consists of a
tube passing from the mouth to the anus. The wall of this tube is
known technically as the splanchnopleure in contradistinction to
the somatopleure or body-wall (Ballour). It consists of an inner
lining epithelium, the endodcrm, cnsheathcd in a complex coating
of mesoderm——the splanchnic mesodern1———consisting of connective
tissue, blood-vessels, lymphatics, nerves, and coelomic or peritoneal
epithelium.
As is commonly the case in other metazoa the cndodermal
lining is in the Vertebrate more or less encroached upon at’ the
oral and anal ends of the tube by the spreading inwards of
ectoderm. The parts of the tube which come thus to be lined with
ectoderm are known as stomodaeum and proctodaeum (L-ankester,
1876) while the intervening region lined by cndoderm is known as
the mesenteron. In the Vertebrata there is very slight develop-
ment of proctodaeum but an important section of the buccal cavity
is, as will be seen later, stomodaeal in its nature.
It is also customary in embryological writings to use the some-
what loose expression foregut for the anterior portion of the
alimentary canal (reaching back to the pylorus or to the opening
of the bile-duct), which in the meroblastic vertebrates becomes
differentiated oil‘ from the yolk-sac comparatively early in de-
velopment. . _ .
A good idea of the blocking out 01 the main regions of the
alimentary canal in one of the lower vertebrates is got by inspecting
sagittal sections of embryos and larvae at different stages of develop-
ment such as those shown in Fig. 80. From the gastrula stage (A) on
to the stage illustrated in Fig. 80, C, the endoderm forms a simple
sac with its opening posterior (anus) and with its ventral wall
greatly thickened owing to the fact that its cells contain the
main store of yolk. From the stage of Fig. 80, D onwards the
foregut (f.g) becomes gradually constricted oil‘ in a tailward
direction from the mass of yolk, while at the opposite end of the
body, correlated with the outgrowth of the posterior trunk region of
the embryo and the backward shifting of the anus, the yolky mass
144
152 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.
Wards of the communication between olfactory and buccal cavities,
a process which reachesits extreme in the Crocodilia where the palate
extends back to about the level of the glottis.
STOMODAEAI. GLANDS.———Whereas in the majority of Fislies the
stomodaeal lining possesses only isolated gland-cells, in the air-
breathers on the other hand there are developed definite multicellular
glands. These originate as a rule from solid down—growths of the
F10. 85.-View of the roof of the mouth in three species of Lizard (A, 19'_(/«ernw Ifingjivf ;
B, Mabuia. qmfnqmflaemfata; U, Lygosonm. ‘l“ll.f(.’.S'('(’I'l.S‘), illustrating the shifting back of
the communication between nose and month. (_ After Voeltzkow. 1899.)
rh, recess into which primitive posterior nan-s open ; pal, palatim.-. ; pt, pterygoid ;
tr, transverse hone; no, vomer.
lining epithelium which develop a cavity secondarily. In Urodeles
there is, as already mentioned, a special aggregation of these glands
forming the gland-field in front of the tongue, while a single gland of
considerable size develops from the roof of the mouth in the region
between the olfactory sacs (lnterniaxillary or internasal gland).
In terrestrial Reptiles glands are present in numbers on ‘the roof
of the mouth (Palatine), beneath the tongue on each side of the
middle line (Sublingual) and along the edge of the month just
external to the row of teeth -(Labial). The poison glands are
specialized and enlarged labial glands of the upper jaw except in
146 EMBRYOLOGY 014‘ THE LO\V'ER VI|+}l't'l.‘EBRA’l.‘el'<}S (“.11.
case with I’roto1;le'2--u..s:, the huccal roof‘ in froiit, that is to say in the
neighbourhood of the mesial plane, 1)&Lb'SGH without interi-upticm into
the external skin: in other wo_rds the maxillary ridge is not con-
tinued to the mesial plane so as to meet its fellow. In later stages
I~‘1o. 80.——Sagitt9.1 sections through P()l;/p/.(:.-e:l.s‘.
A. 3t9-L'.0 14.: 13. St--".‘-W W: C. Stage 20: 0, stage 2: ; E, stage-24 +. (1., mos; m-, :ll.1'llI--llt.I'l‘()Il ; e-ml,
"-l1‘l"J"1<‘J‘||l1 "71’: ‘‘“l'‘'''_‘(‘- W‘ ll"-.\' 3 f-’’- ‘‘”\'“.V H!‘ forvln-uin: f.!7. fun-gut: N. uo1..nclmr(l 2 2).,/I. l""i"“"‘.V "*1"
(If hruin ll-mr; pin, pnneul rmlivm-n1"; .-_:_-, ¢-;u-i1_\' of spinal cum"! ; 3/, yolk,
the roof of the mouth would be hidden in a view from the ventra
side owing to the forward growth of the lower jaw. '
The anterior portion of the buccal cavity in Urodele A11l1)l'1il)ifl.l1S
arises in a manner essentially similar to that descrihed above.
In the G-ymnophiona and the Amniota a characteristic 1'nodifi.ca-
tion of the mouth margin is‘ brought ahout hy the fact that, as
III BUCCAL CAVITY 147
already mentioned, the maxillary ridge is cut across by the olfactory
groove and so divided into the outer maxillary process and the
inner median nasal process, the latter of which is continuous with
its fellow across the mesial plane, forming with it the so-called
fronto-nasal process (see Chap. X.).
Fm. 8OA.~-—eS:t;;'lll:I.l Ht'('-ll()IlH txhroligh .I‘u/_:/}af:‘:'u.s".
1.‘, _\.1_ug., 3.3; G‘ smge -39; H, St:l‘L‘D‘[| :;-_>_ n, anus; u_«-, :ll|l.f‘l'l0l‘ (-onnnissllrn; 4-lo, optic cliiusrnu:
l clones.‘ ml enlmic c:l\'it.- : 1-]. heart : hm. halu-nnlar u-onnnissui'e: l1'., li\'<'l': m.r. m:m«lil.ul:u* r-i«lgo- ,
. . , Y _ _ _
2,, pjt;ujt;n~y -;m-ulutimi ; pm, [_'M)h‘l.('l'lH1‘('l)]]1l|)iSfil|1‘!'; ,.n._:7, pH.~4l..'{ll:ll _-.;ut.: yum, pzuu-I-o-:it'Ir rudiment‘; /"rm.
pineal rudiim-.nt.; 5’, .<t«mi:u:ln : y, yolk.
It is of interest to notice that in various Vertebrates the buccal
opening is at first elongated in an antero-posterior direction instead
of from side to side. Such is the case with Scylliuqn (Sedgwick,
see Fig. 81) and ’1'o'rpedo amongst Elasinobranchs. In these cases
the slit-like mouth is bounded on each side by a longitudinal ridge.
148 EMBRYOLOGY or rm: LOWER VERTEBRATES (:11.
Later on each ridge becomes sharply bent, about the middle of its
length, in such a way as to give the buccal opening a rhomboidal
shape and at the same time to mark oil’ the ridge into a maxillary
portion in front and a mandibular portion behind. In Anura a
somewhat similar arrangement is found.
“ENnonEuMAL” SECTION or BUCCAL CAvrrv.-—'l"‘he fully
developed buecal ea.vity has incorporated in it a posterior portion-
varying in relative extent in dil'l'erent Vertebrates—which is de-
rived not from the ectoderm but from the anterior portion of the
“endodermal” enteric rudiment. The simplest way in- which this
portion becomes added to the anterior portion is seen in those
Vertebrates in which the anterior part of the cnteric cavity is patent
throughout develop-
ment. In this case
the velar membrane
simply r u ptures——-its
reinnants soon be-
coming absorbed--
and the stomodaeal
cavity is thrown into
open communication
with ‘ the cnteric
cavity. This is the
case in certain
Anura (Rana) and
in Amniota.
Fm. 8l.—--Ventral \'lt‘\\‘ of head region of embryos of Sag‘:/lliu-nz
¢-mu}-u/u. (After Sedgwick, 1892.)
A, 7—8 mm. ; 13, Sll_L','l)ll_\-' more :ulv:uu-ed than .\ ; C, H -12 mm. ;
I), '16 mm.
brat-es no velar mem-
brane is present, owing to the fact that the foregut either becomes
solid for a time (Pol;/pteru.s, Fig. 80, D—Gr) or is so at the beginning
(Teleostei, Urodela, Lepirlosvlren and Protopterus). In such cases the
peripheral layer of the yolky foregut rudiment gradually assumes
an epithelial character and the yolk along its middle breaks down,
so that a cavity arises—continuous with the stomodaeal cavity and
forming the hinder section of the definitive buccal cavity. The pro-
portion which this posterior portion bears to tlfe anterior section
derived directly from the outer surface is very different in different
groups. It apparently attains its maximum" in Teleosts where
-it forms practically the whole of the. buecal cavity.
' Points of critical importance to the germ—1ayer theory are raised
in this connexion by the fact that teeth, organs belonging originally to
the outer surface, are developed in this posterior region of the buccal
cavity from yolky “ endederm.” This is well seen in a Urodele, ‘or
a lung-fish such as Lepidomlren or Protopterus (Fig. 82). The attempt
is made to get round this difficulty by assuming that the layer of
epithelium which makes its appearance over the surface of the buecal
rudiment, and in relation with which the teeth develop, is really
an ingrowth from the ectoderm.
In many V erte- T
III BUCCAL CAVITY 149
It is, as a. matter of fact, quite continuous with the ectoderm,
FIG. 8‘2.—Sagittal section tl1rou;;l1 lu-.:ul I't’gi0Il of a Protopturus larva (Stage 33).
Inc, buccul ts-uvit-y: h.I, :ml<-riur l_u_nn1<l:u‘_\' of tongue; N, nulm-lnm‘41: pin, pine":-al lmtly: /W-I‘.
pm-uphysi.-.: l’iI., pit: 5t.:u-_y bc«l_\': Th, tllymitl ruuliment; Lu, H.-rtum «-ptimluv. Th.-. p()sil.inn nr dvlllul
rudiments is in<li<-.atml by Hue hm upwzu-d pr(r_ic:(:l.i()nS of the dOI".~m| wall of the buccal cavity.
but exaniinution of carefully prepared celloidin sections (Fig. 83)
shows that at its inner end the epithelium passes by imperceptible
A 8
FIG. 83.—Sagittal N'(_‘llHllH t.h1'ough the 1'egi<_n1 of the lulucul cavity of (A) Lcpi¢.io.s£'rc1t,
stage 30, and (B) .lmI:[.;/.s-Iowa, 7'5 mm. in i(‘ll§'.'_,'iiI.
b.c, bu(‘c::l opitllvlilllll ; 4'-cl, l‘L'tmlBl.'lll : _I/, .s'(_)litl Illziss of yolk-(.'I-ll.~: in pu.\'itiun 01' i.|ll(.‘('2tl vzivity.
gradations into the ordinary yolky endoderm, with no trace of the
sharply defined edge which it would possess were it a 1uyer__of
150 EMBRYOIJOGY OF THE LOWER VERTEBRATES CH.
ectoclerm pushing its way inwards. It extends inwards simply by
a process of delamination from the yolky “ endoderm.”
The real lesson to be learnt from these cases is that the
charactcrs of one gcrm—layer are liable to spread over its boundary
into l3C.5]‘l‘ll'.()Ty belonging to another layer or, in other words, that
the territories of the various layers are liable to be separated by an
indefinite debatable zone rather than by a mathematically sharp
li.ne. It follows that the apparent position of an organ-rudiment
in relation to such a boundary is not necessarily to be taken as
Fm. 84. —-Sagittal sections illustrating the development of the tongue in l_.l1'm_lclc..~'.
.\ and I5, Triton; C, Sula.-armndra (after Kallius, luol); _«_/.1‘, gland tie1d;__M, mandibular arch ;
7».I, priuuu-y t.ongLu.-.
giving any definitive proof as to which of the two cell-layers that
organ belongs to.
Tim 'I"<mcUE.——The tongue is a portion of the buccal floor which
becomes demarcated off from the rest by a split formed by a down-
growth of the lining epithelium of the mouth. is mode of develop-
ment is well illustrated by what happens in Urodele Amphibians_as
described by Kallius. Here tlwru develops first a primary tongue,
ensheathing the anterior and ventral portion of the hyoid arch
(Fig. 84, pt), which becomes marked off, except at its hinder end, by
a deep groove in the floor of the mouth.
A liorseslioasliaped thickening of the buccal epithelium now
III BUCCAL CAVITY 151
develops external to, and parallel with, the groove bounding the
primary tongue, and consequently lying on the floor of the month
between the primary tongue and the lower jaw. The thyroid
involution is situated between this thickening and the tip of the
tongue.
The ectodermal thickening develops numerous glands, each
originating as a solid ectodermal down-growth, and is known as the
gland-field. Externally it is bounded by a shallow groove. Later
on the cleft or groove separating the gland-field from the primary
tongue becomes obliterated by fusion ol‘_its walls, and the gland-field
becomes raised up in a dorsal direction (Fig. 84, B) the tongue-tip
shrinking backwards so that eventually the demarcation between
primary tongue and gland-field disappears (Fig. 84, 0). Meanwhile
the groove bounding the gland-field externally becomes deepened.
It forms the outer limit of the definitive tongue which is thus a
compound structure, its tip and edges developed from the original
gland—field, its postero-median part from the primary tongue.
In the fishes the tongue remains non-muscular and non-glandular:
it is simply the primary tongue. In the Axolotl the tongue appears
also to be a primary tongue, the gland-field making a transient
appearance as a rudiment but eventually undergoing atrophy
(Kallius).
In the Amniota the tongue is, as in the terrestrial Urodeles, a
compound structure, the primary tongue rudiment becoming fused
with an elevation of the floor of the mouth lying in front of the
Thyroid rudiment. This elevation, called by His the tuberculum
impar, represents morphologically the gland-field of the Urodeles.
The tongue of Cyclostomes is remarkable for its complexity: it
has complex muscular and skeletal arrangements and on its surface
it develops the horny spines which function as teeth and simulate
teeth in their appearance. In Bdellostoma. the tongue develops as a
cushion-like swelling of the floor of the mouth at an early period
while the velar membrane is still intact. In J’et9°0m_2/zen, on the
other hand, it does not develop until the time of metamorphosis.
It has already been shown how the olfactory organs come to
communicate with the buccal cavity by the posterior nares. In the
Amniota these become sunk into a recess in the roof of the mouth
and in the higher Reptiles, as in the Mammals, this recess becomes
shut off from the buceal cavity by a horizontal shelf which grows in
from the side and meets its fellow to form the palate. How this has
come about in evolution is illustrated by the three Lizards shown
in Fig. 85.
In ontogeny the mode of origin may be similar,’ the palatine out-
growths meeting and fusing with one another in the middle line
(Crocodiles) or, as happens more usually, a median ridge or--septum
extends backwards from between the primitive posterior nares: and
the palatine processes meet and fuse with its ventral edge. In the
two cases the physiological result is the same—-the shunting back-
170 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.
twists upon itself, in such a way that points upon its ventral surface
would move towards the embryo’s right side. (In other words the
lung-rudiment rotates about its long axis in a counter-clockwise
direction as seen from behind, its front end remaining fixed.) The
two lobes are the right and the left lung-rudiment but on account of
the rotation just mentioned which extends through more than 180°
the left lobe at this stage represents what was originally the right
side of the rudiment.
The two lungs of Lepiclcisiren or Prrotoptems are thus reversed in
A 5 C D
Fm. 96.-—-Dissections of mid-gut of L8})?:d()8t’I‘8‘?2- at stages 32 (A), 35 (B), 36 (C), and
37 (D), showing the modelling of the intestine and also the later stages in the
development of the lungs. Seen from the dorsal side. ~
c.c, eloaeal caecum ; int, intestine; (.1, left lung; (Ii, liver; mun.d, Wolfllan duct; pan, pancreas ;
ph, pharynx; r.(, right lung; sp, spleen.
position-—-the right lung of these forms being homologous with the
left of other Vertebrates. An important detail is that in early stages
the original right lung, '£.e. the definitive left, is decidedly larger than
its fellow (Fig. 95, B). In later stages this inequality disappears, the
smaller lung overtaking, the other in its growth (Fig. 96). .
In the ease of most individuals the lungs assume their dorsal
position simply by growing directly tailwards, the oesophagus being
pushed out of the way towards the left side (Graham Kerr, 1910).
In certain specimens however, which doubtless in this respect retain
I11 PH ARYN X 153
Ifeloderma. where they are the enormously enlarged sublingual
glands.
Similar localized developments of the buccal glands occur in
Birds and some of them may reach a great size as, for example, the
enormous sublingual glands of the Woodpeckers.
PIIAI’.YN.\'.-—-The part of the alimentary canal which follows
immediately behind the lmccal cavity is highly characteristic from
the fact that in Vertebrates it is concerned with the function of
breathing. The special organs which are developed to carry out this
respiratory function fall into two groups one represented by the
Lung‘——adapted for respiratory exchange with the atmosphere, the
other by the Gills~—-adapted for respiratory exchange with gases
in solution in the water. As the balance of probability is in
favour of the latter being the more archaic they will here be
considered first. .
The gills are seen in their most typical and familiar form in the
various groups of Fishes where there is present upon each side of the
pharyngeal region a series of visceral clefts—-slit-like openings lead-
ing from the pharyngeal cavity to the extei-ior—-—separated from one
another by masses of solid tissue known as the visceral arches or
gill septa. The walls of the clefts are highly vascular and their
surface is commonly raised into conspicuous plate-like projections-
the respiratory lamellae —which serve to increase the area of
respiratory tissue.
In the most archaic arrangement, seen in Elasmobranch fishes,
the front lip of each cleft, except the first, is prolonged backwards to
form a small valvular flap overlapping the external opening. In the
Holocephali, Teleostonii, and Dipnoi the anterior one of these flaps,
that projecting back from the hyoid arch, becomes greatly enlarged
to form the operculum which overlaps not merely one but the whole
series of clefts lying behind it. Correlated with this the outer
portion of each succeeding septum, which in the Elasmobranch gave
origin to its valvular flap, has disappeared, leaving only the portion
lying next the pharyngeal cavity.
The cleft lying in front of the hyoid arch—-the spiracle is usually
modified, its respiratory tissue having been reduced and even its
opening being diminished in size or completely absent, but its general
relations in the adult are such as to permit of no doubt as to its
serial homology with the clefts behind it.
Most usually there are on each side six clel'ts——a spiracle and five
branchial clefts~ —but there is reason to believe that there was a
greater number present in primitive Vertebrates——seeing that the
number of persistent clefts becomes on the whole less as one ascends
the vertebrate scale and that here and there among the more archaic
forms a greater number than the usual is found (Bdellostoma, up to 14,
Notidanus cinereus 7, N. griseus 6).
In a few of the more archaic Vertebrates there develop during
larval life, in addition to the visceral clefts with their respiratory
154 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.
lamellae or internal gills, respiratory organs of another type——-—the
external gills. As there is some reason to believe that these are more
ancient organs than the gill-clefts they will here be considered first
although they are much less familiar than the clefts with their internal
gills. The branchial organs will therefore be considered in the follow-
ing order: (1.) External gills, (II.) Visceral clefts, (III.) Internal gills.
(L) Ex'1‘1«3RNAL GI[.I.S.—~Tl1e true external gills are organs which
are commonly confounded with the ordinary or internal gills developed
in the walls of the gill-clefts. They appear however to be quite in-
dependent of these in their origin and they would probably have
attracted more attention and interest than they have done had it not
been for the fact that they occur in their typical form in only three
subdivisions of the Vertebrates (Crossopterygii, Dipnoi, Amphibia)
and that two out of these three groups comprise animals of extreme
rarity, the developmental
mz_]V stages of which have not
been generally accessible
to emhryologists.
9-9-17 The typical External
“C a W gill is a projection from
' ' the surface of the body
- on the outer side of a
visc.eral arch. It con-
sists of a core of mesen-
chyme with a covering
Flu. 86.—-Diagrammatic longitudinal section through the (,f ectodenn; it is LI-a_
early rudiments of the external gills of Lepidosircn
(Stage 25). versed by a vascular loop
e.g, external 1.',lll; end, endoderm; ma, \lHCel-‘ll arch; consistlng of ,the nlaln
m-, visceral cleft rudnm-nt. aortic avrcll Whlch P333353
out to its tip and then
doubles back; and it commonly has a pinnate form, paired projections
growing out so as to increase its respiratory surface. It is provided
with muscles by means of which the possessor is able to flick it
sharply backwards so as to renew the water in contact with it.
The external gill as a rule is without any special skeletal support
but in the larval Polypterus a short rod of cartilage projects into its
base, and in the extinct Dolichosoma of the Gas coal of Bohemia there
was apparently present a well-developed segmented skeleton within
the substance of the external gills.
The external gill develops as an outgrowth from the tissue of the
visceral arch at a period at which the clefts are not yet perforated.
It arises as a bulging of the surface (Fig. 86) and in the author’s
opinion the endoderm of the cleft rudiments takes no part in.its
formation. At the same time it is only right to state that the pre-
valent opinion in the past has been different. The outer surface of
the visceral arch in the region where the external gill will develop is
covered by a layer of cells thicker than the neighbouring ectoderm,
and in some cases this thickened portion of the ectoderm shows in its
e.g.I
There is however no definite evi-
III EXTERNAL GILLS 155
deeper portions a rich deposit of yolk, so as to look exactly like the
yolk-laden encloderm. Grcil explains this appearance by supposing
that true endoderm cells actually
spread outwards and replace the
deep layer of the ectoderm, so that
the external gill-rudiment would be
partly endodermal in its nature.
dence of any such process taking
place and the present writer would
interpret the appearances as mean~
ing simply that the ectoderm cover-
ing the external gill-rudiment
becomes thickened, and stores up
a supply 01' yolk‘ in its deeper layers,
as a physiological preparation for
the active processes of growth which
are about to take place as the
external gill rapidly increases in
length. In this he agrees with
Marcus (1908).
The general appearance of the
developing external gills is well
seen in Hypogcopms (Fig. 87) or
in Lepidoswlren (Fig. 200). In
Lepvlolosiren there are present four B‘.1<_:, 37.---Hypogeophis eIul)i'y0s showing
upon each side of the body. At ‘l3’,°1?1§“°“t_ ‘if89}}‘“ “"“""““l gm“-
first the four are quite independent ( W m“’_ ") _
of one another but as development .,.;-;;ii;...;.;‘l:;1i:,l.‘.‘,‘.. ""‘«i~§.. ’.’.;...§i?{Z.‘{‘ ..“.f.§1‘,‘..‘ ...if.’£;
g0(-3S 011 they b£‘.COII18 raised UPOII EL projecting in Bfi-mu the hyoid 8.I‘(‘ll, and also
conlu-1011 base SO as to give the from the mandibular arch in front of it, are
__ . _ . p0ssil)l_\' u-xiurnal gill rudiments which do not
3:PP93—T3'l1(39 of 3' 3111819 Organ wlth go on with their development.
four branches (Fig. 200, B-E).
The distribution of true external gills amongst the main groups
of Vertebrates is shown in the following table:
1
,—-.-—-q-——.._.—_.__—j__..._ . __ - .. .- ._  . ...--..- -.
\
l 3
V  I. II. III. I\'. ‘V. ‘ ' VI.” '
iscvral .\l'L'lI. ' _ . . . l-‘irsl ' .\'.4-Hnltl 'l‘ llI'( u Four‘:
M‘l'"1lb“l‘w‘l Hymd‘ Jlr:1m-hi:ll. Iii‘.-lnuliinl. 3 Bram-hinl. 3 ll:'.'ui(.-lii:Il.g
Elasmobranchii. . ;
Crossopterygii . . 5 x .
lhpnoi. . . . g x x x x
Amphibia . . . - 'v.*" 2:. x y x x
i Amniota . . ' i
4 I 1
* r:..\'o'sLi_~,'iul.
In those animals in which they are well clovoloped the external
gills are for a time the main functional breathing organs. They are
156 EMBRYOL()GY OF THE LOWER VERTEBRATES CH.
richly vascular and the renewal of the water in contact with their
surface is provided for by a well-developed muscular mechanism by
which they are sharply flicked from time to time, or, in early stages,
by rich ciliation ol"tl1eir surface as in the Frog (Assheton, 1896) or
6'73:/ptolzramz/ms (Smith, 1912). They are as a rule merely temporary
organs. As the respiratory function comes to be sufficiently per-
formed by other organs their circulation becomes sluggish, their
tissues moribund. They become invaded by leucocytcs and eventually
unclergo complete atrophy. in .l’o~otopm~us distinct vestiges persist
for a prolonged period while in various Urodeles they remain func-
tional throughout life.
The external gills, highly vascular and projecting freely into the
surrounding medimn, present tempting objects for attack by other
organisms. They are therefore extremely liable to injury, and cor-
related with this they present a high power of regeneration. in
correlation also with the same fact we find that they tend to be
eliminated from development in certain members of groups which are
as a whole characterized by their presence. Such is the ease in the
Amphibia where they are characteristic of the group in general but
where in particular cases they are reduced (II;z/la n;'rb0'rea) or com-
pletely absent (}>’ovmb'mator) although we must believe they were
present in the ancestors of these forms.
This tendency for the external gills to become eliminated from
development in the process of evolution raises the interesting morpho-
logical question: were External Gills at any period more widely dis-
tributed amongst Vertebrates than they are at present? And, if so,
are their vestigial representatives still to be found in any cases where
they no longer develop as functional respiratory organs?
This interesting problem, which offers an inviting field for research,
has not yet had sufficient attention devoted to it. Even if it were the
case that external gills once existed in the ancestors of forms in
which they are no longer present as functional organs there is always
the possibility if not probability that their disappearancehas been so
complete as to leave no observable trace. Nevertheless such vestiges
might persist and are worth looking for.
Under these circumstances it is of interest to note that already
certain structures are known which are interpretable as vestiges of
once-present external gills. Thus in Gymnophiona what appear to
be transient rudiments of mandibular and hyoidean external gills
make their appearance during development (Fig. 87, B). Again in
the case of the Mandibular and Hyoid arches of Urodeles, on which
no functional external gills develop, Driiner (1901) has found what
appear to be vestiges of the muscles of external gills. Again in
the larvae of various Urodeles there occurs in connexion with
each mandibular arch a curious styliform projection known as the
balancer, from the fact that the larva balances itself upon them as
upon a pair of limbs (Fig. 88, b). Each of these has a vascular loop
within it and it in fact appears to be the modified external gill of
III . EXTERNAL G-ILLS 157
the mandilmlar arch which has lost its respiratory and taken on a
supporting function.
While external gills occur within three main subdivisions of the
Vertebrates, namely Teleostomatous fishes (Crossopterygians——the
most a.rchaic of existing Teleostomes), Lung-fishes, and Amphibians,
there are two main groups-—Elas1nohranchs and Amniotes---in which
they are conspicuous by their absence. Having regard to the
tendency of the organs in question to disappear (as in the cases
already alluded to amongst the Amphibia) their absence in a
special group would not
in any case constitute
strong evidence that they
were never present in
the ancestors of that
group. As it happens
however there is in the
two groups mentioned
a definite cause which
seems quite competent
to account for the dis-
appearance of external
gills, namely the de-
velopment of'_ a new
organ —— the yolk - sac
with its highly developed
vitelline network of
blood-vessels»--which in
addition to its primitive
function Inust neces-  88.%l‘hii'eie larval (_lt:l't'l()})lllt‘lll. of a ‘l'l(f\\'loW
sarily also function as it  famiu/us) as seen from above. (After Egert,
very efficient organ of '
respiratory exchange and what looks like :1 posit-rior 4-..\'tc-rnal gill is the ]w(:L-()1‘fll limh.
SO render 311)’ Pre'eX-1st‘ In l"ii-_:.s'. ll and (l flu-1-Xternal _«_;'ill:~' lmve l)l',‘(‘ll cut away leaving
ing respiratbry organ no only tll(‘ll,'l)-‘mill .~'i-urnps.
longer necessary.
Taking into consideration the presence of external gills in three
archaic groups of Vertebrates it seems to the present writer to be
clearly indicated that these organs are a very ancient characteristic of
the Vertebrate phylum. The only alternative indeed is to regard
them as having become evolved independently in the three groups
in which they occur. It is diflicult to accept this as in any way
probable having regard to the similar morphological relations of the
organs in question.
It might be suggested that somewhere on the course of a large
blood-vessel, such as an aortic arch, would be a most natural place
for the development of a new respiratory organ. Such a suggestion
however is entirely fallacious for simple physical reasons: for new
breathing organs will tend to become evolved -not on the course of a
b, lnilaiurei-; !'.§I,i'_\t91‘l1:ll gillol'lir.-1. ln'anchial:1rch. In l«‘i_«,v-. A '
158 EMBRYOLOGY OF THE LOWER V ERTEBI-LATES (311.
large vessel where the quantitative relation of surface to volume in
the blood-vessel is at its minimum but rather where there is present
a rich superficial network of capillaries, in which the ratio in question
is at its maximum. .
(IL) VISCERAL CLEFTS. --The visceral clefts develop in what
appears to be the most archaic method in Lampreys and Elasmo-
branehs Where each arises as a lateral pocket (visceral pouch) of
the pharyngeal wall which meets and fuses with a., much shallower,
ingrowth of the ectoderm, the apposed portion of cndoderm and
ectoderm breaking down so as to bring about a free communication
between pharynx and exterior. Each cleft thus consists of a, usually
much larger, inner portion lined with endoderm and an outer portion
lined with ectoderm.
The most frequent type of modification of this probably primitive
mode of cleft development is that so usually met with in the develop-
ment of hollow organs, namely that the cleft-rudiment, instead of
being a hollow pouch from the beginning, is for a time in the form of
a solid lamina of endoderm, which only at a later period develops a
cavity in its interior and becomes an open cleft. This modification
is found in Teleostomatous fishes, Lung-fishes and Amphibians.
111 the young Elasmobraneh the gill-clefts are at first long slits
"traversing the whole dorsi-ventral extent of the lateral wall of the
pharynx. Each septum or arch grows back at its outer edge to form
a valvular flap overlapping the cleft next behind it. In most cases
this backgrowth fuses with the next septum at its dorsal and ventral
ends so as to reduce the external opening of the cleft to a compara-
tively small dorsi-ventral extent.
In all Gnathostonies, excepting the typical Elasmobranehs but
including the Holocephali, the hyoidean backgrowth becomes greatly
enlarged to form the operculum which overlaps the whole series of
clefts behind it. Correlated with this the outer portions of the sub-
sequent septa with their backgrowths become reduced. I11 these
cases we frequently find a marked tendency for the edge of the
opercular backgrowth to become fused with the body so as to restrict
the size of the opening behind it. Thus in the Eel the opercular
opening becomes reduced to a small persistent ventral portion, while
in S3/mbmncltas the same holds but in this case the two openings
have fused together to form a small ventrally placed median
ore.
P A similar condition to this occurs in the tadpole of Discoglossus
while in other Anura the persisting opening is displaced to the left
side. Finally in Amniotes the fusion of opercular margin with body-
wall takes place along its whole extent so that the branchial region
becomes completely enclosed (see Chap. X.).
SPIRACLE.-——The spiraele or hyomandibular cleft always shows a
considerable amount of modification. In Elasmobranehs its dorsal
portion alone becomes perforate, although fusion of the pouch with
the ectoderm takes place throughout its whole dorsi-ventral extent.
.the Amniota the distal portion of the
I I r GILLS ' ' _ 159
hespiratory lamellae develop only on its anterior wall and these, as
development proceeds, become vestigial forming the pseudobranch.
In Teleostean fishes the spiracular pouch (Fig. 89 A, cc. I) flattens
out and disappears (Goette) so that the pseudobranch (pa) on its
anterior wall comesto lie on the inner face of the base of the operculum
and appears to belong to the second cleft (Fig. 89, B). In Lung-fishes
the soli.d endodermal rudiment never becomes perforate. It becomes
gradually reduced during development while "its outer ectodermal
portion becomes, as already indicated,
converted into a special sense-organ.
In Anurous Amphibians and in
cleft rudiment becomes greatly dilated
to form the tympanic cavity, while the
proximal part forms the relatively
narrow Eustachian tube.
Just as the varying condition of
the spiracle indicates a tendency for
this cleft to undergo reduction so a
similar but still more marked tendency
exists for the gill clefts to become
reduced at the other (posterior) end
of the series. This is illustrated in
the first place by the reduction in the
number of functional clefts seen in
passing from the lower Vertebrates
to the higher. It is also frequently
manifested in developmental stages.
Thus 81110118317 the Amphibia we find Flu. 89.—-Horizontal sections through
that in the Gry1llI'l()pl1l0Ifl& (Hyp0g(3- Salmon embryos explaining position
Ophis, Marcus) 3 rudilnentary 7th cleft of pseudobranch. on inner surface of
_ . . operculum. (Atter (Joctte, 1901.)
makes its appearance though it never _ ' L. ‘
reaches the eehederm, while the 6th ...;i;Z'.'..i‘.i1'.?."i...:f:I?f:...:f:f:...?:II%‘:'§1..?鑧?'.;....:iZ.;
lS 0p9Il £01‘ 3. time. III UFOdBl8S EL  l and II; II;/,l1_yoi«l ar«.'.l1; -Ti-, ope-rculum;
rudiment appears and is for a time :"{"\"i"“l'jl‘-I3"Cf:-¥.g1*ll1tl'3'IIx2  1»-'vwlobw'=tnc1»;
connected with the ectoderm but does °’ W” (T '
not become perforate, while in Anura this cleft appears only as
a small and transient rudiment which never reaches the ectoderm.
(III.) INTERNAL G1LLs.——’_l‘he internal gills or respiratory lamellae
arise as ridge-like or, at first, finger-like projections of the cleft
lining. The chief matter of dispute regarding their development
has been the question whether they belong to the endodermal or
the ectodermal portion of the cleft lining. In cases where, as
frequently happens, the lamellae begin to develop after the cleft is
completely formed, the appearances are sometimes in favour of the
one sometimes in favour of the other interpretation. Goette (1901)
in fact goes the length of regarding the lamellae as being of endo-
dermal origin in the case of the spiracle and ectodermal in the case
160 EMBRYOLOGY 0 F THE LOWER Vl1‘.lt"El3l\’.A'l‘l+]S (‘.11.
of the succeeding clefts, so that the spiracular pseudoln-ancli would
on a strict interpretation of the germ-layer theory not be serially
homologous with the other gills.
In the present writur’s opinion, as already indicated, such ul)S61‘-
vations upon the first origin of organs which develop in the region
of the blurred boundary between two layers are not to be taken as
afihrding evidence ol' any serious importance in regard to the
morphological nature of such organs. Greater weight however seems
due to evidence obtained from cases where the hrst traces of gill
laniellae are visiblq; at a period before the bounding inmnbrane of
the cleft is ruptured, when the cleft consists still of two distinct
pnnches—ene eetoderinal, the other endodermal——separatcd by a
still eeuiplete partition. Such is the case in Aci_pc'nscr and (ioette
shows that in this case the laurella-rudiments arise outside the
partition from what is undoubtedly an
ectodermal surface (see Fig. 90, g.l).
 
Pl’ :3" '|‘he same discussion extends to the
' general lining cl’ the cleft~—as to how
go. much of the lining of the adult cleft is
/ ectodermal and how much endodermal.
-7" }octte and Morofl'(1902) hold that only
|"1u.90.—~ll0rizontal:-.m~1ionthrough the portion of Lhe cleft -in the innue-
bmwhial reg.“ M. ymmg AOL d1ate_ IlBlg'lll)Olll‘l100(‘l of its pharyngeal
peust-r showing the ('('f()de‘[‘[[]a1 opening 18 to be regarded as endodermal,
<(>‘I3:.:':It1e01'1f)1(I)*51s)i1l1am011ne- (Atter all therest. being ectodermal. But here
‘ ’ ‘ ° again 11] view of the blurred character
l.ll'iiI"‘ll‘.'ll”,Iiill,:i|l\(ill«l:ii(ill?:i:;‘,]ii;:.:iI('lii.llfllll: (.)f the boundary betvlreen the two layers
p;,, ..,...._,. .,,~,,1...,_,..x_ it seems hardly profitable to speculate
on the matter.
In certain fishes the gill-lamellae are for a time prolonged out-
wards into long threads which project through the cleft opening into
the surrounding fluid. Such is the case in the embryos of F.lasn1e-
branchs, in which it is only the lamellae upon the posterior face of
each arch that become prolonged, those on the anterior face not
projecting beyond the edge of the septum. Eventually the pro-
jecting part of the filament disappears while its attached basal
portion becomes the definitive lamella. In a few Teleosts a similar
temporary modification of the lamellae takes place ——~perhups the
best example being Gymnarclms (Budgett, 1901; Assheton, 1907.
See Fig. 199).
EVOLUTIONARY HISTORY or rm-1 BRANLIHIAL RESPIRATORY
()RGANs.——-As regards the early evolutionaryhistory of these branclnal
respiratory organs one very generally accepted View looks upon the
visceral clefts as being the most primitive, the internal gills as
having developed next, and the external gills as being due to
secondary extension of respiratory tissue outwards from the clefts.
It seems however, bearing in mind what we now know regarding the
development and distribution of external gills, at least equally ii’ llnl.
III LUNG 161
more probable that the evolution of these organs has been in the
opposite direction.
On this latter hypothesis the external gills would be regarded
as the primitive respiratory organs, inherited probably from pre-
vertebrate ancestral forms. The evolution of clefts between their
bases would be explicable as an arrangement for pumping water
over the surface of the external gills, while it could be readily
understood that the respiratory tissue would then tend to spread
inwards along the lining of the clefts, where it would be both
advantageously situated for carrying out its breathing function and,
at the same time, protected from the dangers to which external gills
are exposed. The development of respiratory lamellae to increase
the area of this respiratory tissue on the wall of the cleft would be a
further and natural development.
The chief difficulty in the way of accepting this as a working
hypothesis lies in the existence of animals admittedly near the base
of the Vertebrate scale—such as Amp/2/ioxus and the Cyclosto_
mata-—in which there are no external gills and no vascular
yolk-sac to account for their disappearance. This difficulty is
undoubtedly a serious one but on the whole the present writer is
inclined to think the difficnlty is not so great as to justify the
immediate rejection of the hypothesis: it becomes less formidable
when it is borne in mind that the forms mentioned although
evidently archaic in some of their characteristics bear in others
equally convincing evidence of high specialization. _
LUNG.—-In all the groups of Gnathostomata excepting the Elasmo-
branch fishes the pharyngeal wall develops a great outgrowth
which, as will become apparent later, is to be looked upon as home-
logous throughout the series and as primarily respiratory in its
function-——the lung. The lung appears in its most familiar and
typical form in the tetrapod Vertebrates and its development in
these will accordingly be considered first.
Here in an early stage of its development the lung is in the
form of a pocket of the pharyngeal floor projecting downwards in
the mid—ventral line. This pocket commonly makes its first
appearance as a longitudinal groove or gutter in the floor of the
pharynx at about the level of the last ‘visceral cleft. The groove
becomes constricted off from behind forwards, so as to form a
blindly ending pocket communicating in front with the pharyngeal
cavity by a narrow opening—the g‘lottis—and extending back
immediately ventral to the pharynx. The blind end of the pocket
grows actively tailwards and becomes deeply bi1obed—-—the two
lobes becoming respectively the right and left lung, while the
unpaired portion connecting them with the glottis becomes the
trachea or pneumatic duct.
While the lung passes in its early history through stages corre-
sponding on the whole with those described there are differences in
detail in different groups-—-the most conspicuous of these variations
VOL. II ' M
162 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.
being, as is so often the case in the development of hollow organs,
that the rudiment is at first solid and the cavity appears secondarily
in its interior. This is the case in various anurous amphibians and
in Jlepiolosofirevz and .1’-r0t01ate'/"as.
It has been indicated that the lung is primarily a ventra.lly
placed pocket of the pharyngeal wall, that is to say its wall is a
portion of splanchnopleure. It follows that the cavity of the lung
is lined by endoderm while its outer layers (connective tissue, blood-
vessels, muscles, etc.) are composed of splanchnic mesoderm.
As regards the further development of the lung, the main steps
are concerned with its respiratory function and have to do with the
increase of the respiratory surface. In such an animal as the Newt,
where the lung retains a relatively primitive condition, the endo-
dcrmal lining grows equally as the organ increases in size, so that
even in the adult the lung has the form of a simple sac with smooth
endodermal lining. In a Frog or a Lizard, however, growth activity
is specially marked at particular spots so that at these spots the
cndoderm forms outward bulgings into the covering of splanchnic
mesoderm.
In these Sauropsida in which the pulmonary apparatus reaches
its highest degree of evolution (Tortoises, Turtles, Crocodiles and
Birds, in an ascending series) these pockets of the endodermal
lining become more and more extensive, and more and more com-
plicated, so as to give rise to a thick spongy mass, which forms the
bulk of the lung, surrounding the now relatively small clear central
space. The latter, forming as it does an apparent continuation
of the bronchus or paired portion of the trachea, is spoken of as
the intrapulmonary bronchus. Further the respiratory function
becomes concentrated towards the terminal portions of the pockets,
their proximal portions forming simply conducting channels-—
branches of the intrapulmonary bronchus.
In the Chameleons, towards the end of development, a number
of the endederm outgrowths bulge out beyond the general level of
the surface of the lung upon its ventral side. These persist in the
adult as large diverticula which when the animal blows itself out
are inflated with air. In the embryos of Birds similar outgrowths
make their appearance, four from each lung, but in this case as
development goes on the outgrowths continue to increase in size
and form the characteristic air-sacs of the adult bird.
THE LUNG or BIRDs.—-—As the Birds, in correlation with the
intensely active metabolism as indicated e.g. by their high body
temperature, stand pre-eminent amongst Vertebrates in the high
stage of evolution which has been reached by their lung, the onto-
genetic development of this organ will be followed out in a little
more detail (Moser, 1902; J uillet, 1912).
In the Fowl the pulmonary diverticulum of the pharyngeal floor
makes its appearance about the beginning of the third day. By the
end of this day the rudiment is bifurcated at'its hind end, each lobe
III LUNG 163
being the rudiment of a lung in the restricted sense and containing
a prolongation of the enteric cavity lined by tall columnar endoderm
cells. Outside the eiidoderm is a thick layer of inesenchyme and
this in turn is covered by columnar coelomic epithelium.
The endoderm-lined cavity is destined to become the main
intrapulmonary bronchus—-the mesobronchus. This remains un-
branched until the fifth day when its cndoderm begins to bulge
out, near the point where it enters the lung, to form the first ento-
bronchus. During further development a. series of three other
entobronchial outgrowths sprout out from the external surface of
the inesohronchus close behind the first outgrowth. The four ento-
bronchi so arising are closely contiguous and form a longitudinal
row (Fig. 92, El-E4).
A set of similar outgrowths make their appearance spaced out
along the mesial side of the mesobronchus posterior to the ento-
bronchi: these are the rudiments of the ectobronchi. A third set of
outgrowths on the lateral 0
side of the mesobronchus ejcf.
are the rudiments of the Z‘
small secondary lateral
bronchi (Campana). Of
these sets of outgrowths
the first and second are
the most important and
they are arranged in a
slightly spiral row along
the wall of the meso-
51:
bronchus.
The mesobronchus, as FIG. 9l.—_Diagraiii illiistratiiig the arrangement of the
it grows in length main air-passages in the lung of the Fowl as seen
3
h b from the mesial plane. (After J uillet, 1912.)
assumes a Somew a ' l(’ is‘ c .. uni‘ an eii'.0i« '-
m-shaped curvature. by M’ l'its?‘.1...;o§i3o:.:iii§?',..i,-,',....r:£.,.;~.)i.¢l.i.m"
which the Group of ecto- ~
bronchi are: carried towards the (1'lO1‘Sa.fl facéa fof the lgng while the
entobronchi are nearer the ventra sur ace c . Fig. 91 . Both ecto-
bronchi and entobronchi grow rapidly parallel with and close to
the surface of the lung-rudiment. They soon produce secondary
branches as projections of their walls and these secondary branches
increase greatly in length traversing the substance of the lung at
first close to its median surface and, later, deep down in its sub-
stance as well—-—the eiitobronchial branches growing in a dorsal and
the ectobrauchial in a ventral direction.‘
The two sets of branches fits their t1% 1E:p‘pI‘01f1it(3l1 1(l)I1e another Iarg
seen to alternate in position ( ig. 91). en t ey ave approac e
closely each branch bifurcates and its two tips become closely
apposed to the two tips belonging to the other serieswhich lie
closest to them. About the thirteenth day these apposed tips become
completely fused and their cavities continuous so that there is now
I/I///‘I/l-:’I"'.. T '
//((!l{!)ll‘Z‘llE};';
164 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.
established a series of channels running in a dorsiventral direction
through the substance of the lung aml communicating dorsally with
the ectobrcnchi and ventrally with the entobronchi. The channels
in question are termed parabronchi (Fig. 91, par). These are
embedded in an abundant matrix of mesenchymc which from about
the tenth day becomes divided up into more or less prismatic
masses each having in its axis an individual parabronchus—the
prisms being delimited from one another by the development of
intervening blood-vessels. The mesenehyme which constitutes the
inner portion of this sheath round each parabronchus becomes later
replaced by a layer of smooth muscle fibres.
At about the same period as the fusion of the parabronchial tips
takes place, the Wall of the parabronchus begins to grow out into
numerous little pockets arranged in radiating fashion. These extend
outwards, perforating; the muscular sheath, and at a short distance
from the parabronchus divide into branches which in turn elongate
and become the air-capillaries of the fully developed lung. Judging
from adult structure it would appear that the tips of these fuse
with others to form the continuous air-capillaries so that the latter
would be formed much in the same way as the parabronchi but
it has not been possible, so far, to demonstrate this by actual
observation.
The essential features of the development of the Bird’s lung as
above outlined may be summed up in the statement that in this
type of lung the diverticula of the intrapulmonary bronchus, which
in other Vertebrates end blindly, become here joined together tip
to tip to form continuous tubular channels. To allow this arrange-
ment to function efficiently an apparatus is needed to force the air
throu h the system of respiratory tubes: such an apparatus is
provi ed by the air—sacs.
AIR-SACS.-—-The ventral part of the lung-rudiment is for a time
formed of a thick mass of mesenchymatous tissue which has been
termed by Bertelli the primary diaphragm, from the fact that it
becomes continuous along its lateral margin with the side wall of
the splanchnocoele, so as to form a kind of floor separating off the
lung from the splanchnocoele which lies ventral to it. The air-sacs
arise as outgrowths of the bronchial cavities and are on each side
four in number: the first or most anterior giving rise to the cervical
sac, the second by bifurcation to interclavicular and anterior
thoracic sacs, the third to the posterior thoracic and the fourth to
the abdominal sac. The rudiments sprout out into the substance
of the primary diaphragm and become greatly distended within it,
bulging out ventrally amongst the viscera so that the ventral layer
of the diaphragm becomes stretched ‘out into a thin membranous
wall delimiting the cavity of the air-sac on its ventral side. The
dorsal part of the primary diaphragm, lying above the air-sacs,
persists as the floor of the lung or secondary diaphragm (ornithic
diaphragm of Bertelli, pulmonary aponeurosis of Huxley).
III T AIR-SACS 165
The air—sac rudiments sprout out (Fig. 92) from the main
pulmonary cavities-—the cervical from the first entobronchus, the
interclavicular and anterior thoracic jointly from the third ento-
bronchus, the posterior thoracic and the abdominal from the meso-
bronchus. Later on additional secondary communications between
the air-sac cavity and the pulmonary cavities are established (except
in the case of the cervical air-sac) by means of the recurrent
bronchi of J uillet. These arise in the ordinary fowl about the
tenth day of incubation in C3,.
the form of outgrowths of
the wall of the air-sac either
near its tip (interclavicular
and anterior thoracic) or just
before it emerges through the
general surface of the lung
(posterior thoracic and abdo-
minal) as shown in Fig. 92.
These outgrowths burrow
into the superficial layer of
the lung, branch and become
joined up, in a manner the
details of which have not yet
been worked out, with the
system of parabronchi. The
communications are visible
in suitable preparations of
the adult lung as groups of
openings, each group leading in
into the lung from the appro- /0’ ./
priate air-sac——those of the
interclavicular and anterior 05-
thoracic lying towards the FIG. 92.——])iagranuuatic view of the right lung of
lateral edge Of ’Dl]6 ventral a Fowl embryo of the tenth day as seen from
surface of the lung, about the “:9 V°‘:"“‘(j{%:éri11;1::fi%::i'1s1 ;>1'is_iI{Ihe0fflt)1l:<;
. a r-sac . c '-, ~ -
level of the attaclllllent of entobronchi are shaded.
the bronchus’ and those of rib, abdominal air-sac; at, anterior thoracic air-sac:
the POSl73ri0r th0ra»0i0 and car, cervical air-sac; 14."! and 164, llrst and fourth ento-
abdonlinal sacs  near bronchi; tc, iiiterclapicular air-sac‘; -nies,tn:)¢sst)ll;1;otrl1sch1is;
      pl, pUHl3('3I'10I‘bl'|0I‘8a('alL fllI"8{lC, T, I‘l,LllII‘0-ll P01. 1 ...
close to the direct opening between it and the corresponding air-sac.
It would appear that the function of these recurrent channels
is to conduct the air forced out of the air-sacs in the expiratory
effort through the system of air-capillaries, the muscular coat of the
parabronchi doubtless playing an important part in directing the
passage of the air through the system of air-capillaries rather than
through the parabronchi themselves. a
The formation of the air-sacs does not exhaust the remarkable
proliferative powers of the wall of the lung in Birds. Further out-
III A IR—‘I'._LA DDER 167
FIG. 93.-—-Development of the air-bladder of n Teleost. (After Moser, 19,,4.)
A, Jmodeus, 5 mm., longitudinal section; B, Rh-Od¢'ll.$', 6 mm., longitudinal S(‘(!U()lI2 (.‘., Rlmdemz,
7 mm., trans-vt-rse section, showing small pouch-like mxtgrowtli of pneumatic duct; uml, emlu«lu'r1|1; cut,
enteric cavity; 2, uir-bladder; Ii, liver; N, notochord: mt, pronephric chmnbur; p.41, pm-.Iu1m.tic
duct; '_l/, yolk.
168 EMBRYOLOGY OF THE LOWER VERTEBRATES (in.
to form a kind of diaphragm perforated in its centre and capable of
being thrown into vibration by air being forced from one chamber
into the other so as to function as a sound-producing organ (e-._g.
Gurnards). Other outgrowths may develop: thus for example in
many Siluroids numerous branched projections are formed along each
side of the air-bladder.
The air-bladder rudiment is at its first appearance in some cases
approximately dorsal in position (Selma). In Jihodeus Moser (1904)
has shown that the diverticulum is at first on the right side of the
alimentary canal. The same observer found that during the early
stages of development of the air-bladder the portion of alimentary
canal from which it springs undergoes a process of rotation about its
long axis in such a direction that a point on its dorsal surface is
carried towards the left side.
Although the actual development has been worked out only in a
few cases, we may infer safely from the adult relations (Rowntrce,
1903) that the amount of this rotation differs greatly in different
.members of the group Teleostei. Thus in Siluroids and Cyprinodonts
the glottis or pharyngeal opening is in the adult still to the right of
the mesial plane; in others such as the genera 0smer'us, Olupea,
Olwrocentrus it is practically median; in still others such as
Mormyrids, Characinids, Gymnotids and Cyprinids it has passed the
mesial plane so as to lie upon its left side, while in the case of the
Characinids Jllacrodon, Erythmlnus and ]}r’b'ias'i'na the glottis has come
to be completely lateral on the left side. This rotation of the gut in
the region of the glottis is of much morphological importance as will
be shown later.
In the young Rhodeus, 7 111111. in length, Moscr finds that a well-
marked diverticulum from the pneumatic duct is present (Fig. 93, 0).
Later on it gradually disappears. A similar diverticulum occurs in
Salmo and in the Carp, and in all probability in numerous other
Teleosts: its morphological significance will be discussed later.
ACTINOPTERYGIAN GANOIDS.——In these fishes the development of
the air-bladder takes place on similar lines to that described for
Teleosts. In Amda the additional detail has been made out that the
rudiment is at first in the form of a longitudinally placed groove
which becomes constricted off from the alimentary canal from behind
forwards just as frequently happens in the case of the typical lung-
rudiment of air - breathing Vertebrates (Bashford Dean, 1896;
Piper, 1902). A rotation of the section of alimentary canal in the
region of the glottis takes place similar to that which occurs in the
Teleost.
LUNG-FISHES.-—In the adult Oeratodus an organ occurs which is
equally lung and air-bladder. It forms an unpaired sac lying dorsal
to the splanchnocoele just like a typical air-bladder, but the pneu-
matic duct, instead of opening directly into the alimentary canal
dorsally, passes round the right side and opens by a ventrally placed
glottis. In Lepidosiren and Protopterus the general arrangement is
m i LUNG _ 169
the same except that here the organ is deeply bilohed: a right aml a
left lung or air-bladder occupying the place of the single organ of
0'e'ratodus.
The meaning of the ventral position of the glottis in these Lung-
fishes, and, in fact, the morphological nature of the whole organ, is
Flo. 94.--Transverse sections through the endoderm of the pharynx showing an early
stage in the development of the lung.
A, Polypterus, B, (}'era,tmIu.,g, and O, Bmn..h1',nato1' (O aTl5er Goette, 1875). 1, lung-rudiment;
ph, pharynx.
demonstrated by the examination of early stages in development.
In these the organ is found to be a perfectly typical lung-rudiment
(Fig. 94, B)-——a mid—ventral projection from the pharyngeal floor of
precisely the same kind as that found in te_trapodous vertebrates (C).1
Fm. 95.——Views showing early stages of the lung-rudiment of Protopterus as seen from
the ventral side (stages xxxii, xxxiv, xxxv).
e.g, external gill; I, lung; oes, oesophagus; pan, dorsal pancreas; ,2. f, pectoral limb; Th, thyroid ;
v.c, visceral cleft rudiment. (Cut surfaces are inclieatml by uniform light tone.)
Subsequent stages are illustrated by Figs. 95 and 96. The lung
rudiment at first a rounded knob (Fig. 95, A) grows backwards and
soon becomes bilobed (B). The figure does not bring out one im-
portant fact namely that the lung-rudiment as it grows backwards
1 The projection is at first solid in the case of Lcpvidoseren and Protopter-us.
III CEMENT-ORGANS . 179
head on each side as shown in Figs. 100, A, and 197, C, 0.0. A longj-
tudinal section through the centre of the organ at about this stage
(stage 26, Fig. 101, E) shows that the organ is covered hy the
ordinary 2-layered ectoderm. Round the lip of the opening at its
Flo. l0l.——Illustrating the development of the cement-organ of l’oly_pterus. B represents
part of a transverse section, the other figures portions of horizontal sections.
A and B, stage 20; C, stage 23; D, stage 24; E, stage 26. mo, cement-organ.
The darker tone indicates ectoderm.
free end, the superficial layer of ectoderm stops, while the deep layer
seems to dip down as a deep involution to form the secretoryepithelium
(c.o) which lines the cavity. All the appearances seem to point to
the secretory epithelium being ectodermal in its nature. How
deceptive these appearances are will be gathered from an inspection
of ‘ig. 101, A-E.
III LUNG 171
the archaic mode of development, the lung-rudiment (Fin. 97, Z)
describes a spiral curve round the oesophagus so that the bifurcated
FIG. 97.———Porti0ns oi‘ l.l‘{Ll1SV8I'S0 sections through :1 Lepiulosiren larva (stage 34) to
illustrate the eli:u1gin;_:' relations of lung to gut from at short distance behind the glottis
l2tliW:ll'1lH. In .\ l.h«- lung is ventral to the :Llirn(-.ntary canal _; in B it is directly to the
riglit ; in (3 it has lm_-mm: displaced dorsally ; while in D (where it is commencing to
bifurcate) it has come to he llll(l-(iflrfial in position.
.4, aorti; gt, glomerulus ot'pron«_-phros; I, lung; N, notochord; ues, oesophagus.
hinder end of the rudiment, which will give rise to the lungs in the
restricted sense, comes to lie dorsal to the alimentary canal. ~
The lungs continue their tailward growth in the substance of the
172. EMBRYOL()GrY OF THE LOWER VERTEBRATES OH.
dorsal mcsentery (Fig. 97, 1)) but eventually the portion of this
mesentery containing the lung and dorsal to it becomes greatly
thickened from side to side and finally merges completely in the roof
of the splanchnocoele, so that in the adult condition the lungs lie
completely outside the body-cavity——between it and the vertebral
column.
In Uemtodus (Gregg Wilson, 1901; N cumayr, 1904) the lung is
at first, as in the other two lung—fishes, ventral in position (Fig. 94, B)
but in this case the originally left lung, which in Lepidostrevz, and
I’7"utopte'rus is for a time during development reduced in size, seems
to have disappeared almost entirely, being represented only by'a small
and transient rudiment. Further detailed studies of the early stages
in the development of the lung of Uemtoclus are much needed to
make clear the origin and fate of this vestigial left lung. But it
seems clear from what is already known that the monopncumatic
condition of Ceratndlzzis has come about in evolution through the
suppression of the originally left lung.
As the lung completes its development, its cavity becomes en-
croachcd upon by two median longitudinal ridge-like ingrowths, one
dorsal and the other ventral. It used to be supposed that these
marked an incipient division of the l11ng into a right and a left half
so as to bring about the condition seen in Leptdostren or Protopter-as
—the monopneumatic condition being supposed to be the more
nearly primitive. It will have been gathered from what has been
said that this point of view is no longer tenable and that the n1ono-
pneumatic condition of Cemtoalus is to he looked on as secondary and
not primary.
CROSSOPTERYGIANS. — Of the two surviving examples of the
Crossopterygian ganoids—the most archaic existing members of the
Ganoid-Teleostean stem—a few stages in the development of the lung
have been investigated in Poly/pterras (Graham Kerr, 1907). In the
earliest stage observed the lung—rudi1nent was in the form of a mid-
ventral groove formed by an outgrowth of the pharyngeal lining
(Fig. 94, A, Z). This groove becomes deeper and towards its posterior
end widens out ventrally so as to have a .L-shape in transverse section.
Posteriorly the lung-rudiment grows back into a pair of horn-like
projections——the rudiments of the right and left lung. These extend
backwards in the connective tissue of the splanchnopleure and they
very soon show a marked inequality in their rate of growth the left
lagging behind the right. As growth goes on this inequality becomes
more and more marked, so that in a larva of about 30 mm. in length
the right‘ lung extended right back to the cloaca while the left pro-
jected back only about 3 mm. behind the glottis.
In these later stages another important feature is to be noticed,
one which is correlated with the fact that the air-filled lung neces-
sarily acts as a float in an aquatic animal. This feature is that the
lung tends to assume a position symmetrical about the median plane.
Thus in the anterior region where both lungs are present they are
m  AIR-BLADDER  173 ,
situated laterally, balancing one another, while farther back where
only the right lung is present this shifts towards the mesial plane
until it is symmetrical about that plane, lying in the dorsal
mesentery (Fig. 98, A and B).
EVOLUTION on THE Am-BLADDER.-—-'l‘he facts that have been
enunciated above, with regard to the development of the lung in
Dipnoan and Crossopterygian fishes, are of much morphological
interest. When pieced together with what has been said regarding
the development of the air-bladder of Teleostcan fishes they afford
data from which the evolutionary history of the Teleostean air-
bladder can be traced out with a high degree of probability.
That history may be
stated in a few words
to have probably
been as follows:
1. The primitive
condition was that
of a lung, communi-
eating with the
pharynx by a ven- '
trally placed glottis
——-for we have seen
that the‘ embryonic
rudiment of the
organ in the most
archaic forms pos-
sessing it is a typical
lun,r_f-rudiment.
2. The organ
became bilobed,
growing back into a
right‘, lung and a, left FIG. 98.-—S_ections through the lungs of a larva of
hula. Polypterus 30 mm. in length.
,__,.
'3_ In the for-Ins 1 f1:,1lnO!'O1l;llbeI'€0I‘l; Ba more postplrior; 1.4, aorta; mg, enteron ;i Ll,
. . e ung; no 00101‘ ' opn Opls xonvp nos: 1». 1-, pm monary ve us;
Wh]-ch took to 3' rnl, right lurig; 1:, lntcrrenal vein.
purely swimming
existence, and became specialized in the direction of adaptation to this,
l)l]_(_‘.1‘(‘. ('..'Hn(__‘. about an asymmetry of the lungs, the right lung increas-
ing and the left lung diminishing. Why this should have happened
is not yet absolutely certain: it may probably have been in adapta-
tion to active movements of ‘lateral flexure, for we see the same thing
taking place in Grymnophiona, Snakes and Snu.l<o—like Lizards. That
it has been the right rather than the left lung which has increased
in size, is probably correlated with the rotation of this region of
the alimentary canal in a counter-clockwise direction as seen from
behind (seep. 168) which would tend to interfere more with the
circulation through the left lung than with that through the right,
by lengthening the course of the left pulmonary artery. Steps
174 EMBRYOLOGY OF THE LOWER VERTEBRATES GIL
in the development of this asymmetry are seen in Poly/ptems and in
the Lung-fislics.
4. In purely aquatic creatures the dictates of adaptation would
naturally cause the air-filled lung to assume a dorsal position. An
initial phase of this is repeated in Polyptems where the right lung
has become dorsal and median in its hinder portion. In the Lung-
fishes a further step is takcn—--the whole of the lung becoming dorsal
except the pneumatic duct which still remains to mark out the path
by which the lung moved dorsalwards round the right side of the
alimentary canal.
That the movement dorsalwards was round the right side was no
doubt due to the right lung being predominant and the left reduced
in size. In the case of Oezatodus the predominance of the original
right lung has been retained, the other being completely obsolete
except for a short period during development. In Lepidosvlzen and
Protopterzzs, on the other hand, the lopsidedness disappears, the
original left lung regaining during ontogeny its primitive equality in
size with its follow.
5. In the Actinopterygians——those fishes which show the highest
degree of evolution in adaptation to a swimming mode of 1ife———the
lung has in the course of its evolution passed through similar stages
to those exemplified by Poly/pterus and Oeratodus. Here again only
the original right lung persists as the air-bladder, the vestige of the
left lung being possibly represented by the little diverticulum found
by Moser upon the pneumatic duct in early stages of development}
In the Actinopterygians a further step onwards has been made in
that the glottis has assumed a dorsal position. This is fully ex-
plicable by the rotation which this part of the gut has undergone,
aided no doubt by the principle of economy of tissue which would
tend to bring about a shortening of the unnecessarily long pneumatic
duct. In some cases there still persist vestiges of the ancient cellular
respiratory lining of the swim-bladder (ag. LeZn'asz'na, Ezytlmnas).
6. Finally in the Physoclistic forms-——the most highly specialized
of all-—the swim-bladder has become completely isolated from the gut,
its respiratory function has gone and it subserves a mainly hydro-
static function.
The outline given above represents a scheme of evolution which
in the light of modern research has a high degree of probability. Of
course as in all such evolutionary speculations there exist details
which are still difficult to explain. While most of the facts of com-
parative anatomy fit in well with it, some do not——such as, for
example, the nerve-supply and the blood-supply of the air-bladder
of Am1Ia——-but it may be anticipated with considerable confidence that
these difficulties will be lessened or disappear with the progress of
research.
' See p. 168. This matter affords an interesting subject for further research.
III . THY R0 ID 17_5
DERIVATIVES OF PHARYNGEAL "WALL OTHER THAN THE
RESPIRATORY ORGANS
THYROID.——The Thyroid gland arises as a mid-ventral outgrowth
of the pharyngeal or buccal floor about the level of the Hyoid
FIG. 99.—Sagitta1 set-.t..i0ns through :mturior portion of :llilllI.‘Hl:U'_\' Uttlllll of l.¢jlm'do.w'n-1
illustrating the (l(‘.\'L‘l()plll('.lli- of the 'l‘hyroi«1.
A, I}, C from specinuyns of sttlgn 30; I), :-'et.‘l;.,'- 3| ; 'I‘h, thyroid: I, t.on:.rn¢-_
arch. In those Vertebrates in which the pharyngeal rudiment is solid
at this stage the thyroid outgrowth is also solid at its first appearance
(Fig. 99, A, T/2,) and develops its cavity secondarily by eytolysis.
176 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.
The Thyroid becomes gradually constricted off from the pharynx
(Fig. 99, B and C) remaining for a time connected by a narrow stalk
or duct with the pharyngeal or rather buecal floor just in front of
the primary tongue (see Fig. 82, p. 149). This stalk of attachment
becomes nipped across and the thyroid forms a mass (Fig. 99, D) or
vesicle rounded in form or somewhat elongated in an antero-posterior
direction lying in the mid-ventral line beneath the pharynx and
just in front of the ventral aorta.
The originally simple vesicle undergoes a process of sprouting
and division by which it becomes converted into a mass of rounded
vesicles, each possessing a wall composed of a single layer of cubical
epithelial cells and separated from its neighbours by highly vascular
mesenchyme which penetrates in between the vesicles to form the
stroma of the organ.
During later development the Thyroid undergoes characteristic
changes of form in different subdivisions of the Vertebrata. Thus in
Teleosts it frequently assumes a more or less diffuse character, the
follicles being distributed in the neighbourhood of the ventral aorta
and roots of the aifcrent branchial vessels. In the Amphibia and
Amniota the organ becomes deeply constricted into two laterally
placed lobes which may remain connected or may become separated,
so that it assumes a paired character as happens in Amphibians
and Birds.
With the processes of differential growth involved in the develop-
ment of the neck, the thyroid may undergo considerable displace-
ment from its point of origin. Thus in adult Lizards it lies across
the trachea well forwards from its hind end while in other reptiles
and in birds it lies farther back close to the roots of the great
arteries.
It is now generally accepted that the clue to the _phylogenetic
history of the Thyroid is afforded by its development in Petromyzon
(W. Muller, 1871). Here there develops a mid-ventral outgrowth of
the pharyngeal floor, forming a short gutter in the branchial region,
the lining of Which is composed partly of glandular cells which
secrete a sticky mucus and partly of cells which bear powerful
flagella. Morphologically this gutter is the same as the endostyle
of Ampkiowus and during larval life its function is also similar: it
appears to be in fact simply a shortened up endostyle. The slit-like
pharyngeal opening becomes gradually reduced in length till it forms
merely a small pore. _
At the time of metamorphosis the pore becomes obliterated so
that the organ becomes a closed vesicle underlying the pharynx.
This vesicle divides up into a number of small vesicles and its
mucous secretion accumulates in their interior as a colloid substance
like that of the Thyroid vesicles of the Grnathostomata. In a word,
the endostyle of the Ammocoetes stage becomes the Thyroid of the
adult, and there seems no reason to dpubt that the same has
happened in phylogeny and that the thyroid of the Vertebrate is
111 BRANCHIAL BU DS 177
simply the modern representative of the endostyle of the proto-
chordate ancestor.
An interesting feature is that while the physiological importance
of the thyroid in the modern Vertebrate is that of a ductless gland
for the production of internal secretion to be absorbed by the blood,
it still goes on producing the mucous material used by the far back
protochordate ancestor for entangling food particles, though that
substance is no longer, owing to the disappearance of the duct,
discharged into the pharyngeal cavity.
BRANCIIIAL BUDs.——There make their appearance in the develop
ing Vertebrate a series of bud-like proliferations of the endodermal
epithelium of -the branchial clefts which may be known as branchial
buds. They appear at the upper and lower angles of the clefts and
the series shows its fullest development in the Lampreys, where buds
develop at the dorsal and ventral angles of all the clefts. In the
majority of fishes investigated they have been found to appear at
the dorsal angles of all the clefts eficept the first; in Urodele
Amphibians at the dorsal angle of . clefts and at the ventral
angle of II., III. and IV.; in Anura at the dorsal ends of I. and II.
and at the ventral ends of ll.-V.; in Lacerta at the dorsal ends of
I.-III. and the ventral ends of III. and IV.; in Gallus at dorsal
and ventral ends of III. and IV.
The morphological significance of these organs is still completely
obscure. Physiologically some of them appear to be of importance
during the later stages of development preceding sexual maturity
inasmuch as they give rise to that often bulky organ the Thymus.
This arises by the fusion together of more or fewer of the dorsal
buds, the others undergoing no further development. Thus in
Lepvldosvlren (Bryce, 1906) dorsal buds III. and IV. develop into
thymus while II. and V. undergo no further development: in
Oeratodus (Grreil, 1913) II., III. and IV. give rise to Thymus while
V. and VI. do not develop further: in H3/pogeopltds II., III., IV.
and V. give rise to Thymus while rudiments on I. and VI. atrophy.
In regard to the much discussed histogenesis of the thymus all
that need be said here is that the originally solid epithelial rudiment
becomes in -the course of development loosened out into a sparse
reticulum interpenetrated by mesenchyme richly traversed by blood-
vessels and crowded with leucocytes.
The ventral buds, where they occur, become constricted off from
the branchial epithelium forming simple rounded masses of epithelial
cells (Amphibians) or they may be subdivided up by intrusive con-
nective tissue into solid portions (Reptiles) or hollow vesicles (Birds).
The small organs so formed are termed by their discoverer Maurer
epithelial bodies: their physiological significance is quite unknown.
There normally develops in the Vertebrate either on both sides
or only on the left side a small pouch-like diverticulum of the
pharyngeal wall close to the ventral edge of the last gill cleft, what-
ever the number of this be in the morphological series. The
VOL. II N
178 EMBRYOLOGY 01+‘ THE LOWER iVE_R'l‘EBIx’.A'1‘ES en.
divert culum becomes" separated from the pharynx and commonly
gives 'se to numerous rounded vesicles somewhat resembling those
of the yroid in appearance. The organ thus formed was named by
van Be melen who discovered it in Elasmobranchs--—suprapericardial
body—— iile Maurer has termed it the postbranchial body. Nothing
is delini ely known regarding either its function or its evolutionary
history, though it is someti.mes regarded as representing a vestigial
last gill—pouch. A curious point is the tendency of the organ to
unilateral development  it makes its appearance only upon the
left side in a large number of cases (Aca.nthz'as, Lepidosirevz and
1’7‘0t0pz1e'ms——-see Fig. 109, B-—most Urodeles, some Lizards).
CEMENT ()1z.m\Ns or 'J;m.sosroMA'i'oUs FlSHES.———-It has long been _
FIG. l00.—— Ventral views of Polyptcrus larva to show the cement-organs.
A, Stage 80; B, Stage 33; c.o, cement-org:-m ; «.71, olfactory ox-gun; m, mouth ; V, ventric-le of heart.
known that the larvae of Actinopterygian ganoids possess cement-
orgaus on the head in front of the mouth. Balfour (1881) wrote of
this as “ a very primitive Vertebrate organ, which has disappeared
in the adult state of almost all the Vertebrata; but it is probable
that further investigations will show that the Teleostei, and especially
the Siluroids, are not without traces of a similar structure.”
The organs in question were generally regarded as being developed
from a thickening of the ectoderm. Miss Phelps (1899) lirst stated
that they originated from endoderm (Amie) and the present writer,
at the time ignorant of her work, was greatly surprised to find
himself forced to this same conclusion by the examination of
I'5udgett’s material of Poly/pterrus.
The cement-organ of Poly/pterus (Graham Kerr, 1906 and 1907.),
when at the height of its development,_ forms a stout cylindrical
structure with a deep hollow at its free end, projecting from the
188 EMBRYOLOGY OF THE‘ LOWER VERTEBRATES
FIG. 108. Illustrating early development of the
liver in Birds.
A, 47-hour chick; B, 52-hour chick; C, 50-hour chick
(after Brouha, 1898); D, fourth-day chick; E, 7 mm.
embryo of the Roseate Tern--Sterne paradi.«n'aca.-(after
Hammer, 1807). M 1, rudiment of anterior (“1eft") bile-
CH.
portion of the rudiment. The
gall bladder originates as a
bulging of the floor of the
bile-duct towards its anterior
end. A
The formation of the pos-
terior and longer section of
the bile-duct, Which will be
extrahepatic in the adult,
lagsin its development behind
the anterior portions of the
rudiment. Such differences
in the time of appearance of
different parts of the hepatic
apparatus——1iver, gall-bladder,
bile-duct—-—are to be looked on
as mere secondary modifica-
tions of development,——the
primitive condition being that i
of a simple pocket of the gut-
wall such as persists in Am’-
phioasus.
SAUROPSIDA.-—-The hepatic
apparatus here again makes
its appearance as a longi-
tudinally situated pocket of
the morphologically ventral
Wall of the gut. In birds
this is situated at first on the
anterior wall of the yolk—stalk
(Fig. 108, A). The diverti-
culum grows actively into an
anterior (dorsal) and a pos-
terior (ventral) pocket (Fig.
108, C, Z73. 1 and Z7}. 2) while
the intervening portion be-
comes flattened out and incor-
porated in the gut-wall.
There thus come to be two
distinct liver-rudiments an
anterior and a posterior. Of
these each sprouts out at its
end into irregular projections
which eventually fuse and
form a spongy mass, surround-
ing the cavity of the ductus
duct; bd°. posterior (“risht") bile-duct; ent, cavity or venosus, and havingin its
fore-gut; gb, rudiment of gall-bladder; la‘. 1 and 2, anterior
and posterior liver - rudiments; pa.‘n,\ dorsal rudiment
of pancreas.
meshes blood-spaces which
180 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.
The first rudiment oi’ the organ is seen to bee simple pocket-like
outgrowth of the gut-wall (A, c.o): this becomes more and more
prominent (B, C): it becomes gradually constricted oh" at its base
from the gut-Wall, its cavity becoming isolated first  Finally it
separates completely from the main endoclerm and its outer end
undergoes fusion with the deep layer of the ectoderm. lts cavity
then opens to the exterior and the fully functional condition is
reached——the endodermal origin of the secretory lining being for a
time betrayed by the conspicuous persistent yolk granules in its cells.
It will be noted that the exposed side of the secretory epithelium,
that on which the secretion is extruded, is that which originally
faced inwards towards the lumen of the alimentary canal. In other
words the direction in which the extrusion takes place is morpho-
logically the same as that of any other part of the glandular lining
of the gut-wall.
As is the case in other forms the cement—org-an is a transient,
purely larval, structure. About stage 31 (Fig. 197, D) degeneration
commences: the gland shrivels up, the gland-cells becoming more
slender and dark pigment making its appearance in their interior,
the epithelium becomes penetrated by ingrowing blood-vessels, its
cell-boundaries become indistinct. The process of atrophy goes on
rapidly and by stage 36 (Fig. 197, F) the organ has completely
disappeared.
An interesting variation from the normal course of development
is found in specimens in which the cement-organ rudiments are
more or less approximated to one another. This variation reaches
its maximum in occasional individuals in which they are completely
fused and form an unpaired structure, continuous across the mesial
lane.
P In the actinopterygian Ganoids the cement—organ develops along
the same general lines as those just indicated. In the Sturgeons
the development has been worked out recently by Sawadsky (1911)
in Acipenser ruthenus. Here the organ forms a rounded projection,
very much in the same position as that of Polypterus, but in this
case each becomes divided by a groove so as to form two rounded
knobs. These knobs eventually grow out to form the tactile barbels
of the adult, the secretory epithelium being carried out on the
surface of the barbel as it grows.
The secretory epithelium is here also endodermal, its rudiment
being the gut-wall immediately dorsal to the position in which the
mouth will develop later and being continuous across the mesial
plane. The unpaired condition which occurs in Polypterus as a
variation is thus normal in the case of the sturgeon. As the head
increases in length the secretory epithelium becomes carried out on
its ventral surface, looking just as if it were the thickened ectoderm
of this surface. Finally the paired condition comes about, ‘the lateral
parts of the secretory epithelium coming. to be supported by the
knob-like projections already mentioned.
III CEMENT-ORGANS 181
Am/ia is of special interest in regard to its cement-organs as it
was in this form that their endodermal origin was first announced.‘
The organs are for a time in the form of a pair of rounded knobs,
one on each side, but these take on a crescentic shape so that together
they form a circular wall, interrupted anteriorly and posteriorly.
Each organ contains a pocket-like projection of the gut—wall which
takes on a somewhat sausage-like form in correlation with the curved
shape of the organ as a whole. This endodermal sac separates from
the main endoderm and becomes constricted across, so as to form°a
curved row of closed vesicles from six to ten in number. Each
vesicle fuses with the ectoderm and develops an opening to the
exterior so that it takes on the appearance of a cup at first deep and
narrow, later shallow and wider, its lining continuous with the deep
layer of the ectoderm.
When the larva reaches a length of 13-14 mm. it makes less use
of its cement-organ and the latter commences to degenerate, sinking
beneath the surface with which, however, it remains connected by
a narrow tubular channel. By about the 20 mm. stage this has
disappeared and soon there is no trace of the organ to be found even
in sections.
In Lepidosteus the organ appears to be similar while in the other
ganoids its development still remains to be worked out.
These cement-organs are of special interest and importance for
more than one reason. In the first place they are of importance in
revealing a quite unexpected pitfall in the way of the investigator
trained to have implicit faith in the germ-layer theory, for they show
how a particular organ may become transferred from one g'erm—layer
to another even though not belonging to the transitional zone where
the two layers are continuous. A very common modification of
ontogenetic development consists in the slurring over or even
omission of particular stages in early development. Were this to
happen in the case of the early stages in the development of the
cement—organ say of Polypterus, it is easy to see that the organ
might have every appearance of being purely ectodermal in its
nature, although it is, as a matter of fact, endodermal.
It appears to the present writer quite possible, if not probable,
that this modification has actually come about in the Dipnoi and
Amphibians, and that the cement-organs of these groups, although
they develop from the ectoderm in those forms which have been
investigated (p. 79), are really homologous with the cement-organs
of the Teleostomi, their cndodermal stage having been eliminated
from ontogenetic development. Further investigations are needed
in the Amphibia——to see whether no trace exists, in any member of
the group, of an original connexion with the endoderm.
As regards the original nature of these organs it is impossible
to arrive at any certain conclusion. Arising as they do in the form
‘ Phelps (1899). The actual discovery seems to have been made by Rcighard.
Cf. Reighard and Phelps (1908).
182 EMBRYOLOGY OF THE LOWER VERTEBRATES 011.
of endodermal pockets, they obviously recall gill pouches on the
one hand and coelenteric pouches on the other. Their position
suggests a pair of preniandibular gill pouches: their function, that
of forming an excretion (cement), perhaps indicates rather coelomic
afiinities and the present writer suggested (1906) their possible
correspondenee with premandibular head cavities of other Vertebrates.
Reighard and Phelps
(1908) hornologize
them wi th the anterior
pair of head-cavities of
Elasmobranchs while
van Wijhc (1914) sup-
l+‘m. I02. -Larva of Sa'rr_'.('u_l¢I..r_t(?s amlon. (After Budgett, 1901.) P‘-’I't3 3' homology With"
the ciliated organ of
Amphiowus.
Altogether these cement-organs are very interesting and puzzling
structures and would well repay further investigation. A thorough
comparative study should be made of their development in the
archaic Crossopterygians and of their possible homologues in
Elasmobranehs.
Little is known regarding cement-organs in Teleosts, though it
is proliable they will be found to occur in various tropical fresh-
water fishes. Budgett ' s
(1901) found a large P, _
cement-organ on the  he  . I « ,
head of the larva of the '1 /if/“‘jX~”
Characinid Sarcodaces 
odéie (Fig. 102, 0.0). Ina A 0 / (
larva believed to be that 9 ' 
of the Mormyrid IIype7°o- lg J
«an, or-ment-organ.
pisus babe he found six ’ ‘(
Well-marked cement 6.
glands on the head which 1 .
in this case secrete fine " U
threads by which the
larva hangs suspended
' ' F 1' 103 ——Teleostean l as in“ )()‘8l to be those of
in the water until the "' p "  s ““’*°' *1’! ~“ ’_
lk . _ _ _ ,. II;/_,;er0pos1ts bebe, suspended from the rootlets 111 the
18 H11_St‘3d t1_1P (15 1gd' nest. (From Budgett, 190].)
. 8 670 18 3.11
Gymnarclms also possess similar organs—-very small in the latter case 0
(Assheton, 1907).
The organs in these various fishes present, the appearance of
being ectodermal thickenings: we have as yet no information as to
whether, as may be suspected, they really originate from the
endoderm.
DIGESTIVE TRACT. —- The respiratory region of the alimentary
canal is succeeded by the true digestive _.tract and this shows
more or less pronounced differentiation into successive portions-—
III THE ALIMENTARY CANAL 183
oesophagus, stomach, intestine and its subdivisions, cloaca. In
correlation with the digestive and assiniilative function of the
intestinal endoderm this serves during early stages as the favourite
storehouse of food-yolk, and the concentration of yolk in the
abapical portion of the unsegmented egg is to be looked on as a
foreshadowing of the fact that this portion of the egg will later
become the endoderm. .
In the holoblastic Vertebrates the mass of heavily yolked endo-
derm cells becomes, as it were, modelled into a tubular shape by the
Fnz. 104. ----Illustrating the modelling of the yolk in .I¢.-/4././¢_:/u/;/u'.s-. (After Sarasins, 1889.)

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Kerr JG. Text-Book of Embryology II (1919) MacMillan and Co., London.

Textbook Chapters: 1 Formation of the Germ Layers | 2 Skin and Derivatives | 3 Alimentary Canal | 4 Coelomic Organs | 5 Skeleton | 6 Vascular | 7 Internal Body Features | 8 Adaptation to Environmental Conditions | 9 General Considerations | 10 Common Fowl | 11 Lower Vertebrates | Appendix

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Chapter III The Alimentary Canal

CHAP'l_‘l+3R III THE ALIMENTARY CANAL

THE alimentary canal or enteron‘ of the V crtebratc consists of a tube passing from the mouth to the anus. The wall of this tube is known technically as the splanchnopleure in contradistinction to the somatopleure or body-wall (Ballour). It consists of an inner lining epithelium, the endodcrm, cnsheathcd in a complex coating of mesoderm——the splanchnic mesodern1———consisting of connective tissue, blood-vessels, lymphatics, nerves, and coelomic or peritoneal epithelium.

As is commonly the case in other metazoa the cndodermal lining is in the Vertebrate more or less encroached upon at’ the oral and anal ends of the tube by the spreading inwards of ectoderm. The parts of the tube which come thus to be lined with ectoderm are known as stomodaeum and proctodaeum (L-ankester, 1876) while the intervening region lined by cndoderm is known as the mesenteron. In the Vertebrata there is very slight develop- ment of proctodaeum but an important section of the buccal cavity is, as will be seen later, stomodaeal in its nature.

It is also customary in embryological writings to use the some- what loose expression foregut for the anterior portion of the alimentary canal (reaching back to the pylorus or to the opening of the bile-duct), which in the meroblastic vertebrates becomes differentiated oil‘ from the yolk-sac comparatively early in de-

velopment. . _ . A good idea of the blocking out 01 the main regions of the

alimentary canal in one of the lower vertebrates is got by inspecting sagittal sections of embryos and larvae at different stages of develop- ment such as those shown in Fig. 80. From the gastrula stage (A) on to the stage illustrated in Fig. 80, C, the endoderm forms a simple sac with its opening posterior (anus) and with its ventral wall greatly thickened owing to the fact that its cells contain the main store of yolk. From the stage of Fig. 80, D onwards the foregut (f.g) becomes gradually constricted oil‘ in a tailward direction from the mass of yolk, while at the opposite end of the

body, correlated with the outgrowth of the posterior trunk region of

the embryo and the backward shifting of the anus, the yolky mass 144 152 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

Wards of the communication between olfactory and buccal cavities, a process which reachesits extreme in the Crocodilia where the palate extends back to about the level of the glottis.

STOMODAEAI. GLANDS.———Whereas in the majority of Fislies the stomodaeal lining possesses only isolated gland-cells, in the air- breathers on the other hand there are developed definite multicellular glands. These originate as a rule from solid down—growths of the

F10. 85.-View of the roof of the mouth in three species of Lizard (A, 19'_(/«ernw Ifingjivf ; B, Mabuia. qmfnqmflaemfata; U, Lygosonm. ‘l“ll.f(.’.S'('(’I'l.S‘), illustrating the shifting back of the communication between nose and month. (_ After Voeltzkow. 1899.)

rh, recess into which primitive posterior nan-s open ; pal, palatim.-. ; pt, pterygoid ; tr, transverse hone; no, vomer.

lining epithelium which develop a cavity secondarily. In Urodeles there is, as already mentioned, a special aggregation of these glands forming the gland-field in front of the tongue, while a single gland of considerable size develops from the roof of the mouth in the region between the olfactory sacs (lnterniaxillary or internasal gland).

In terrestrial Reptiles glands are present in numbers on ‘the roof of the mouth (Palatine), beneath the tongue on each side of the middle line (Sublingual) and along the edge of the month just external to the row of teeth -(Labial). The poison glands are specialized and enlarged labial glands of the upper jaw except in 146 EMBRYOLOGY 014‘ THE LO\V'ER VI|+}l't'l.‘EBRA’l.‘el'<}S (“.11.

case with I’roto1;le'2--u..s:, the huccal roof‘ in froiit, that is to say in the neighbourhood of the mesial plane, 1)&Lb'SGH without interi-upticm into the external skin: in other wo_rds the maxillary ridge is not con- tinued to the mesial plane so as to meet its fellow. In later stages

I~‘1o. 80.——Sagitt9.1 sections through P()l;/p/.(:.-e:l.s‘.

A. 3t9-L'.0 14.: 13. St--".‘-W W: C. Stage 20: 0, stage 2: ; E, stage-24 +. (1., mos; m-, :ll.1'llI--llt.I'l‘()Il ; e-ml, "-l1‘l"J"1<‘J‘||l1 "71’: ‘‘“l'‘_‘(‘- W‘ ll"-.\' 3 f-’’- ‘‘”\'“.V H!‘ forvln-uin: f.!7. fun-gut: N. uo1..nclmr(l 2 2).,/I. l""i"“"‘.V "*1" (If hruin ll-mr; pin, pnneul rmlivm-n1"; .-_:_-, ¢-;u-i1_\' of spinal cum"! ; 3/, yolk,

the roof of the mouth would be hidden in a view from the ventra side owing to the forward growth of the lower jaw. ' The anterior portion of the buccal cavity in Urodele A11l1)l'1il)ifl.l1S arises in a manner essentially similar to that descrihed above. In the G-ymnophiona and the Amniota a characteristic 1'nodifi.ca- tion of the mouth margin is‘ brought ahout hy the fact that, as III BUCCAL CAVITY 147

already mentioned, the maxillary ridge is cut across by the olfactory groove and so divided into the outer maxillary process and the inner median nasal process, the latter of which is continuous with its fellow across the mesial plane, forming with it the so-called

fronto-nasal process (see Chap. X.).

Fm. 8OA.~-—eS:t;;'lll:I.l Ht'('-ll()IlH txhroligh .I‘u/_:/}af:‘:'u.s".

1.‘, _\.1_ug., 3.3; G‘ smge -39; H, St:l‘L‘D‘[| :;-_>_ n, anus; u_«-, :ll|l.f‘l'l0l‘ (-onnnissllrn; 4-lo, optic cliiusrnu:

l clones.‘ ml enlmic c:l\'it.- : 1-]. heart : hm. halu-nnlar u-onnnissui'e: l1'., li\'<'l': m.r. m:m«lil.ul:u* r-i«lgo- , . . , Y _ _ _ 2,, pjt;ujt;n~y -;m-ulutimi ; pm, [_'M)h‘l.('l'lH1‘('l)]]1l|)iSfil|1‘!'; ,.n._:7, pH.~4l..'{ll:ll _-.;ut.: yum, pzuu-I-o-:it'Ir rudiment‘; /"rm. pineal rudiim-.nt.; 5’, .<t«mi:u:ln : y, yolk.

It is of interest to notice that in various Vertebrates the buccal opening is at first elongated in an antero-posterior direction instead of from side to side. Such is the case with Scylliuqn (Sedgwick, see Fig. 81) and ’1'o'rpedo amongst Elasinobranchs. In these cases the slit-like mouth is bounded on each side by a longitudinal ridge. 148 EMBRYOLOGY or rm: LOWER VERTEBRATES (:11.

Later on each ridge becomes sharply bent, about the middle of its length, in such a way as to give the buccal opening a rhomboidal shape and at the same time to mark oil’ the ridge into a maxillary portion in front and a mandibular portion behind. In Anura a somewhat similar arrangement is found.

“ENnonEuMAL” SECTION or BUCCAL CAvrrv.-—'l"‘he fully developed buecal ea.vity has incorporated in it a posterior portion- varying in relative extent in dil'l'erent Vertebrates—which is de- rived not from the ectoderm but from the anterior portion of the “endodermal” enteric rudiment. The simplest way in- which this portion becomes added to the anterior portion is seen in those Vertebrates in which the anterior part of the cnteric cavity is patent throughout develop- ment. In this case the velar membrane simply r u ptures——-its reinnants soon be- coming absorbed-- and the stomodaeal cavity is thrown into open communication with ‘ the cnteric cavity. This is the case in certain Anura (Rana) and in Amniota.


Fm. 8l.—--Ventral \'lt‘\\‘ of head region of embryos of Sag‘:/lliu-nz ¢-mu}-u/u. (After Sedgwick, 1892.)

A, 7—8 mm. ; 13, Sll_L','l)ll_\-' more :ulv:uu-ed than .\ ; C, H -12 mm. ; I), '16 mm.

brat-es no velar mem- brane is present, owing to the fact that the foregut either becomes solid for a time (Pol;/pteru.s, Fig. 80, D—Gr) or is so at the beginning (Teleostei, Urodela, Lepirlosvlren and Protopterus). In such cases the peripheral layer of the yolky foregut rudiment gradually assumes an epithelial character and the yolk along its middle breaks down, so that a cavity arises—continuous with the stomodaeal cavity and forming the hinder section of the definitive buccal cavity. The pro- portion which this posterior portion bears to tlfe anterior section derived directly from the outer surface is very different in different groups. It apparently attains its maximum" in Teleosts where

-it forms practically the whole of the. buecal cavity.

' Points of critical importance to the germ—1ayer theory are raised in this connexion by the fact that teeth, organs belonging originally to the outer surface, are developed in this posterior region of the buccal cavity from yolky “ endederm.” This is well seen in a Urodele, ‘or a lung-fish such as Lepidomlren or Protopterus (Fig. 82). The attempt is made to get round this difficulty by assuming that the layer of epithelium which makes its appearance over the surface of the buecal rudiment, and in relation with which the teeth develop, is really an ingrowth from the ectoderm.

In many V erte- T III BUCCAL CAVITY 149

It is, as a. matter of fact, quite continuous with the ectoderm,

FIG. 8‘2.—Sagittal section tl1rou;;l1 lu-.:ul I't’gi0Il of a Protopturus larva (Stage 33).

Inc, buccul ts-uvit-y: h.I, :ml<-riur l_u_nn1<l:u‘_\' of tongue; N, nulm-lnm‘41: pin, pine":-al lmtly: /W-I‘. pm-uphysi.-.: l’iI., pit: 5t.:u-_y bc«l_\': Th, tllymitl ruuliment; Lu, H.-rtum «-ptimluv. Th.-. p()sil.inn nr dvlllul rudiments is in<li<-.atml by Hue hm upwzu-d pr(r_ic:(:l.i()nS of the dOI".~m| wall of the buccal cavity.

but exaniinution of carefully prepared celloidin sections (Fig. 83) shows that at its inner end the epithelium passes by imperceptible

A 8

FIG. 83.—Sagittal N'(_‘llHllH t.h1'ough the 1'egi<_n1 of the lulucul cavity of (A) Lcpi¢.io.s£'rc1t, stage 30, and (B) .lmI:[.;/.s-Iowa, 7'5 mm. in i(‘ll§'.'_,'iiI.

b.c, bu(‘c::l opitllvlilllll ; 4'-cl, l‘L'tmlBl.'lll : _I/, .s'(_)litl Illziss of yolk-(.'I-ll.~: in pu.\'itiun 01' i.|ll(.‘('2tl vzivity.

gradations into the ordinary yolky endoderm, with no trace of the sharply defined edge which it would possess were it a 1uyer__of 150 EMBRYOIJOGY OF THE LOWER VERTEBRATES CH.

ectoclerm pushing its way inwards. It extends inwards simply by a process of delamination from the yolky “ endoderm.”

The real lesson to be learnt from these cases is that the charactcrs of one gcrm—layer are liable to spread over its boundary into l3C.5]‘l‘ll'.()Ty belonging to another layer or, in other words, that the territories of the various layers are liable to be separated by an indefinite debatable zone rather than by a mathematically sharp li.ne. It follows that the apparent position of an organ-rudiment in relation to such a boundary is not necessarily to be taken as

Fm. 84. —-Sagittal sections illustrating the development of the tongue in l_.l1'm_lclc..~'.

.\ and I5, Triton; C, Sula.-armndra (after Kallius, luol); _«_/.1‘, gland tie1d;__M, mandibular arch ; 7».I, priuuu-y t.ongLu.-.

giving any definitive proof as to which of the two cell-layers that organ belongs to.

Tim 'I"<mcUE.——The tongue is a portion of the buccal floor which becomes demarcated off from the rest by a split formed by a down- growth of the lining epithelium of the mouth. is mode of develop- ment is well illustrated by what happens in Urodele Amphibians_as described by Kallius. Here tlwru develops first a primary tongue, ensheathing the anterior and ventral portion of the hyoid arch (Fig. 84, pt), which becomes marked off, except at its hinder end, by a deep groove in the floor of the mouth.

A liorseslioasliaped thickening of the buccal epithelium now III BUCCAL CAVITY 151

develops external to, and parallel with, the groove bounding the primary tongue, and consequently lying on the floor of the month between the primary tongue and the lower jaw. The thyroid involution is situated between this thickening and the tip of the tongue.

The ectodermal thickening develops numerous glands, each originating as a solid ectodermal down-growth, and is known as the gland-field. Externally it is bounded by a shallow groove. Later on the cleft or groove separating the gland-field from the primary tongue becomes obliterated by fusion ol‘_its walls, and the gland-field becomes raised up in a dorsal direction (Fig. 84, B) the tongue-tip shrinking backwards so that eventually the demarcation between primary tongue and gland-field disappears (Fig. 84, 0). Meanwhile the groove bounding the gland-field externally becomes deepened. It forms the outer limit of the definitive tongue which is thus a compound structure, its tip and edges developed from the original gland—field, its postero-median part from the primary tongue.

In the fishes the tongue remains non-muscular and non-glandular: it is simply the primary tongue. In the Axolotl the tongue appears also to be a primary tongue, the gland-field making a transient appearance as a rudiment but eventually undergoing atrophy (Kallius).

In the Amniota the tongue is, as in the terrestrial Urodeles, a compound structure, the primary tongue rudiment becoming fused with an elevation of the floor of the mouth lying in front of the Thyroid rudiment. This elevation, called by His the tuberculum impar, represents morphologically the gland-field of the Urodeles.

The tongue of Cyclostomes is remarkable for its complexity: it has complex muscular and skeletal arrangements and on its surface it develops the horny spines which function as teeth and simulate teeth in their appearance. In Bdellostoma. the tongue develops as a cushion-like swelling of the floor of the mouth at an early period while the velar membrane is still intact. In J’et9°0m_2/zen, on the other hand, it does not develop until the time of metamorphosis.

It has already been shown how the olfactory organs come to communicate with the buccal cavity by the posterior nares. In the Amniota these become sunk into a recess in the roof of the mouth and in the higher Reptiles, as in the Mammals, this recess becomes shut off from the buceal cavity by a horizontal shelf which grows in from the side and meets its fellow to form the palate. How this has come about in evolution is illustrated by the three Lizards shown in Fig. 85.

In ontogeny the mode of origin may be similar,’ the palatine out- growths meeting and fusing with one another in the middle line (Crocodiles) or, as happens more usually, a median ridge or--septum extends backwards from between the primitive posterior nares: and the palatine processes meet and fuse with its ventral edge. In the two cases the physiological result is the same—-the shunting back- 170 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

twists upon itself, in such a way that points upon its ventral surface would move towards the embryo’s right side. (In other words the lung-rudiment rotates about its long axis in a counter-clockwise direction as seen from behind, its front end remaining fixed.) The

two lobes are the right and the left lung-rudiment but on account of

the rotation just mentioned which extends through more than 180° the left lobe at this stage represents what was originally the right side of the rudiment.

The two lungs of Lepiclcisiren or Prrotoptems are thus reversed in

A 5 C D

Fm. 96.-—-Dissections of mid-gut of L8})?:d()8t’I‘8‘?2- at stages 32 (A), 35 (B), 36 (C), and 37 (D), showing the modelling of the intestine and also the later stages in the development of the lungs. Seen from the dorsal side. ~

c.c, eloaeal caecum ; int, intestine; (.1, left lung; (Ii, liver; mun.d, Wolfllan duct; pan, pancreas ; ph, pharynx; r.(, right lung; sp, spleen.

position-—-the right lung of these forms being homologous with the left of other Vertebrates. An important detail is that in early stages the original right lung, '£.e. the definitive left, is decidedly larger than its fellow (Fig. 95, B). In later stages this inequality disappears, the smaller lung overtaking, the other in its growth (Fig. 96). .

In the ease of most individuals the lungs assume their dorsal position simply by growing directly tailwards, the oesophagus being pushed out of the way towards the left side (Graham Kerr, 1910). In certain specimens however, which doubtless in this respect retain I11 PH ARYN X 153

Ifeloderma. where they are the enormously enlarged sublingual glands.

Similar localized developments of the buccal glands occur in Birds and some of them may reach a great size as, for example, the enormous sublingual glands of the Woodpeckers.

PIIAI’.YN.\'.-—-The part of the alimentary canal which follows immediately behind the lmccal cavity is highly characteristic from the fact that in Vertebrates it is concerned with the function of breathing. The special organs which are developed to carry out this respiratory function fall into two groups one represented by the Lung‘——adapted for respiratory exchange with the atmosphere, the other by the Gills~—-adapted for respiratory exchange with gases in solution in the water. As the balance of probability is in favour of the latter being the more archaic they will here be considered first. .

The gills are seen in their most typical and familiar form in the various groups of Fishes where there is present upon each side of the pharyngeal region a series of visceral clefts—-slit-like openings lead- ing from the pharyngeal cavity to the extei-ior—-—separated from one another by masses of solid tissue known as the visceral arches or gill septa. The walls of the clefts are highly vascular and their surface is commonly raised into conspicuous plate-like projections- the respiratory lamellae —which serve to increase the area of respiratory tissue.

In the most archaic arrangement, seen in Elasmobranch fishes, the front lip of each cleft, except the first, is prolonged backwards to form a small valvular flap overlapping the external opening. In the Holocephali, Teleostonii, and Dipnoi the anterior one of these flaps, that projecting back from the hyoid arch, becomes greatly enlarged to form the operculum which overlaps not merely one but the whole series of clefts lying behind it. Correlated with this the outer portion of each succeeding septum, which in the Elasmobranch gave origin to its valvular flap, has disappeared, leaving only the portion lying next the pharyngeal cavity.

The cleft lying in front of the hyoid arch—-the spiracle is usually modified, its respiratory tissue having been reduced and even its opening being diminished in size or completely absent, but its general relations in the adult are such as to permit of no doubt as to its serial homology with the clefts behind it.

Most usually there are on each side six clel'ts——a spiracle and five branchial clefts~ —but there is reason to believe that there was a greater number present in primitive Vertebrates——seeing that the number of persistent clefts becomes on the whole less as one ascends the vertebrate scale and that here and there among the more archaic forms a greater number than the usual is found (Bdellostoma, up to 14, Notidanus cinereus 7, N. griseus 6).

In a few of the more archaic Vertebrates there develop during larval life, in addition to the visceral clefts with their respiratory 154 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

lamellae or internal gills, respiratory organs of another type——-—the external gills. As there is some reason to believe that these are more ancient organs than the gill-clefts they will here be considered first although they are much less familiar than the clefts with their internal gills. The branchial organs will therefore be considered in the follow- ing order: (1.) External gills, (II.) Visceral clefts, (III.) Internal gills. (L) Ex'1‘1«3RNAL GI[.I.S.—~Tl1e true external gills are organs which are commonly confounded with the ordinary or internal gills developed in the walls of the gill-clefts. They appear however to be quite in- dependent of these in their origin and they would probably have attracted more attention and interest than they have done had it not been for the fact that they occur in their typical form in only three subdivisions of the Vertebrates (Crossopterygii, Dipnoi, Amphibia) and that two out of these three groups comprise animals of extreme rarity, the developmental

mz_]V stages of which have not

been generally accessible

to emhryologists. 9-9-17 The typical External “C a W gill is a projection from ' ' the surface of the body - on the outer side of a

visc.eral arch. It con- sists of a core of mesen-

chyme with a covering Flu. 86.—-Diagrammatic longitudinal section through the (,f ectodenn; it is LI-a_

early rudiments of the external gills of Lepidosircn (Stage 25). versed by a vascular loop

e.g, external 1.',lll; end, endoderm; ma, \lHCel-‘ll arch; consistlng of ,the nlaln

m-, visceral cleft rudnm-nt. aortic avrcll Whlch P333353

out to its tip and then

doubles back; and it commonly has a pinnate form, paired projections

growing out so as to increase its respiratory surface. It is provided

with muscles by means of which the possessor is able to flick it sharply backwards so as to renew the water in contact with it.

The external gill as a rule is without any special skeletal support but in the larval Polypterus a short rod of cartilage projects into its base, and in the extinct Dolichosoma of the Gas coal of Bohemia there was apparently present a well-developed segmented skeleton within the substance of the external gills.

The external gill develops as an outgrowth from the tissue of the visceral arch at a period at which the clefts are not yet perforated. It arises as a bulging of the surface (Fig. 86) and in the author’s opinion the endoderm of the cleft rudiments takes no part in.its formation. At the same time it is only right to state that the pre- valent opinion in the past has been different. The outer surface of the visceral arch in the region where the external gill will develop is covered by a layer of cells thicker than the neighbouring ectoderm, and in some cases this thickened portion of the ectoderm shows in its

e.g.I There is however no definite evi-

III EXTERNAL GILLS 155

deeper portions a rich deposit of yolk, so as to look exactly like the yolk-laden encloderm. Grcil explains this appearance by supposing that true endoderm cells actually spread outwards and replace the deep layer of the ectoderm, so that the external gill-rudiment would be partly endodermal in its nature.

dence of any such process taking place and the present writer would interpret the appearances as mean~ ing simply that the ectoderm cover- ing the external gill-rudiment becomes thickened, and stores up a supply 01' yolk‘ in its deeper layers, as a physiological preparation for the active processes of growth which are about to take place as the external gill rapidly increases in length. In this he agrees with Marcus (1908).

The general appearance of the developing external gills is well seen in Hypogcopms (Fig. 87) or in Lepidoswlren (Fig. 200). In Lepvlolosiren there are present four B‘.1<_:, 37.---Hypogeophis eIul)i'y0s showing upon each side of the body. At ‘l3’,°1?1§“°“t_ ‘if89}}‘“ “"“""““l gm“- first the four are quite independent ( W m“’_ ") _ of one another but as development .,.;-;;ii;...;.;‘l:;1i:,l.‘.‘,‘.. ""‘«i~§.. ’.’.;...§i?{Z.‘{‘ ..“.f.§1‘,‘..‘ ...if.’£; g0(-3S 011 they b£‘.COII18 raised UPOII EL projecting in Bfi-mu the hyoid 8.I‘(‘ll, and also conlu-1011 base SO as to give the from the mandibular arch in front of it, are

__ . _ . p0ssil)l_\' u-xiurnal gill rudiments which do not 3:PP93—T3'l1(39 of 3' 3111819 Organ wlth go on with their development.

four branches (Fig. 200, B-E). The distribution of true external gills amongst the main groups of Vertebrates is shown in the following table:

1

,—-.-—-q-——.._.—_.__—j__..._ . __ - .. .- ._ . ...--..- -.

\

l 3 V I. II. III. I\'. ‘V. ‘ ' VI.” ' iscvral .\l'L'lI. ' _ . . . l-‘irsl ' .\'.4-Hnltl 'l‘ llI'( u Four‘: M‘l'"1lb“l‘w‘l Hymd‘ Jlr:1m-hi:ll. Iii‘.-lnuliinl. 3 Bram-hinl. 3 ll:'.'ui(.-lii:Il.g Elasmobranchii. . ; Crossopterygii . . 5 x . lhpnoi. . . . g x x x x Amphibia . . . - 'v.*" 2:. x y x x i Amniota . . ' i 4 I 1

  • r:..\'o'sLi_~,'iul.

In those animals in which they are well clovoloped the external gills are for a time the main functional breathing organs. They are 156 EMBRYOL()GY OF THE LOWER VERTEBRATES CH.

richly vascular and the renewal of the water in contact with their surface is provided for by a well-developed muscular mechanism by which they are sharply flicked from time to time, or, in early stages, by rich ciliation ol"tl1eir surface as in the Frog (Assheton, 1896) or 6'73:/ptolzramz/ms (Smith, 1912). They are as a rule merely temporary organs. As the respiratory function comes to be sufficiently per- formed by other organs their circulation becomes sluggish, their tissues moribund. They become invaded by leucocytcs and eventually unclergo complete atrophy. in .l’o~otopm~us distinct vestiges persist for a prolonged period while in various Urodeles they remain func- tional throughout life.

The external gills, highly vascular and projecting freely into the surrounding medimn, present tempting objects for attack by other organisms. They are therefore extremely liable to injury, and cor- related with this they present a high power of regeneration. in correlation also with the same fact we find that they tend to be eliminated from development in certain members of groups which are as a whole characterized by their presence. Such is the ease in the Amphibia where they are characteristic of the group in general but where in particular cases they are reduced (II;z/la n;'rb0'rea) or com- pletely absent (}>’ovmb'mator) although we must believe they were present in the ancestors of these forms.

This tendency for the external gills to become eliminated from development in the process of evolution raises the interesting morpho- logical question: were External Gills at any period more widely dis- tributed amongst Vertebrates than they are at present? And, if so, are their vestigial representatives still to be found in any cases where they no longer develop as functional respiratory organs?

This interesting problem, which offers an inviting field for research, has not yet had sufficient attention devoted to it. Even if it were the case that external gills once existed in the ancestors of forms in which they are no longer present as functional organs there is always the possibility if not probability that their disappearancehas been so complete as to leave no observable trace. Nevertheless such vestiges might persist and are worth looking for.

Under these circumstances it is of interest to note that already certain structures are known which are interpretable as vestiges of once-present external gills. Thus in Gymnophiona what appear to be transient rudiments of mandibular and hyoidean external gills make their appearance during development (Fig. 87, B). Again in the case of the Mandibular and Hyoid arches of Urodeles, on which no functional external gills develop, Driiner (1901) has found what appear to be vestiges of the muscles of external gills. Again in the larvae of various Urodeles there occurs in connexion with each mandibular arch a curious styliform projection known as the balancer, from the fact that the larva balances itself upon them as upon a pair of limbs (Fig. 88, b). Each of these has a vascular loop within it and it in fact appears to be the modified external gill of III . EXTERNAL G-ILLS 157

the mandilmlar arch which has lost its respiratory and taken on a supporting function.

While external gills occur within three main subdivisions of the Vertebrates, namely Teleostomatous fishes (Crossopterygians——the most a.rchaic of existing Teleostomes), Lung-fishes, and Amphibians, there are two main groups-—Elas1nohranchs and Amniotes---in which they are conspicuous by their absence. Having regard to the tendency of the organs in question to disappear (as in the cases already alluded to amongst the Amphibia) their absence in a special group would not in any case constitute strong evidence that they were never present in the ancestors of that group. As it happens however there is in the two groups mentioned a definite cause which seems quite competent to account for the dis- appearance of external gills, namely the de- velopment of'_ a new organ —— the yolk - sac with its highly developed vitelline network of blood-vessels»--which in addition to its primitive

function Inust neces- 88.%l‘hii'eie larval (_lt:l't'l()})lllt‘lll. of a ‘l'l(f\\'loW

sarily also function as it famiu/us) as seen from above. (After Egert, very efficient organ of '

respiratory exchange and what looks like :1 posit-rior 4-..\'tc-rnal gill is the ]w(:L-()1‘fll limh. SO render 311)’ Pre'eX-1st‘ In l"ii-_:.s'. ll and (l flu-1-Xternal _«_;'ill:~' lmve l)l',‘(‘ll cut away leaving ing respiratbry organ no only tll(‘ll,'l)-‘mill .~'i-urnps.

longer necessary.

Taking into consideration the presence of external gills in three archaic groups of Vertebrates it seems to the present writer to be clearly indicated that these organs are a very ancient characteristic of the Vertebrate phylum. The only alternative indeed is to regard them as having become evolved independently in the three groups in which they occur. It is diflicult to accept this as in any way probable having regard to the similar morphological relations of the organs in question.

It might be suggested that somewhere on the course of a large blood-vessel, such as an aortic arch, would be a most natural place for the development of a new respiratory organ. Such a suggestion however is entirely fallacious for simple physical reasons: for new breathing organs will tend to become evolved -not on the course of a

b, lnilaiurei-; !'.§I,i'_\t91‘l1:ll gillol'lir.-1. ln'anchial:1rch. In l«‘i_«,v-. A ' 158 EMBRYOLOGY OF THE LOWER V ERTEBI-LATES (311.

large vessel where the quantitative relation of surface to volume in the blood-vessel is at its minimum but rather where there is present a rich superficial network of capillaries, in which the ratio in question is at its maximum. .

(IL) VISCERAL CLEFTS. --The visceral clefts develop in what appears to be the most archaic method in Lampreys and Elasmo- branehs Where each arises as a lateral pocket (visceral pouch) of the pharyngeal wall which meets and fuses with a., much shallower, ingrowth of the ectoderm, the apposed portion of cndoderm and ectoderm breaking down so as to bring about a free communication between pharynx and exterior. Each cleft thus consists of a, usually much larger, inner portion lined with endoderm and an outer portion lined with ectoderm.

The most frequent type of modification of this probably primitive mode of cleft development is that so usually met with in the develop- ment of hollow organs, namely that the cleft-rudiment, instead of being a hollow pouch from the beginning, is for a time in the form of a solid lamina of endoderm, which only at a later period develops a cavity in its interior and becomes an open cleft. This modification is found in Teleostomatous fishes, Lung-fishes and Amphibians.

111 the young Elasmobraneh the gill-clefts are at first long slits "traversing the whole dorsi-ventral extent of the lateral wall of the pharynx. Each septum or arch grows back at its outer edge to form a valvular flap overlapping the cleft next behind it. In most cases this backgrowth fuses with the next septum at its dorsal and ventral ends so as to reduce the external opening of the cleft to a compara- tively small dorsi-ventral extent.

In all Gnathostonies, excepting the typical Elasmobranehs but including the Holocephali, the hyoidean backgrowth becomes greatly enlarged to form the operculum which overlaps the whole series of clefts behind it. Correlated with this the outer portions of the sub- sequent septa with their backgrowths become reduced. I11 these cases we frequently find a marked tendency for the edge of the opercular backgrowth to become fused with the body so as to restrict the size of the opening behind it. Thus in the Eel the opercular opening becomes reduced to a small persistent ventral portion, while in S3/mbmncltas the same holds but in this case the two openings have fused together to form a small ventrally placed median

ore. P A similar condition to this occurs in the tadpole of Discoglossus while in other Anura the persisting opening is displaced to the left side. Finally in Amniotes the fusion of opercular margin with body- wall takes place along its whole extent so that the branchial region becomes completely enclosed (see Chap. X.).

SPIRACLE.-——The spiraele or hyomandibular cleft always shows a considerable amount of modification. In Elasmobranehs its dorsal portion alone becomes perforate, although fusion of the pouch with the ectoderm takes place throughout its whole dorsi-ventral extent. .the Amniota the distal portion of the

I I r GILLS ' ' _ 159

hespiratory lamellae develop only on its anterior wall and these, as development proceeds, become vestigial forming the pseudobranch. In Teleostean fishes the spiracular pouch (Fig. 89 A, cc. I) flattens out and disappears (Goette) so that the pseudobranch (pa) on its anterior wall comesto lie on the inner face of the base of the operculum and appears to belong to the second cleft (Fig. 89, B). In Lung-fishes the soli.d endodermal rudiment never becomes perforate. It becomes gradually reduced during development while "its outer ectodermal portion becomes, as already indicated, converted into a special sense-organ. In Anurous Amphibians and in

cleft rudiment becomes greatly dilated to form the tympanic cavity, while the proximal part forms the relatively narrow Eustachian tube.

Just as the varying condition of the spiracle indicates a tendency for this cleft to undergo reduction so a similar but still more marked tendency exists for the gill clefts to become reduced at the other (posterior) end of the series. This is illustrated in the first place by the reduction in the number of functional clefts seen in passing from the lower Vertebrates to the higher. It is also frequently manifested in developmental stages. Thus 81110118317 the Amphibia we find Flu. 89.—-Horizontal sections through that in the Gry1llI'l()pl1l0Ifl& (Hyp0g(3- Salmon embryos explaining position Ophis, Marcus) 3 rudilnentary 7th cleft of pseudobranch. on inner surface of

_ . . operculum. (Atter (Joctte, 1901.) makes its appearance though it never _ ' L. ‘ reaches the eehederm, while the 6th ...;i;Z'.'..i‘.i1'.?."i...:f:I?f:...:f:f:...?:II%‘:'§1..?鑧?'.;....:iZ.; lS 0p9Il £01‘ 3. time. III UFOdBl8S EL l and II; II;/,l1_yoi«l ar«.'.l1; -Ti-, ope-rculum; rudiment appears and is for a time :"{"\"i"“l'jl‘-I3"Cf:-¥.g1*ll1tl'3'IIx2 1»-'vwlobw'=tnc1»; connected with the ectoderm but does °’ W” (T ' not become perforate, while in Anura this cleft appears only as a small and transient rudiment which never reaches the ectoderm.

(III.) INTERNAL G1LLs.——’_l‘he internal gills or respiratory lamellae arise as ridge-like or, at first, finger-like projections of the cleft lining. The chief matter of dispute regarding their development has been the question whether they belong to the endodermal or the ectodermal portion of the cleft lining. In cases where, as frequently happens, the lamellae begin to develop after the cleft is completely formed, the appearances are sometimes in favour of the one sometimes in favour of the other interpretation. Goette (1901) in fact goes the length of regarding the lamellae as being of endo- dermal origin in the case of the spiracle and ectodermal in the case 160 EMBRYOLOGY 0 F THE LOWER Vl1‘.lt"El3l\’.A'l‘l+]S (‘.11.

of the succeeding clefts, so that the spiracular pseudoln-ancli would on a strict interpretation of the germ-layer theory not be serially homologous with the other gills.

In the present writur’s opinion, as already indicated, such ul)S61‘- vations upon the first origin of organs which develop in the region of the blurred boundary between two layers are not to be taken as afihrding evidence ol' any serious importance in regard to the morphological nature of such organs. Greater weight however seems due to evidence obtained from cases where the hrst traces of gill laniellae are visiblq; at a period before the bounding inmnbrane of the cleft is ruptured, when the cleft consists still of two distinct pnnches—ene eetoderinal, the other endodermal——separatcd by a still eeuiplete partition. Such is the case in Aci_pc'nscr and (ioette shows that in this case the laurella-rudiments arise outside the

partition from what is undoubtedly an ectodermal surface (see Fig. 90, g.l).


Pl’ :3" '|‘he same discussion extends to the ' general lining cl’ the cleft~—as to how

go. much of the lining of the adult cleft is

/ ectodermal and how much endodermal.

-7" }octte and Morofl'(1902) hold that only

|"1u.90.—~ll0rizontal:-.m~1ionthrough the portion of Lhe cleft -in the innue- bmwhial reg.“ M. ymmg AOL d1ate_ IlBlg'lll)Olll‘l100(‘l of its pharyngeal peust-r showing the ('('f()de‘[‘[[]a1 opening 18 to be regarded as endodermal, <(>‘I3:.:':It1e01'1f)1(I)*51s)i1l1am011ne- (Atter all therest. being ectodermal. But here ‘ ’ ‘ ° again 11] view of the blurred character l.ll'iiI"‘ll‘.'ll”,Iiill,:i|l\(ill«l:ii(ill?:i:;‘,]ii;:.:iI('lii.llfllll: (.)f the boundary betvlreen the two layers p;,, ..,...._,. .,,~,,1...,_,..x_ it seems hardly profitable to speculate on the matter.

In certain fishes the gill-lamellae are for a time prolonged out- wards into long threads which project through the cleft opening into the surrounding fluid. Such is the case in the embryos of F.lasn1e- branchs, in which it is only the lamellae upon the posterior face of each arch that become prolonged, those on the anterior face not projecting beyond the edge of the septum. Eventually the pro- jecting part of the filament disappears while its attached basal portion becomes the definitive lamella. In a few Teleosts a similar temporary modification of the lamellae takes place ——~perhups the best example being Gymnarclms (Budgett, 1901; Assheton, 1907. See Fig. 199).

EVOLUTIONARY HISTORY or rm-1 BRANLIHIAL RESPIRATORY ()RGANs.——-As regards the early evolutionaryhistory of these branclnal respiratory organs one very generally accepted View looks upon the visceral clefts as being the most primitive, the internal gills as having developed next, and the external gills as being due to secondary extension of respiratory tissue outwards from the clefts. It seems however, bearing in mind what we now know regarding the development and distribution of external gills, at least equally ii’ llnl. III LUNG 161

more probable that the evolution of these organs has been in the opposite direction.

On this latter hypothesis the external gills would be regarded as the primitive respiratory organs, inherited probably from pre- vertebrate ancestral forms. The evolution of clefts between their bases would be explicable as an arrangement for pumping water over the surface of the external gills, while it could be readily understood that the respiratory tissue would then tend to spread inwards along the lining of the clefts, where it would be both advantageously situated for carrying out its breathing function and, at the same time, protected from the dangers to which external gills are exposed. The development of respiratory lamellae to increase the area of this respiratory tissue on the wall of the cleft would be a further and natural development.

The chief difficulty in the way of accepting this as a working hypothesis lies in the existence of animals admittedly near the base of the Vertebrate scale—such as Amp/2/ioxus and the Cyclosto_ mata-—in which there are no external gills and no vascular yolk-sac to account for their disappearance. This difficulty is undoubtedly a serious one but on the whole the present writer is inclined to think the difficnlty is not so great as to justify the immediate rejection of the hypothesis: it becomes less formidable when it is borne in mind that the forms mentioned although evidently archaic in some of their characteristics bear in others equally convincing evidence of high specialization. _

LUNG.—-In all the groups of Gnathostomata excepting the Elasmo- branch fishes the pharyngeal wall develops a great outgrowth which, as will become apparent later, is to be looked upon as home- logous throughout the series and as primarily respiratory in its function-——the lung. The lung appears in its most familiar and typical form in the tetrapod Vertebrates and its development in these will accordingly be considered first.

Here in an early stage of its development the lung is in the form of a pocket of the pharyngeal floor projecting downwards in the mid—ventral line. This pocket commonly makes its first appearance as a longitudinal groove or gutter in the floor of the pharynx at about the level of the last ‘visceral cleft. The groove becomes constricted off from behind forwards, so as to form a blindly ending pocket communicating in front with the pharyngeal cavity by a narrow opening—the g‘lottis—and extending back immediately ventral to the pharynx. The blind end of the pocket grows actively tailwards and becomes deeply bi1obed—-—the two lobes becoming respectively the right and left lung, while the unpaired portion connecting them with the glottis becomes the trachea or pneumatic duct.

While the lung passes in its early history through stages corre- sponding on the whole with those described there are differences in detail in different groups-—-the most conspicuous of these variations

VOL. II ' M 162 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

being, as is so often the case in the development of hollow organs, that the rudiment is at first solid and the cavity appears secondarily in its interior. This is the case in various anurous amphibians and in Jlepiolosofirevz and .1’-r0t01ate'/"as.

It has been indicated that the lung is primarily a ventra.lly placed pocket of the pharyngeal wall, that is to say its wall is a portion of splanchnopleure. It follows that the cavity of the lung is lined by endoderm while its outer layers (connective tissue, blood- vessels, muscles, etc.) are composed of splanchnic mesoderm.

As regards the further development of the lung, the main steps are concerned with its respiratory function and have to do with the increase of the respiratory surface. In such an animal as the Newt, where the lung retains a relatively primitive condition, the endo- dcrmal lining grows equally as the organ increases in size, so that even in the adult the lung has the form of a simple sac with smooth endodermal lining. In a Frog or a Lizard, however, growth activity is specially marked at particular spots so that at these spots the cndoderm forms outward bulgings into the covering of splanchnic mesoderm.

In these Sauropsida in which the pulmonary apparatus reaches its highest degree of evolution (Tortoises, Turtles, Crocodiles and Birds, in an ascending series) these pockets of the endodermal lining become more and more extensive, and more and more com- plicated, so as to give rise to a thick spongy mass, which forms the bulk of the lung, surrounding the now relatively small clear central space. The latter, forming as it does an apparent continuation of the bronchus or paired portion of the trachea, is spoken of as the intrapulmonary bronchus. Further the respiratory function becomes concentrated towards the terminal portions of the pockets, their proximal portions forming simply conducting channels-— branches of the intrapulmonary bronchus.

In the Chameleons, towards the end of development, a number of the endederm outgrowths bulge out beyond the general level of the surface of the lung upon its ventral side. These persist in the adult as large diverticula which when the animal blows itself out are inflated with air. In the embryos of Birds similar outgrowths make their appearance, four from each lung, but in this case as development goes on the outgrowths continue to increase in size and form the characteristic air-sacs of the adult bird.

THE LUNG or BIRDs.—-—As the Birds, in correlation with the intensely active metabolism as indicated e.g. by their high body temperature, stand pre-eminent amongst Vertebrates in the high stage of evolution which has been reached by their lung, the onto- genetic development of this organ will be followed out in a little more detail (Moser, 1902; J uillet, 1912).

In the Fowl the pulmonary diverticulum of the pharyngeal floor makes its appearance about the beginning of the third day. By the end of this day the rudiment is bifurcated at'its hind end, each lobe III LUNG 163

being the rudiment of a lung in the restricted sense and containing a prolongation of the enteric cavity lined by tall columnar endoderm cells. Outside the eiidoderm is a thick layer of inesenchyme and this in turn is covered by columnar coelomic epithelium.

The endoderm-lined cavity is destined to become the main intrapulmonary bronchus—-the mesobronchus. This remains un- branched until the fifth day when its cndoderm begins to bulge out, near the point where it enters the lung, to form the first ento- bronchus. During further development a. series of three other entobronchial outgrowths sprout out from the external surface of the inesohronchus close behind the first outgrowth. The four ento- bronchi so arising are closely contiguous and form a longitudinal row (Fig. 92, El-E4).

A set of similar outgrowths make their appearance spaced out along the mesial side of the mesobronchus posterior to the ento- bronchi: these are the rudiments of the ectobronchi. A third set of outgrowths on the lateral 0 side of the mesobronchus ejcf. are the rudiments of the Z‘ small secondary lateral bronchi (Campana). Of these sets of outgrowths the first and second are the most important and they are arranged in a slightly spiral row along the wall of the meso-

51: bronchus.

The mesobronchus, as FIG. 9l.—_Diagraiii illiistratiiig the arrangement of the it grows in length main air-passages in the lung of the Fowl as seen 3

h b from the mesial plane. (After J uillet, 1912.) assumes a Somew a ' l(’ is‘ c .. uni‘ an eii'.0i« '- m-shaped curvature. by M’ l'its?‘.1...;o§i3o:.:iii§?',..i,-,',....r:£.,.;~.)i.¢l.i.m" which the Group of ecto- ~

bronchi are: carried towards the (1'lO1‘Sa.fl facéa fof the lgng while the entobronchi are nearer the ventra sur ace c . Fig. 91 . Both ecto- bronchi and entobronchi grow rapidly parallel with and close to the surface of the lung-rudiment. They soon produce secondary branches as projections of their walls and these secondary branches increase greatly in length traversing the substance of the lung at first close to its median surface and, later, deep down in its sub- stance as well—-—the eiitobronchial branches growing in a dorsal and the ectobrauchial in a ventral direction.‘

The two sets of branches fits their t1% 1E:p‘pI‘01f1it(3l1 1(l)I1e another Iarg seen to alternate in position ( ig. 91). en t ey ave approac e closely each branch bifurcates and its two tips become closely apposed to the two tips belonging to the other serieswhich lie closest to them. About the thirteenth day these apposed tips become completely fused and their cavities continuous so that there is now

I/I///‘I/l-:’I"'.. T '

//((!l{!)ll‘Z‘llE};'; 164 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

established a series of channels running in a dorsiventral direction through the substance of the lung aml communicating dorsally with the ectobrcnchi and ventrally with the entobronchi. The channels in question are termed parabronchi (Fig. 91, par). These are embedded in an abundant matrix of mesenchymc which from about the tenth day becomes divided up into more or less prismatic masses each having in its axis an individual parabronchus—the prisms being delimited from one another by the development of intervening blood-vessels. The mesenehyme which constitutes the inner portion of this sheath round each parabronchus becomes later replaced by a layer of smooth muscle fibres.

At about the same period as the fusion of the parabronchial tips takes place, the Wall of the parabronchus begins to grow out into numerous little pockets arranged in radiating fashion. These extend outwards, perforating; the muscular sheath, and at a short distance from the parabronchus divide into branches which in turn elongate and become the air-capillaries of the fully developed lung. Judging from adult structure it would appear that the tips of these fuse with others to form the continuous air-capillaries so that the latter would be formed much in the same way as the parabronchi but it has not been possible, so far, to demonstrate this by actual observation.

The essential features of the development of the Bird’s lung as above outlined may be summed up in the statement that in this type of lung the diverticula of the intrapulmonary bronchus, which in other Vertebrates end blindly, become here joined together tip to tip to form continuous tubular channels. To allow this arrange- ment to function efficiently an apparatus is needed to force the air throu h the system of respiratory tubes: such an apparatus is provi ed by the air—sacs.

AIR-SACS.-—-The ventral part of the lung-rudiment is for a time formed of a thick mass of mesenchymatous tissue which has been termed by Bertelli the primary diaphragm, from the fact that it becomes continuous along its lateral margin with the side wall of the splanchnocoele, so as to form a kind of floor separating off the lung from the splanchnocoele which lies ventral to it. The air-sacs arise as outgrowths of the bronchial cavities and are on each side four in number: the first or most anterior giving rise to the cervical sac, the second by bifurcation to interclavicular and anterior thoracic sacs, the third to the posterior thoracic and the fourth to the abdominal sac. The rudiments sprout out into the substance of the primary diaphragm and become greatly distended within it, bulging out ventrally amongst the viscera so that the ventral layer of the diaphragm becomes stretched ‘out into a thin membranous wall delimiting the cavity of the air-sac on its ventral side. The dorsal part of the primary diaphragm, lying above the air-sacs, persists as the floor of the lung or secondary diaphragm (ornithic diaphragm of Bertelli, pulmonary aponeurosis of Huxley). III T AIR-SACS 165

The air—sac rudiments sprout out (Fig. 92) from the main pulmonary cavities-—the cervical from the first entobronchus, the interclavicular and anterior thoracic jointly from the third ento- bronchus, the posterior thoracic and the abdominal from the meso- bronchus. Later on additional secondary communications between the air-sac cavity and the pulmonary cavities are established (except in the case of the cervical air-sac) by means of the recurrent bronchi of J uillet. These arise in the ordinary fowl about the tenth day of incubation in C3,. the form of outgrowths of the wall of the air-sac either near its tip (interclavicular and anterior thoracic) or just before it emerges through the general surface of the lung (posterior thoracic and abdo- minal) as shown in Fig. 92.

These outgrowths burrow into the superficial layer of the lung, branch and become joined up, in a manner the details of which have not yet been worked out, with the system of parabronchi. The communications are visible in suitable preparations of the adult lung as groups of openings, each group leading in into the lung from the appro- /0’ ./ priate air-sac——those of the interclavicular and anterior 05- thoracic lying towards the FIG. 92.——])iagranuuatic view of the right lung of lateral edge Of ’Dl]6 ventral a Fowl embryo of the tenth day as seen from

surface of the lung, about the “:9 V°‘:"“‘(j{%:éri11;1::fi%::i'1s1 ;>1'is_iI{Ihe0fflt)1l:<; . a r-sac . c '-, ~ - level of the attaclllllent of entobronchi are shaded.

the bronchus’ and those of rib, abdominal air-sac; at, anterior thoracic air-sac: the POSl73ri0r th0ra»0i0 and car, cervical air-sac; 14."! and 164, llrst and fourth ento- abdonlinal sacs near bronchi; tc, iiiterclapicular air-sac‘; -nies,tn:)¢sst)ll;1;otrl1sch1is; 

     pl, pUHl3('3I'10I‘bl'|0I‘8a('alL fllI"8{lC, T, I‘l,LllII‘0-ll P01. 1 ...

close to the direct opening between it and the corresponding air-sac. It would appear that the function of these recurrent channels is to conduct the air forced out of the air-sacs in the expiratory effort through the system of air-capillaries, the muscular coat of the parabronchi doubtless playing an important part in directing the passage of the air through the system of air-capillaries rather than through the parabronchi themselves. a The formation of the air-sacs does not exhaust the remarkable

proliferative powers of the wall of the lung in Birds. Further out-

III A IR—‘I'._LA DDER 167

FIG. 93.-—-Development of the air-bladder of n Teleost. (After Moser, 19,,4.)

A, Jmodeus, 5 mm., longitudinal section; B, Rh-Od¢'ll.$', 6 mm., longitudinal S(‘(!U()lI2 (.‘., Rlmdemz, 7 mm., trans-vt-rse section, showing small pouch-like mxtgrowtli of pneumatic duct; uml, emlu«lu'r1|1; cut, enteric cavity; 2, uir-bladder; Ii, liver; N, notochord: mt, pronephric chmnbur; p.41, pm-.Iu1m.tic duct; '_l/, yolk. 168 EMBRYOLOGY OF THE LOWER VERTEBRATES (in.

to form a kind of diaphragm perforated in its centre and capable of being thrown into vibration by air being forced from one chamber into the other so as to function as a sound-producing organ (e-._g. Gurnards). Other outgrowths may develop: thus for example in many Siluroids numerous branched projections are formed along each side of the air-bladder.

The air-bladder rudiment is at its first appearance in some cases approximately dorsal in position (Selma). In Jihodeus Moser (1904) has shown that the diverticulum is at first on the right side of the alimentary canal. The same observer found that during the early stages of development of the air-bladder the portion of alimentary canal from which it springs undergoes a process of rotation about its long axis in such a direction that a point on its dorsal surface is carried towards the left side.

Although the actual development has been worked out only in a few cases, we may infer safely from the adult relations (Rowntrce, 1903) that the amount of this rotation differs greatly in different

.members of the group Teleostei. Thus in Siluroids and Cyprinodonts

the glottis or pharyngeal opening is in the adult still to the right of the mesial plane; in others such as the genera 0smer'us, Olupea, Olwrocentrus it is practically median; in still others such as Mormyrids, Characinids, Gymnotids and Cyprinids it has passed the mesial plane so as to lie upon its left side, while in the case of the Characinids Jllacrodon, Erythmlnus and ]}r’b'ias'i'na the glottis has come to be completely lateral on the left side. This rotation of the gut in the region of the glottis is of much morphological importance as will be shown later.

In the young Rhodeus, 7 111111. in length, Moscr finds that a well- marked diverticulum from the pneumatic duct is present (Fig. 93, 0). Later on it gradually disappears. A similar diverticulum occurs in Salmo and in the Carp, and in all probability in numerous other Teleosts: its morphological significance will be discussed later.

ACTINOPTERYGIAN GANOIDS.——In these fishes the development of the air-bladder takes place on similar lines to that described for Teleosts. In Amda the additional detail has been made out that the rudiment is at first in the form of a longitudinally placed groove which becomes constricted off from the alimentary canal from behind forwards just as frequently happens in the case of the typical lung- rudiment of air - breathing Vertebrates (Bashford Dean, 1896; Piper, 1902). A rotation of the section of alimentary canal in the region of the glottis takes place similar to that which occurs in the Teleost.

LUNG-FISHES.-—In the adult Oeratodus an organ occurs which is equally lung and air-bladder. It forms an unpaired sac lying dorsal to the splanchnocoele just like a typical air-bladder, but the pneu- matic duct, instead of opening directly into the alimentary canal dorsally, passes round the right side and opens by a ventrally placed glottis. In Lepidosiren and Protopterus the general arrangement is m i LUNG _ 169

the same except that here the organ is deeply bilohed: a right aml a left lung or air-bladder occupying the place of the single organ of 0'e'ratodus.

The meaning of the ventral position of the glottis in these Lung- fishes, and, in fact, the morphological nature of the whole organ, is


Flo. 94.--Transverse sections through the endoderm of the pharynx showing an early stage in the development of the lung.

A, Polypterus, B, (}'era,tmIu.,g, and O, Bmn..h1',nato1' (O aTl5er Goette, 1875). 1, lung-rudiment; ph, pharynx.

demonstrated by the examination of early stages in development. In these the organ is found to be a perfectly typical lung-rudiment (Fig. 94, B)-——a mid—ventral projection from the pharyngeal floor of precisely the same kind as that found in te_trapodous vertebrates (C).1

Fm. 95.——Views showing early stages of the lung-rudiment of Protopterus as seen from the ventral side (stages xxxii, xxxiv, xxxv).

e.g, external gill; I, lung; oes, oesophagus; pan, dorsal pancreas; ,2. f, pectoral limb; Th, thyroid ; v.c, visceral cleft rudiment. (Cut surfaces are inclieatml by uniform light tone.)

Subsequent stages are illustrated by Figs. 95 and 96. The lung rudiment at first a rounded knob (Fig. 95, A) grows backwards and soon becomes bilobed (B). The figure does not bring out one im- portant fact namely that the lung-rudiment as it grows backwards

1 The projection is at first solid in the case of Lcpvidoseren and Protopter-us. III CEMENT-ORGANS . 179

head on each side as shown in Figs. 100, A, and 197, C, 0.0. A longj- tudinal section through the centre of the organ at about this stage (stage 26, Fig. 101, E) shows that the organ is covered hy the ordinary 2-layered ectoderm. Round the lip of the opening at its

Flo. l0l.——Illustrating the development of the cement-organ of l’oly_pterus. B represents part of a transverse section, the other figures portions of horizontal sections.

A and B, stage 20; C, stage 23; D, stage 24; E, stage 26. mo, cement-organ. The darker tone indicates ectoderm.

free end, the superficial layer of ectoderm stops, while the deep layer seems to dip down as a deep involution to form the secretoryepithelium (c.o) which lines the cavity. All the appearances seem to point to the secretory epithelium being ectodermal in its nature. How deceptive these appearances are will be gathered from an inspection

of ‘ig. 101, A-E. III LUNG 171

the archaic mode of development, the lung-rudiment (Fin. 97, Z) describes a spiral curve round the oesophagus so that the bifurcated

FIG. 97.———Porti0ns oi‘ l.l‘{Ll1SV8I'S0 sections through :1 Lepiulosiren larva (stage 34) to illustrate the eli:u1gin;_:' relations of lung to gut from at short distance behind the glottis l2tliW:ll'1lH. In .\ l.h«- lung is ventral to the :Llirn(-.ntary canal _; in B it is directly to the riglit ; in (3 it has lm_-mm: displaced dorsally ; while in D (where it is commencing to bifurcate) it has come to he llll(l-(iflrfial in position.

.4, aorti; gt, glomerulus ot'pron«_-phros; I, lung; N, notochord; ues, oesophagus.

hinder end of the rudiment, which will give rise to the lungs in the restricted sense, comes to lie dorsal to the alimentary canal. ~ The lungs continue their tailward growth in the substance of the 172. EMBRYOL()GrY OF THE LOWER VERTEBRATES OH.

dorsal mcsentery (Fig. 97, 1)) but eventually the portion of this mesentery containing the lung and dorsal to it becomes greatly thickened from side to side and finally merges completely in the roof of the splanchnocoele, so that in the adult condition the lungs lie completely outside the body-cavity——between it and the vertebral column.

In Uemtodus (Gregg Wilson, 1901; N cumayr, 1904) the lung is at first, as in the other two lung—fishes, ventral in position (Fig. 94, B) but in this case the originally left lung, which in Lepidostrevz, and I’7"utopte'rus is for a time during development reduced in size, seems to have disappeared almost entirely, being represented only by'a small and transient rudiment. Further detailed studies of the early stages in the development of the lung of Uemtoclus are much needed to make clear the origin and fate of this vestigial left lung. But it seems clear from what is already known that the monopncumatic condition of Ceratndlzzis has come about in evolution through the suppression of the originally left lung.

As the lung completes its development, its cavity becomes en- croachcd upon by two median longitudinal ridge-like ingrowths, one dorsal and the other ventral. It used to be supposed that these marked an incipient division of the l11ng into a right and a left half so as to bring about the condition seen in Leptdostren or Protopter-as —the monopneumatic condition being supposed to be the more nearly primitive. It will have been gathered from what has been said that this point of view is no longer tenable and that the n1ono- pneumatic condition of Cemtoalus is to he looked on as secondary and not primary.

CROSSOPTERYGIANS. — Of the two surviving examples of the Crossopterygian ganoids—the most archaic existing members of the Ganoid-Teleostean stem—a few stages in the development of the lung have been investigated in Poly/pterras (Graham Kerr, 1907). In the earliest stage observed the lung—rudi1nent was in the form of a mid- ventral groove formed by an outgrowth of the pharyngeal lining (Fig. 94, A, Z). This groove becomes deeper and towards its posterior end widens out ventrally so as to have a .L-shape in transverse section.

Posteriorly the lung-rudiment grows back into a pair of horn-like projections——the rudiments of the right and left lung. These extend backwards in the connective tissue of the splanchnopleure and they very soon show a marked inequality in their rate of growth the left lagging behind the right. As growth goes on this inequality becomes more and more marked, so that in a larva of about 30 mm. in length the right‘ lung extended right back to the cloaca while the left pro- jected back only about 3 mm. behind the glottis.

In these later stages another important feature is to be noticed, one which is correlated with the fact that the air-filled lung neces- sarily acts as a float in an aquatic animal. This feature is that the lung tends to assume a position symmetrical about the median plane. Thus in the anterior region where both lungs are present they are m AIR-BLADDER 173 ,

situated laterally, balancing one another, while farther back where only the right lung is present this shifts towards the mesial plane until it is symmetrical about that plane, lying in the dorsal mesentery (Fig. 98, A and B).

EVOLUTION on THE Am-BLADDER.-—-'l‘he facts that have been enunciated above, with regard to the development of the lung in Dipnoan and Crossopterygian fishes, are of much morphological interest. When pieced together with what has been said regarding the development of the air-bladder of Teleostcan fishes they afford data from which the evolutionary history of the Teleostean air- bladder can be traced out with a high degree of probability. That history may be stated in a few words to have probably been as follows:

1. The primitive condition was that of a lung, communi- eating with the pharynx by a ven- ' trally placed glottis ——-for we have seen that the‘ embryonic rudiment of the organ in the most archaic forms pos- sessing it is a typical lun,r_f-rudiment.

2. The organ became bilobed, growing back into a

right‘, lung and a, left FIG. 98.-—S_ections through the lungs of a larva of hula. Polypterus 30 mm. in length. ,__,.

'3_ In the for-Ins 1 f1:,1lnO!'O1l;llbeI'€0I‘l; Ba more postplrior; 1.4, aorta; mg, enteron ;i Ll, . . e ung; no 00101‘ ' opn Opls xonvp nos: 1». 1-, pm monary ve us; Wh]-ch took to 3' rnl, right lurig; 1:, lntcrrenal vein.

purely swimming

existence, and became specialized in the direction of adaptation to this, l)l]_(_‘.1‘(‘. ('..'Hn(__‘. about an asymmetry of the lungs, the right lung increas- ing and the left lung diminishing. Why this should have happened is not yet absolutely certain: it may probably have been in adapta- tion to active movements of ‘lateral flexure, for we see the same thing taking place in Grymnophiona, Snakes and Snu.l<o—like Lizards. That it has been the right rather than the left lung which has increased in size, is probably correlated with the rotation of this region of the alimentary canal in a counter-clockwise direction as seen from behind (seep. 168) which would tend to interfere more with the circulation through the left lung than with that through the right, by lengthening the course of the left pulmonary artery. Steps 174 EMBRYOLOGY OF THE LOWER VERTEBRATES GIL

in the development of this asymmetry are seen in Poly/ptems and in the Lung-fislics.

4. In purely aquatic creatures the dictates of adaptation would naturally cause the air-filled lung to assume a dorsal position. An initial phase of this is repeated in Polyptems where the right lung has become dorsal and median in its hinder portion. In the Lung- fishes a further step is takcn—--the whole of the lung becoming dorsal except the pneumatic duct which still remains to mark out the path by which the lung moved dorsalwards round the right side of the alimentary canal.

That the movement dorsalwards was round the right side was no doubt due to the right lung being predominant and the left reduced in size. In the case of Oezatodus the predominance of the original right lung has been retained, the other being completely obsolete except for a short period during development. In Lepidosvlzen and Protopterzzs, on the other hand, the lopsidedness disappears, the original left lung regaining during ontogeny its primitive equality in size with its follow.

5. In the Actinopterygians——those fishes which show the highest degree of evolution in adaptation to a swimming mode of 1ife———the lung has in the course of its evolution passed through similar stages to those exemplified by Poly/pterus and Oeratodus. Here again only the original right lung persists as the air-bladder, the vestige of the left lung being possibly represented by the little diverticulum found by Moser upon the pneumatic duct in early stages of development} In the Actinopterygians a further step onwards has been made in that the glottis has assumed a dorsal position. This is fully ex- plicable by the rotation which this part of the gut has undergone, aided no doubt by the principle of economy of tissue which would tend to bring about a shortening of the unnecessarily long pneumatic duct. In some cases there still persist vestiges of the ancient cellular respiratory lining of the swim-bladder (ag. LeZn'asz'na, Ezytlmnas).

6. Finally in the Physoclistic forms-——the most highly specialized of all-—the swim-bladder has become completely isolated from the gut, its respiratory function has gone and it subserves a mainly hydro-

static function. The outline given above represents a scheme of evolution which

in the light of modern research has a high degree of probability. Of course as in all such evolutionary speculations there exist details which are still difficult to explain. While most of the facts of com- parative anatomy fit in well with it, some do not——such as, for example, the nerve-supply and the blood-supply of the air-bladder of Am1Ia——-but it may be anticipated with considerable confidence that these difficulties will be lessened or disappear with the progress of

research. ' See p. 168. This matter affords an interesting subject for further research. III . THY R0 ID 17_5

DERIVATIVES OF PHARYNGEAL "WALL OTHER THAN THE RESPIRATORY ORGANS

THYROID.——The Thyroid gland arises as a mid-ventral outgrowth of the pharyngeal or buccal floor about the level of the Hyoid

FIG. 99.—Sagitta1 set-.t..i0ns through :mturior portion of :llilllI.‘Hl:U'_\' Uttlllll of l.¢jlm'do.w'n-1 illustrating the (l(‘.\'L‘l()plll('.lli- of the 'l‘hyroi«1.

A, I}, C from specinuyns of sttlgn 30; I), :-'et.‘l;.,'- 3| ; 'I‘h, thyroid: I, t.on:.rn¢-_

arch. In those Vertebrates in which the pharyngeal rudiment is solid at this stage the thyroid outgrowth is also solid at its first appearance (Fig. 99, A, T/2,) and develops its cavity secondarily by eytolysis. 176 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

The Thyroid becomes gradually constricted off from the pharynx (Fig. 99, B and C) remaining for a time connected by a narrow stalk or duct with the pharyngeal or rather buecal floor just in front of the primary tongue (see Fig. 82, p. 149). This stalk of attachment becomes nipped across and the thyroid forms a mass (Fig. 99, D) or vesicle rounded in form or somewhat elongated in an antero-posterior direction lying in the mid-ventral line beneath the pharynx and just in front of the ventral aorta.

The originally simple vesicle undergoes a process of sprouting and division by which it becomes converted into a mass of rounded vesicles, each possessing a wall composed of a single layer of cubical epithelial cells and separated from its neighbours by highly vascular mesenchyme which penetrates in between the vesicles to form the stroma of the organ.

During later development the Thyroid undergoes characteristic changes of form in different subdivisions of the Vertebrata. Thus in Teleosts it frequently assumes a more or less diffuse character, the follicles being distributed in the neighbourhood of the ventral aorta and roots of the aifcrent branchial vessels. In the Amphibia and Amniota the organ becomes deeply constricted into two laterally placed lobes which may remain connected or may become separated, so that it assumes a paired character as happens in Amphibians

and Birds. With the processes of differential growth involved in the develop-

ment of the neck, the thyroid may undergo considerable displace- ment from its point of origin. Thus in adult Lizards it lies across the trachea well forwards from its hind end while in other reptiles and in birds it lies farther back close to the roots of the great arteries.

It is now generally accepted that the clue to the _phylogenetic history of the Thyroid is afforded by its development in Petromyzon (W. Muller, 1871). Here there develops a mid-ventral outgrowth of the pharyngeal floor, forming a short gutter in the branchial region, the lining of Which is composed partly of glandular cells which secrete a sticky mucus and partly of cells which bear powerful flagella. Morphologically this gutter is the same as the endostyle of Ampkiowus and during larval life its function is also similar: it appears to be in fact simply a shortened up endostyle. The slit-like pharyngeal opening becomes gradually reduced in length till it forms

merely a small pore. _ At the time of metamorphosis the pore becomes obliterated so

that the organ becomes a closed vesicle underlying the pharynx. This vesicle divides up into a number of small vesicles and its mucous secretion accumulates in their interior as a colloid substance like that of the Thyroid vesicles of the Grnathostomata. In a word, the endostyle of the Ammocoetes stage becomes the Thyroid of the adult, and there seems no reason to dpubt that the same has happened in phylogeny and that the thyroid of the Vertebrate is 111 BRANCHIAL BU DS 177

simply the modern representative of the endostyle of the proto- chordate ancestor.

An interesting feature is that while the physiological importance of the thyroid in the modern Vertebrate is that of a ductless gland for the production of internal secretion to be absorbed by the blood, it still goes on producing the mucous material used by the far back protochordate ancestor for entangling food particles, though that substance is no longer, owing to the disappearance of the duct, discharged into the pharyngeal cavity.

BRANCIIIAL BUDs.——There make their appearance in the develop ing Vertebrate a series of bud-like proliferations of the endodermal epithelium of -the branchial clefts which may be known as branchial buds. They appear at the upper and lower angles of the clefts and the series shows its fullest development in the Lampreys, where buds develop at the dorsal and ventral angles of all the clefts. In the majority of fishes investigated they have been found to appear at the dorsal angles of all the clefts eficept the first; in Urodele Amphibians at the dorsal angle of . clefts and at the ventral angle of II., III. and IV.; in Anura at the dorsal ends of I. and II. and at the ventral ends of ll.-V.; in Lacerta at the dorsal ends of I.-III. and the ventral ends of III. and IV.; in Gallus at dorsal and ventral ends of III. and IV.

The morphological significance of these organs is still completely obscure. Physiologically some of them appear to be of importance during the later stages of development preceding sexual maturity inasmuch as they give rise to that often bulky organ the Thymus. This arises by the fusion together of more or fewer of the dorsal buds, the others undergoing no further development. Thus in Lepvldosvlren (Bryce, 1906) dorsal buds III. and IV. develop into thymus while II. and V. undergo no further development: in Oeratodus (Grreil, 1913) II., III. and IV. give rise to Thymus while V. and VI. do not develop further: in H3/pogeopltds II., III., IV. and V. give rise to Thymus while rudiments on I. and VI. atrophy.

In regard to the much discussed histogenesis of the thymus all that need be said here is that the originally solid epithelial rudiment becomes in -the course of development loosened out into a sparse reticulum interpenetrated by mesenchyme richly traversed by blood- vessels and crowded with leucocytes.

The ventral buds, where they occur, become constricted off from the branchial epithelium forming simple rounded masses of epithelial cells (Amphibians) or they may be subdivided up by intrusive con- nective tissue into solid portions (Reptiles) or hollow vesicles (Birds). The small organs so formed are termed by their discoverer Maurer epithelial bodies: their physiological significance is quite unknown.

There normally develops in the Vertebrate either on both sides or only on the left side a small pouch-like diverticulum of the pharyngeal wall close to the ventral edge of the last gill cleft, what- ever the number of this be in the morphological series. The

VOL. II N 178 EMBRYOLOGY 01+‘ THE LOWER iVE_R'l‘EBIx’.A'1‘ES en.

divert culum becomes" separated from the pharynx and commonly gives 'se to numerous rounded vesicles somewhat resembling those of the yroid in appearance. The organ thus formed was named by van Be melen who discovered it in Elasmobranchs--—suprapericardial body—— iile Maurer has termed it the postbranchial body. Nothing is delini ely known regarding either its function or its evolutionary history, though it is someti.mes regarded as representing a vestigial last gill—pouch. A curious point is the tendency of the organ to unilateral development it makes its appearance only upon the left side in a large number of cases (Aca.nthz'as, Lepidosirevz and 1’7‘0t0pz1e'ms——-see Fig. 109, B-—most Urodeles, some Lizards).

CEMENT ()1z.m\Ns or 'J;m.sosroMA'i'oUs FlSHES.———-It has long been _

FIG. l00.—— Ventral views of Polyptcrus larva to show the cement-organs. A, Stage 80; B, Stage 33; c.o, cement-org:-m ; «.71, olfactory ox-gun; m, mouth ; V, ventric-le of heart.

known that the larvae of Actinopterygian ganoids possess cement- orgaus on the head in front of the mouth. Balfour (1881) wrote of this as “ a very primitive Vertebrate organ, which has disappeared in the adult state of almost all the Vertebrata; but it is probable that further investigations will show that the Teleostei, and especially the Siluroids, are not without traces of a similar structure.”

The organs in question were generally regarded as being developed from a thickening of the ectoderm. Miss Phelps (1899) lirst stated that they originated from endoderm (Amie) and the present writer, at the time ignorant of her work, was greatly surprised to find himself forced to this same conclusion by the examination of I'5udgett’s material of Poly/pterrus.

The cement-organ of Poly/pterus (Graham Kerr, 1906 and 1907.), when at the height of its development,_ forms a stout cylindrical structure with a deep hollow at its free end, projecting from the 188 EMBRYOLOGY OF THE‘ LOWER VERTEBRATES


FIG. 108. Illustrating early development of the liver in Birds. A, 47-hour chick; B, 52-hour chick; C, 50-hour chick (after Brouha, 1898); D, fourth-day chick; E, 7 mm. embryo of the Roseate Tern--Sterne paradi.«n'aca.-(after

Hammer, 1807). M 1, rudiment of anterior (“1eft") bile-

CH.

portion of the rudiment. The gall bladder originates as a bulging of the floor of the bile-duct towards its anterior end. A The formation of the pos- terior and longer section of the bile-duct, Which will be extrahepatic in the adult, lagsin its development behind the anterior portions of the rudiment. Such differences in the time of appearance of different parts of the hepatic apparatus——1iver, gall-bladder, bile-duct—-—are to be looked on as mere secondary modifica- tions of development,——the

primitive condition being that i

of a simple pocket of the gut- wall such as persists in Am’- phioasus.

SAUROPSIDA.-—-The hepatic apparatus here again makes its appearance as a longi- tudinally situated pocket of the morphologically ventral Wall of the gut. In birds this is situated at first on the anterior wall of the yolk—stalk (Fig. 108, A). The diverti- culum grows actively into an anterior (dorsal) and a pos- terior (ventral) pocket (Fig. 108, C, Z73. 1 and Z7}. 2) while the intervening portion be- comes flattened out and incor- porated in the gut-wall.

There thus come to be two distinct liver-rudiments an anterior and a posterior. Of these each sprouts out at its end into irregular projections which eventually fuse and form a spongy mass, surround- ing the cavity of the ductus

duct; bd°. posterior (“risht") bile-duct; ent, cavity or venosus, and havingin its

fore-gut; gb, rudiment of gall-bladder; la‘. 1 and 2, anterior and posterior liver - rudiments; pa.‘n,\ dorsal rudiment of pancreas.

meshes blood-spaces which 180 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

The first rudiment oi’ the organ is seen to bee simple pocket-like outgrowth of the gut-wall (A, c.o): this becomes more and more prominent (B, C): it becomes gradually constricted oh" at its base from the gut-Wall, its cavity becoming isolated first Finally it separates completely from the main endoclerm and its outer end undergoes fusion with the deep layer of the ectoderm. lts cavity then opens to the exterior and the fully functional condition is reached——the endodermal origin of the secretory lining being for a time betrayed by the conspicuous persistent yolk granules in its cells.

It will be noted that the exposed side of the secretory epithelium, that on which the secretion is extruded, is that which originally faced inwards towards the lumen of the alimentary canal. In other words the direction in which the extrusion takes place is morpho- logically the same as that of any other part of the glandular lining of the gut-wall.

As is the case in other forms the cement—org-an is a transient, purely larval, structure. About stage 31 (Fig. 197, D) degeneration commences: the gland shrivels up, the gland-cells becoming more slender and dark pigment making its appearance in their interior, the epithelium becomes penetrated by ingrowing blood-vessels, its cell-boundaries become indistinct. The process of atrophy goes on rapidly and by stage 36 (Fig. 197, F) the organ has completely disappeared.

An interesting variation from the normal course of development is found in specimens in which the cement-organ rudiments are more or less approximated to one another. This variation reaches its maximum in occasional individuals in which they are completely fused and form an unpaired structure, continuous across the mesial

lane.

P In the actinopterygian Ganoids the cement—organ develops along the same general lines as those just indicated. In the Sturgeons the development has been worked out recently by Sawadsky (1911) in Acipenser ruthenus. Here the organ forms a rounded projection, very much in the same position as that of Polypterus, but in this case each becomes divided by a groove so as to form two rounded knobs. These knobs eventually grow out to form the tactile barbels of the adult, the secretory epithelium being carried out on the surface of the barbel as it grows.

The secretory epithelium is here also endodermal, its rudiment being the gut-wall immediately dorsal to the position in which the mouth will develop later and being continuous across the mesial plane. The unpaired condition which occurs in Polypterus as a variation is thus normal in the case of the sturgeon. As the head increases in length the secretory epithelium becomes carried out on its ventral surface, looking just as if it were the thickened ectoderm of this surface. Finally the paired condition comes about, ‘the lateral

parts of the secretory epithelium coming. to be supported by the knob-like projections already mentioned. III CEMENT-ORGANS 181

Am/ia is of special interest in regard to its cement-organs as it was in this form that their endodermal origin was first announced.‘ The organs are for a time in the form of a pair of rounded knobs, one on each side, but these take on a crescentic shape so that together they form a circular wall, interrupted anteriorly and posteriorly. Each organ contains a pocket-like projection of the gut—wall which takes on a somewhat sausage-like form in correlation with the curved shape of the organ as a whole. This endodermal sac separates from the main endoderm and becomes constricted across, so as to form°a curved row of closed vesicles from six to ten in number. Each vesicle fuses with the ectoderm and develops an opening to the exterior so that it takes on the appearance of a cup at first deep and narrow, later shallow and wider, its lining continuous with the deep layer of the ectoderm.

When the larva reaches a length of 13-14 mm. it makes less use of its cement-organ and the latter commences to degenerate, sinking beneath the surface with which, however, it remains connected by a narrow tubular channel. By about the 20 mm. stage this has disappeared and soon there is no trace of the organ to be found even in sections.

In Lepidosteus the organ appears to be similar while in the other ganoids its development still remains to be worked out.

These cement-organs are of special interest and importance for more than one reason. In the first place they are of importance in revealing a quite unexpected pitfall in the way of the investigator trained to have implicit faith in the germ-layer theory, for they show how a particular organ may become transferred from one g'erm—layer to another even though not belonging to the transitional zone where the two layers are continuous. A very common modification of ontogenetic development consists in the slurring over or even omission of particular stages in early development. Were this to happen in the case of the early stages in the development of the cement—organ say of Polypterus, it is easy to see that the organ might have every appearance of being purely ectodermal in its nature, although it is, as a matter of fact, endodermal.

It appears to the present writer quite possible, if not probable, that this modification has actually come about in the Dipnoi and Amphibians, and that the cement-organs of these groups, although they develop from the ectoderm in those forms which have been investigated (p. 79), are really homologous with the cement-organs of the Teleostomi, their cndodermal stage having been eliminated from ontogenetic development. Further investigations are needed in the Amphibia——to see whether no trace exists, in any member of the group, of an original connexion with the endoderm.

As regards the original nature of these organs it is impossible to arrive at any certain conclusion. Arising as they do in the form

‘ Phelps (1899). The actual discovery seems to have been made by Rcighard. Cf. Reighard and Phelps (1908). 182 EMBRYOLOGY OF THE LOWER VERTEBRATES 011.

of endodermal pockets, they obviously recall gill pouches on the one hand and coelenteric pouches on the other. Their position suggests a pair of preniandibular gill pouches: their function, that of forming an excretion (cement), perhaps indicates rather coelomic afiinities and the present writer suggested (1906) their possible correspondenee with premandibular head cavities of other Vertebrates. Reighard and Phelps (1908) hornologize them wi th the anterior pair of head-cavities of Elasmobranchs while van Wijhc (1914) sup-


l+‘m. I02. -Larva of Sa'rr_'.('u_l¢I..r_t(?s amlon. (After Budgett, 1901.) P‘-’I't3 3' homology With"

the ciliated organ of Amphiowus.

Altogether these cement-organs are very interesting and puzzling structures and would well repay further investigation. A thorough comparative study should be made of their development in the archaic Crossopterygians and of their possible homologues in Elasmobranehs.

Little is known regarding cement-organs in Teleosts, though it is proliable they will be found to occur in various tropical fresh- water fishes. Budgett ' s (1901) found a large P, _ cement-organ on the he . I « , head of the larva of the '1 /if/“‘jX~” Characinid Sarcodaces odéie (Fig. 102, 0.0). Ina A 0 / ( larva believed to be that 9 ' of the Mormyrid IIype7°o- lg J

«an, or-ment-organ.

pisus babe he found six ’ ‘( Well-marked cement 6. glands on the head which 1 . in this case secrete fine " U threads by which the

larva hangs suspended ' ' F 1' 103 ——Teleostean l as in“ )()‘8l to be those of in the water until the "' p " s ““’*°' *1’! ~“ ’_

lk . _ _ _ ,. II;/_,;er0pos1ts bebe, suspended from the rootlets 111 the 

18 H11_St‘3d t1_1P (15 1gd' nest. (From Budgett, 190].)

. 8 670 18 3.11

Gymnarclms also possess similar organs—-very small in the latter case 0

(Assheton, 1907).

The organs in these various fishes present, the appearance of being ectodermal thickenings: we have as yet no information as to whether, as may be suspected, they really originate from the endoderm.

DIGESTIVE TRACT. —- The respiratory region of the alimentary canal is succeeded by the true digestive _.tract and this shows more or less pronounced differentiation into successive portions-— III THE ALIMENTARY CANAL 183

oesophagus, stomach, intestine and its subdivisions, cloaca. In correlation with the digestive and assiniilative function of the intestinal endoderm this serves during early stages as the favourite storehouse of food-yolk, and the concentration of yolk in the abapical portion of the unsegmented egg is to be looked on as a foreshadowing of the fact that this portion of the egg will later become the endoderm. .

In the holoblastic Vertebrates the mass of heavily yolked endo- derm cells becomes, as it were, modelled into a tubular shape by the

Fnz. 104. ----Illustrating the modelling of the yolk in .I¢.-/4././¢_:/u/;/u'.s-. (After Sarasins, 1889.)

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