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

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Chapter 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 mesoderm - 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 development 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 somewhat 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 development. 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 development 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 of 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 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.

Stomodaeal Glands

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

Fig. 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.

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 case with Uroto1;le'2--u..s:, the buccal roof in front, that is to say in the neighbourhood of the mesial plane, 1)&Lb'SGH without interi-upticm into the external skin: in other words the maxillary ridge is not continued to the mesial plane so as to meet its fellow. In later stages 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 modiﬁcation of the mouth margin is‘ brought ahout hy the fact that, as 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.).

Fig. 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,

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

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.

“Endodermal” Section of Buccal Cavity

The fully developed buccal cavity has incorporated in it a posterior portionvarying in relative extent in different vertebrates —w hich is derived 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 development. In this case the velar membrane simply r u ptures——-its reinnants soon becoming absorbed-and the stomodaeal cavity is thrown into open communication with the enteric cavity. This is the case in certain Anura (Rana) and in Amniota.

Fig. 8l.—--Ventral 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 membrane 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 proportion 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 Vertebrates

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

FIG. 82.—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 examination of carefully prepared celloidin sections (Fig. 83) shows that at its inner end the epithelium passes by imperceptible gradations into the ordinary yolky endoderm, with no trace of the sharply deﬁned edge which it would possess were it a 1ayer of ectoderm pushing its way inwards. It extends inwards simply by a process of delamination from the yolky “ endoderm.”

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.

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

Fig. 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.-.

The Tongue

The tongue is a portion of the buccal ﬂoor which becomes demarcated off from the rest by a split formed by a downgrowth of the lining epithelium of the mouth. is mode of development 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 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 outgrowths 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 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 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).

Fig. 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.

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 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.

Pharynx

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 leading 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 projectionsthe 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 clefts — 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 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 following 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 independent 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 stages of which have not been generally accessible to embryologists. The typical External “C a W gill is a projection from the surface of the body - on the outer side of a visceral arch. It consists 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 Which 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 prevalent 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 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.

e.g.I There is however no deﬁnite evidence of any such process taking place and the present writer would interpret the appearances as mean~ ing simply that the ectoderm covering 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:

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 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 performed 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 functional 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 correlated 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 completely 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 morphological question: were External Gills at any period more widely distributed 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 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 disappearance of external gills, namely the development of'_ a new organ —— the yolk - sac with its highly developed vitelline network of blood-vessels»--which in addition to its primitive function Inust necessarily 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.

Visceral Clefts

The visceral clefts develop in what appears to be the most archaic method in Lampreys and Elasmobranehs 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 development 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.

1n 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 comparatively 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 subsequent 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 pore. 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 bodywall 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 respiratory 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..?é‘§?'.;....: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 '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.

Internal Gills

The 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 endodermal origin in the case of the spiracle and ectodermal in the case 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 writer’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

Fig. 90. Horizontal -.m~1ionthrough the portion of Lhe cleft -in the innuebmwhial reg.“ M. ymmg AOL d1ate 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 (.)f the boundary betvlreen the two layers p;,, it seems hardly profitable to speculate on the matter.

In certain ﬁshes the gill-lamellae are for a time prolonged outwards into long threads which project through the cleft opening into the surrounding ﬂuid. Such is the case in the embryos of F.lasn1ebranchs, 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 projecting 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 of Rm-1 Branchial Respiratory Organs

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 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 prevertebrate 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 Elasmobranch ﬁshes the pharyngeal wall develops a great outgrowth which, as will become apparent later, is to be looked upon as homelogous 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 corresponding on the whole with those described there are differences in detail in different groups-—-the most conspicuous of these variations 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, bloodvessels, 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 endodcrmal 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 complicated, 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 of 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 ontogenetic development of this organ will be followed out in a little more detail (Moser, 1902; Juillet, 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 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 unbranched until the ﬁfth day when its cndoderm begins to bulge out, near the point where it enters the lung, to form the ﬁrst entobronchus. 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 entobronchi 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 entobronchi: 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 ectobronchi 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 substance 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 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 arrangement 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).

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 entobronchus, the posterior thoracic and the abdominal from the mesobronchus. 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 abdominal) 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 05thoracic 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 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 entoabdonlinal sacs near bronchi; tc, iiiterclapicular air-sac‘; -nies,tn:)¢sst)ll;1;otrl1sch1is; 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 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.

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.

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 mm. in length, Moscr ﬁnds that a wellmarked 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 lungrudiment 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 pneumatic 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 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 Lungﬁshes, and, in fact, the morphological nature of the whole organ, is 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 tetrapodous vertebrates (C).1

Fig. 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.

Fig. 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 important 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.

head on each side as shown in Figs. 100, A, and 197, C, 0.0. A longjtudinal 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 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 fig. 101, A-E.

Fig. 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.

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

FIG. 97.———Portions 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 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 encroachcd 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 n1onopneumatic 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 midventral 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 projected 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 necessarily 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 of the Air-Bladder.

The 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 airbladder 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, communieating 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 possessing 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 increasing and the left lung diminishing. Why this should have happened is not yet absolutely certain: it may probably have been in adaptation 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 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 Lungﬁshes 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 explicable 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 comparative 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 .

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 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 cytolysis.

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¢-_

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 displacement 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 simply the modern representative of the endostyle of the protochordate 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.

Branchial 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 bloodvessels 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 connective 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, whatever the number of this be in the morphological series. The diverticulum 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).

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.

Fishes

It has long been known that the larvae of Actinopterygian ganoids possess cementorgaus 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 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 posterior 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 modiﬁcations of development, — the primitive condition being that of a simple pocket of the gutwall such as persists in Am’phioasus.

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.

Sauropsida

The hepatic apparatus here again makes its appearance as a longitudinally 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 diverticulum grows actively into an anterior (dorsal) and a posterior (ventral) pocket (Fig. 108, C, Z73. 1 and Z7}. 2) while the intervening portion becomes ﬂattened out and incorporated 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, surrounding 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

The first rudiment of 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 morphologically 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—organ 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 plane.

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.

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 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

Phelps (1899). The actual discovery seems to have been made by Rcighard. Cf. Reighard and Phelps (1908).

Fig 102.-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 freshwater 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 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].)

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-— 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 endoderm cells becomes, as it were, modelled into a tubular shape by the reciprocal activity of endoderm and splanchnie mesodermg the rudiment so formed undergoing active growth in length and differentiation of structure while the yolk is being assimilated.

Fig. 104. - Illustrating the modelling of the yolk in .I¢.-/4././¢_:/u/;/u'.s-. (After Sarasins, 1889.) A and B illnslmlu the sauna st::;.:«-, 13 representing a view from the-. dorsal side. The small—celle«.l epithelial port.-inn or the g-nt.-\m,ll is seen passing down the centre of l"i_«_;. ll. (3, I). and }*3r'np1"t-sent later stages «h-awn from the ventral side; F (7 cm. embryo) vent:-o-lateral view frmn the right side.

In the two most archaic groups of holoblastic gnathostomes, the Crossclptm-ygians and the Lung-ﬁshes, a feature of special interest is the development of the spiral valve. In Lepiciosiren, as is indicated by Figs. 105 and 106, this takes its origin by the solid mass of yolk-laden endoderm l)(‘('_ﬁ(‘)llllllg modelled into a right-handed spiral coil——the deep incision xvhich separates successive turns of the spiral being ﬁlled up by ingrowing mesenchyme belonging to the splanclmic mesmlerni. There can be little doubt that this is a secondarily Il'l()(l.lllt__*.(l. mode of development, but nevertheless it is probable that the spiral coiling of the endodermal rudiment-v__is to be explained as a repetition of_ an ancestral condition in which the intestine as a whole was long and spirally coiled.

An important feature of such a spiral coiling of the gut rudiment is that it would necessarily tend to bring about a twisting of the

Fig 105.~--l')issm-t.ion.s- of young In-1)i<lo.<in-..ns of stages 32 (A), 35 (B), 36 (C), and 37 (D), lmm I.lu_: vi-ntral side to show the modelling of the intestine.

g.b, gall-l')la_(lder; Ii, liver; V, \'c-uh-i«_-|(-,

alimentary canal just in front of the spirally coiled portion in a counter-clockwise direction as seen from behind, vie. a movement in which points on the ventral side of the alimentary canal would become shifted towards the 1-iglit side. A_s.a]ready indicated such a twisting of this region of the alimentary canal actually does take 111 THE ,ALIMEN'l‘AR'Y CANAL

place in' development causing the lung rudiment to shift dorsally round the right side of the alimentary canal.

In the more richly yolked Vertebrates the Ventral ‘[N)1'lJl('lllS of the gut-Wall are more and more clogged up with yolk and this results in a greater and greater concentration of developmental activity in the dorsal wall. This is clearly indicated by transverse sections through the developing gut of Vertebrates wl1i_ch though rich in yolk are still holoblastic. Such sections (Fig. 107) show the dorsal wall of the gut to consist of small active cells arranged as a columnar epithelium, while the side walls and ﬂoor consist of large coinparatively inert yolk -laden elements. It

"is only as development goes on,

and as the yolk is consumed, that the epithelial small-celled character gradually spreads ventrally.

In the actually meroblastic Vertebrates, the heavily yolked portions of the primitive gutwall never undergo segmentation at all, unless possibly as regards a thin superﬁcial layer. They remain as a continuous mass of yolk, round which the epithelium gradually spreads. In this case the formation of all the important organs of the alimentary canal is concentrated in the dorsal. portion which heeomes gradually folded off from the main mass of the yolk. This folding-off process takes place most actively in the anterior region, so as to form the tubular l'ore- gut, and also posteriorly, the intermediate portion re 185

FIG. 106.—Dissection of Lepidosiren larva of stage 35.

t.o, tectum o1m2cunz.. pm, pronephros oc.r, occipital rib

u 1

o. c, auditory capsule Ii, liver l, lung ht, heart h, hemisphere 186 EMB‘RYOLOGY or THE LOWER VERTEBRATES on.

maining for a time as a longitudinal groove opening ventrally towards the yolk. As the lips of this groove‘ gradually coalesce at each end the communication between the gut cavity and the,yolk becomes gradually narrowed down to the tubular cavity of the yolkstalk situated at first behind the liver but later becoming shifted forwards by differential growth. Eventually this becomes obliterated and the definitive alimentary canal becomes completely isolated from what remains of the yolk. In many Telcostean fishes this isolation takes place at a very early stage in development. . _ _ The alimentary canal is, in correlation with its dlgestive function, necessarily a highly glandular organ. Primitively the secretory functions are carried out by unicellular glands, scattered about amongst the other epithelial cells of the endoderm, but in the Vertebrates, as in all the more complex Metazoa, special concentrations of gland cells and of secretory activity take place in localized portions of the enteric wall. Each of these specially glandular patches undergoes a great increase in its area, which causes it to bulge outwards as a simple or much subdivided Fro. l07.—'l.‘ransverse section through bind and comphcated pocket’? formlng

portion of intestine of a larva of Ich- ﬂu CllSl':lIlCl: glandular appendage Of

thytlfih-1:8. (After Sarasins, 'l‘he the alimentary canal_ stage of development was that shown in

Fig, 104, F. ' The sheath of splanchnic LIVER‘ _"_Of these 81a’I?d“1‘“' megodgrm is omit,ted_ appendages, 1n the (3359 _Of Verte brates, the most ancient appears to be the liver, which is already present in Amp}:/ioasus. In this animal the liver originates in ontogeny (Hammar, 1893) as a pocket-like outgrowth of the alimentary canal wall on its ventral side and slightly posterior to the hind end of the pharynx. Apart from increase in size and relative narrowing of its base of attachment the liver in Amphiomus undergoes no further complication but retains its extraordinarily primitive pouch-like condition throughout life.

In the holoblastic Craniates the liver arises similarly as a ventral projection of the alimentary canal wall. This shows the customary modiﬁcations in correlation with the presence of yolk, arising in some cases in the more primitive fashion as a hollow pocket (Lampreys, many Amphibians, Cemtodus), in others (many Amphibians, Lep1Sdosiiren and I’-rotopterms) as a solid knob of yolk-laden cells (Fig. 105, Z73). This grows rapidly in size, as it uses up its food-yolk, and becomes constricted off from the main mass of yolk by ingrowing mesenchyme, until its attachment becomes narrowed down to a slender stalk-—-the rudiment of the bile-duct.

The pouch-like rudiment of the liver undergoes an active process of sprouting into numerous secondary pockets, each of which becomes III LIVER 187

greatly elongated and branched, and gives the gland a tubular character. This character may be retained throughout life (Lampreys) but normally the tubules undergo anastomosis so as to form a network of trabeculae. While this is to be regarded as the primitive mode of development of the tubules it is to be noted that they more usually in actual fact show the modiﬁcation of development which we have learned to associate with the presence of yolk, being at ﬁrst solid and taking their origin not by a process of outgrowth but rather by a process of modelling by ingrowing mesenchyme.

In the meroblastic Vertebrates also the liver may be described as originating from a mid-ventral outpushing of the enteric wall. Variations occur in detail, in correlation with the varying relations of the hepatic portion of enteric wall to the fore-gut and yolk-sac. If this part of the gut-wall has already been folded off from the yolk-sac and incorporated in the fore-gut, then the early stages of development of the liver divertieulum pursue their normal course. If, on the other hand, it still forms part of the yolk-sac wall, the hepatic rudiment makes its appearance as a projection from this, and it may be in its first beginnings paired, its two halves separated by the longitudinal slit by which the cavities of the deﬁnitive gut and the yolk-sac are still continuous.

ELASMOBRANCHII.——The hepatic divertieulum at an early stage bulges out to form a conspicuous outgrowth on each side anteriorly ——the rudiments of the right and left lobes of the liver. The median portion between these becomes in its anterior region converted into secretory tissue while its posterior part becomes the bile-duet, with its dilatation the gall-bladder.

In Acanthzas (Scammon, 1913) the ﬁrst rudiment of the liver, which makes its appearance at a time when this region of the enteron is not yet ﬂoored in but opens freely into the subjacent yolk-sac, is distinctly paired. In view of the unpaired condition in Amplmloxus and the holoblastic Craniates there can be little doubt that this condition in Acanthvlas is a secondary modiﬁcation as indicated above. Secondary pockets soon make their appearance on the wall of the secretory portion of the rudiment, and grow actively into elongated and much-branched tubules. These fuse together secondarily to form the network characteristic of the fully developed liver. This network is bathed by the blood of the vitelline veins (see Chap. VI.).

After the embryo (Acamthias) has reached a length of 25-28 mm. the walls of the tubules, or trabeculae of the network,increase greatly in thickness so that both their own cavities and the intervening blood-spaces become relatively reduced and the organ assumes the compact deﬁnitive condition.

Whereas the tubules become throughout the greater part of their extent secretory in function the proximal portions, each common to a group of tubular branches, functionmerelyas ducts. These communicate with the main bile-duct formed from the posterior and median 274 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

of the genital portion of the peritoneal epithelium with the peritoneal funnels, or with the nephrostomes, were in the form of open ciliatecl grooves or gutters on the surface of the peritoneum, that later on these became closed in to form tubular channels, and that in actual ontogenetic development in the modern amphibia the development from the coelomic epithelium has become obscured except for traces now at one end now at the other.

At their distal ends the cell-strands in the male can be traced gradually farther and farther into the genital fold until they come into immediate relationship with the cell-nests of gonocytes. In the female of Urodela and Anura the strands do not spread so far into the genital fold, nor are they, even in early stages, so well developed as in the male.

The fatty body is developmentally simply a portion of the genital fold which becomes specialized as a store-house of fat. In Anura it is the progonal portion which undergoes this differentiation while in Urodeles and Gymnophiona the rudiment of the fatty body is continued backwards as a ridge along the mesial face of the genital fold throughout its extent.

The fat is stored in the connective tissue of the organ, the fat cells being usually interpreted as immigrant mesenchyme cells which have invaded the rudiment by its base of attachment. It has also been suggested that these fat cells are peritoneal in their origin (Abramowicz, 1913)——a suggestion of obvious interest in view of the general tendency in the animal kingdom for potential germ~cells to undergo degeneration in order to provide nourishment for the germcells which become functional.

Testis

The development of the functional testis out of the genital fold is seen in peculiarly simple and diagrammatic form in the Gymnophiona. Here the strands of the urinogenital network, as they sprout into the interior of the testis, anastomose together along its axis so as to form a central canal——around which, embedded in the stroma of the organ, lie the rounded nests of gonocytes. Fusion takes place between each gonocyte-nest and the wall of the central canal and then each nest develops a cavity in its own interior and becomes a hollow ampulla opening into the canal at its inner end.

Various modiﬁcations of this simple scheme are to be found. In Grymnophiona themsel.ves ampulla—formation becomes suppressed except in localized regions between successive vasa etferentia, so that intervening portions of the testis are sterile and form merely thin tubular eonnexions between the bead-like fertile portions. Again the ampullae vary in shape: they may be elongated and tubular (Discoglossas) or, as in the majority of cases, ﬂattened against one another by pressure. The “axial” canal again may lie close to the surface: it may become greatly branched, as in most Urodeles, or may form a complicated network as in most Anura.

Ovary

In the differentiation of the ovary (Bouin, 1901) the most important points to be noted are the following. As regards communicate with the just -mentioned vessel. This spongy mass, the trabeculae of which are at first solid and only secondarily develop a lumen, forms the secretory portion of the liver, while the proximal portions of,the outgrowths persist as the two conspicuous bile-ducts of the adult bird (Fig. 108, D, E, bcl. 1 and M. 2). In such birds as possess a gall-bladder this is formed by a dilatation close to the point of junction of the posterior hile-duct with the gut-wall (Fig. 108, I), E, gb).

Pancreas

The pancreas, though in the adult a single structure, arises typically from three distinct rudiments, each of which is at first a simple pocket-like outgrowth of the splanchnopleure. One of the rudiments (cf. Fig. 80, H) is situated dorsally a little posterior to the stomach, the other two, which appear somewhat later, are ventral and arise as outpushings of the hepatic diverticul11m in the region of the bile-duct. The ventral pancreatic rudiments are commonly paired, arising one on the right and one on the left of the bile~duct.

The three rudiments increase in size, secretory tubules sprout out from them and the two ventral rudiments become carried in a dorsalward direction, up the right side, by the rotation which the gut undergoes in this region (see p. 168). The right ventral rudiment comes in contact with the dorsal rudiment and fusion takes place—all three rudiments forming a single organ the three—fold origin of which is indicated by its three communications with the alimentary canal.

Such may be considered the typical mode of development of the pancreas, but important variations in detail occur in the different groups. In Cyclostomes and Elasmobranchs only the dorsal pancreas is known to occur. Its development in the former group requires further investigation. In Elasmobranchs it arises as a longitudinal groove of the enteric wall dorsally and a little posterior to the opening of the bile-duct. It becomes constricted off’ from before backwards and in accordance with the rotation of the alimentary canal it becomes shifted to the left side and ends up by being ventral.

In Crossopterygians the three typical rudiments appear (Fig. 80, H) but their development has not been followed in detail. Eventually the pancreatic complex extends forwards beneath the liver and completely fuses with it forming a tlfick layer over its ventral surface in the region near the opening of the bile-duct.

In Actinopterygian Granoids also (Piper, 1902; Nicolas, 1904), the pancreatic complex derived from the original three rudiments becomes fused with the substance of the liver, only its posterior dorsal portion remaining extrahepatic. The main duct of the pancreas is the persistent stalk of the right ventral rudiment which opens into the gall-bladder formed by the dilated terminal part of the bile-duct. Of the two other pancreatic ducts the left ventral apparently atrophies entirely, while the dorsal is said in the case of Am/ia to disappear but in the Sterlet (Acipenser ruthenus) to persist. 190 EMBRYOLOGY OF THE LOWER VERTEBRATES CH.

In Teleosts the early development agrees closely with that of the ganoids, only a doubt exists whether the deﬁnitive pancreatic duct (Duct of Wirsung) may not be formed by a fusion of the two ventral ducts rather than by the persistent right duct alone. During later stages great difl'erenees arise between dilferent members of the group. l n some (Silwrus, Esow) the complex forms a single compact gland, in others (ﬂcomber, U3/_7)7"in'w.<¢) it becomes divided i.nto a number of independent lobes, in others, including the majority of the more familiar Teleosts, it becomes greatly branched and is diffused in the substance of the dorsal mesentery while in still others (Labridae, Syngnr.rt7tus) the condition resembles that of the ganoids a large part of the organ being intrahepatic (Laguesse, 1894).

FIG. 109.-—-Dorsal View showing l'udiIm:nts of 1 orsal p:nu:reas .-mil luring in l:u'v:1c of Protopterus (stages 32 and 34). I, lung; op, opercnlum ; pied, dorsal pancreas; p.b, pnstbranchial body; p.f, pectoral limb; 3:-, \'i.~'.«-o-ml t_'l¢'.fL rudiment.

In Lung-ﬁshes the three typical rudiments make their appearance. In Protopterus the dorsal rudiment (see Fig. 109, A, pad) is a solid outgrowth (hollow in Lepidosiren) from the gut-wall, usually rounded in form but occasionally elongated in an antero-posterior direction as in the specimen ﬁgured (Fig. 109, A). The attachment to the gut becomes rapidly constricted to a narrow stalk and a cavity develops in the interior of the rudiment. The ventral rudiments appear a little later, as solid projections one on each side of the attachment of the bile-duct to the gut. The two ventral rudiments, as they increase in size, meet and fuse dorsal to the bile-duct, and later on the dorsal surface of the right ventral rudiment comes in contact and fuses with the ventral surface of the dorsal rudiment. The stalks of the three rudiments remain as three ducts, the two ventral opening just posterior (original right rudiment) and anterior m (original left) respectively to the opening of the bile,-duct, while the dorsal opening is situated at the extremity of the spout-like pyloric valve.

The general course of development in Lepidosiren is similar and in both it is characteristic that the pancreas never bulges beyond the mesodermal coating of the splanchnopleure. It remains embedded throughout life in the gut-wall and is consequently not noticeable in an ordinary dissection.

In Oeratoalus (Neumayr, 1904) the development of the pancreas is similar though here the left ventral rudiment, which in Protoptems is smaller in size than the right, remains rudimentary.

The Amphibia are of special interest from the fact that it was a member of this group (B0m.b7Inat0r) in which Goettc (1875) first observed the origin of the pancreas from three separate rudiments. Groeppert (1891) was able to extend the observation to various other Amphibians, both Urodele and Anuran, and to show that in Urodeles the dorsal rudiment retains its duct, opening just behind the pylorus, while in the Anura this duct disappears. In both cases the ducts of the two ventral rudiments undergo fusion to form a duct of Wirsung which opens into the bile-duct.

In Reptiles (Lace7~ta-—-Brachet, 1896) the right ventral and the dorsal rudiments fuse to form the deﬁnitive pancreas, the left ventral atrophying (cf. Lung-ﬁshes). According to Brachet the duct of the dorsal rudiment does not disappear but fuses with that of the right ventral to form the deﬁnitive pancreatic duct.

Birds show three rudiments which undergo fusion into a complex in the normal fashion, all three ducts remaining functional and conspicuous in the adult. Suppression of the left ventral rudiment occurs as an occasional variation.

The observed facts of development of the Pancreas clearly justify the conclusion that this organ of the modern Vertebrate has arisen in the course of evolution from three originally separate diverticula of the glandular enteric wall-~—-a pair arising from the hepatic pouch and the third from the dorsal wall. The precise localization of the rudiments at comparatively distant points of the enteric wall point to the probability that the nature of the secretion was originally different in the case of the ventral pancreas from that of the dorsal.

Pyloric Caeca

The caeca which are present in the pyloric region in many actinopterygian ﬁshes arise as simple outgrowths of the gut-wall. The interesting suggestion has been made (Taylor, 1913) that the simple circle of these caeca, which is apparently their most primitive arrangement, corresponds morphologically with the curious valve found in various ﬁshes (Amia, Lung-fishes, Symbmnchus, Anguilla, etc.) in which the pyloric end of the stomach is prolonged back into a kind of spout which is ensheathed by the anterior end of the intestine. The circular prolongation forward of the intestinal cavity round the gastric spout might clearly give rise to a circle of pyloric caeca simply by_ subdivision into a number of separate portions each of which continued to open into the gut cavity at its hinder end.

Rectal Gland

ThlS organ, which occurs in Elasmobranchs, arises as a simple pocket-like outgrowth of the gut-wall. The superﬁcially similar caecum of Lung-ﬁshes will be dealt with in connexion with the renal organs.

Cloaca

In the more archaic vertebrates the ducts of the excretory organs open into the terminal part of the intestine which is thus a cloaca. It is believed by many that the excretory ducts originally opened at the hind end of the trunk independently of the alimentary canal and it is natural to suppose that the openings of the ducts have become gradually shifted ﬁrst into close proximity to the aims and ﬁnally on to the lining wall of the alimentary canal. This again suggests that the cloaca may really be a proctodaeum—~that the skin has been involuted to form its lining and that with this involution the renal openings have also been carried inwards.

Unfortunately the facts of ontogenetic development do not so far as can be seen at present fit this simple and attractive hypothesis. The cloaca is, except for a small portion close to its opening, of purely endodermal origin——the renal ducts open on what is part of the primary entcric wall. A suggested explanation of this fact dilfering from that mentioned above will be found in the chapter dealing with the renal organs.

A cloaca seems always to be developed though in some cases (e.g. Teleostean ﬁshes) it ﬂattens out and disappears later so that the renal organs and the gut come to have independent external openings.

The bursa Fabricii, a conspicuous glandular appendage of the dorsal Wall of the cloaca in young birds, has usually been regarded as proctodaeal in its origin but it is now known to arise in ontogeny from vacuolar spaces in a solid projection from the cloacal rudiment, dorsal to the stalk of the allantois (Wenckebach, 1888) and would therefore appear to belong to the mesenteron rather than to the proctodaeum.

The anal opening of the Vertebrate, as may have been gathered from Chap. II., is to be regarded as representing morphologically a portion of the gastrular mouth or protostoma. In a large number of Vertebrates however the opening arises in ontogeny not in this way but rather as a secondary perforation, although even in such cases the perforation arises in the line of the closed protostoma.

Temporary Occlusion of the Alimentary Canal

The alimentary canal is, in correlation with its function, a hollow tube. In a large number of Vertebrates, however, there are more or less extended periods of development during which the cavity is completely absent, either throughout the length of the canal or in certain portions. .

In its simplest condition this occurs as a special case of the temporary absence of lumen so frequently found in the ndevelopment of eventually hollow organs from a richly yolk-laden rudiment. An idea of how it has come about will be got from an inspection of the various stages of the development of the alimentary canal of Poly/pterus as shown in Fig. 80 on p. 146. During early stages the archenteric cavity is seen to be widely patent throughout, except that there is no mouth opening. During the later stages of development, immcdiately prior to the canal becoming functional, its walls throughout the region between the fore-gut and the cloaea become closely apposed, so as almost entirely to obliterate the cavity. Later on the walls recede from one another and the lumen becomes again patent.

It would obviously be merely a slight accentuation of this modiﬁcation of development for the cavity to be completely obliterated for a time. A still further modiﬁcation would be brought about by the omission altogether of the original hollow stage from the ontogenetic record. This actually- occurs in the case of the fore-gut in those Vertebrates in which this region of the enteric rudiment is yolk-laden: where, on the other hand, the yolk is practically completely concentrated in the mid-gut region as in meroblastic Vertebrates it does not occur as a rule.

The most striking temporary occlusions of the alimentary canal during development have to do with its terminal apertures. Thus there is not a single existing Vertebrate, so far as is known, in which the mouth opening persists from the gastrular stage, or in which even any connexion has so far been traced between the deﬁnitive mouth opening and the protostoma. In every case, even in A'2n,p/viowus, the mouth opening develops comparatively late as a secondary perforation. This modiﬁcation of development is in the present writer’s opinion to be attributed to the entire dependence of members of the Vertebrate phylum upon food-yolk during early stages of their development, the need for a functional mouth having thus disappeared.

The anteroposterior extent of this occlusion of the alimentary canal in the region of the oral opening differs in different subdivisions of the phylum. It may include a large part of the stomodaeal as well as the cndodermal portion of the buccal cavity as in the Lung-ﬁshes (p. 148) but more usually it is conﬁned to the boundary between the two, 7§.e. to the site of the original mouth opening the closely apposed ectoderm and endoderm being at this level continuous across the site of the future opening as the velar membrane’ (p. 145). The secondary perforation by which the alimentary canal comes to communicate with the exterior at its front end is in the case of some larval Vertebrates (e.g. Lapidosdren) closely correlated with the commencement of pharyngeal respiration but where the development is embryonic it commonly still takes place long before the.existence of any obvious functional need (ag. Chick, fourth day). At its hinder end the archenteron is, as has been shown in Chap. I., widely open to the exterior in all the lower Vertebrates during early stages and in various cases this opening can be traced either into direct continuity, or into less direct but still clear relationship, with the anal opening. The explanation of this lesser degree of modiﬁcation of the development of the anal opening as compared with the mouth may probably be associated with the less accentuated delay in the functional need for this opening. At stages long before ingestion or inspiration takes place by the mouth, the formation of waste products during the digestion of the yolk necessitates an outlet from the entcrio canal at its hinder end. Where obliteration does take place during still earlier stages this is probably correlated with the fact that the need of the opening is still non-existent.

It is of interest to notice that obliteration of the anal opening which is of a directly adaptive signiﬁcance may take place at a later stage. Thus in Lr,p2Talos2Iq°e71. during about the lirst two weeks of larval life, when large numbers of practically motionless larvae are lying crowded together in the nest, the anal opening, which had been continuously patent in earlier stages, is closed, so as to prevent the poisonous excretory products from ﬁnding their way out. So also in the case of the Elasmobranch embryo enclosed within its egg-shell. In the Amniota the perforation of the anus is delayed to a relatively late period doubtless for a similar reason.

It is characteristic of the phylum Vertebrata that the anal opening no longer occupies its primitive position at the extreme end of the body but has become shifted forwards along the ventral side. This shifting has probably come about with increased specialization for swimming by lateral flexure of the body, the withdrawal of the alimentary canal with its surrounding splanchnocoelic cavity frrim the hinder portion of the body, leaving the space they occupied free for increased development of the lateral muscles. This shifting forwards of the anus, leading to the differentiation of a distinct postanal or tail region, has occurred in all Vertebrates, least markedly in the more archaic groups. It reaches its maximum in some members of that group of Vertebrates which is above all others highly specialized for active swimming, the Teleostei, in some families of which the anus has actually assumed a jugular position.

During the actual ontogeny of the Vertebrate the process by which the anus comes to occupy a position 1nore or less distant from the tip of the tail region is somewhat modiﬁed from that which probably occurred during phyletie evolution. We do not ﬁnd that the anus remains at the tip of the tail during the growth in length and that it then gradually shifts forwards along the ventral side. What happens is that the opening at an early stage assumes a ventral position and that the tail region proceeds to sprout out dorsal to it. The process will be understood from an inspection of Fig. 80 (p. 146). In B the anus is at the binder end, in Cit has assumed a ventral position being overhung by the bulging tail rudiment, in D, E, 14‘, G the tail rudiment is seen to be extending actively past the position of the anus, the specially actively growing tissues being indicated by the darker shading.

In Fig. 80, G, a feature is well shown which occurs in the embryos of most Vertebrates—-—the postanal gut (pay). It was shown in Chap. I. how a connexion-—-the neurenteric canal--—~existed in some Vertebrates between the cavity of the enteron and that of the neural rudiment at their posterior ends. Here, in the postanal gut, we have such a connexion still persisting in a drawn-out form though, as in the present case, it may be a solid strand of yolky cells and not a hollow tube. The postanal gut is a purely transitory structure which at a relatively early period of development disintegrates completely.

In endeavouring to determine the morphological signiﬁcance of the postanal gut it is necessary to bear in mind that the Vertebrate in early stages develops from before backwards and that the growth in length by the addition of new segments takes place at its hinder end where there is a mass of actively growing embryonic tissue forming a kind of “growing point.” The tissue of this, although to the eye quite undifferentiated, contains the elements which form all the various tissues such as nerve cord, notochord, myotomes, alimentary canal, etc. As growth goes on these gradually become differentiated out, the differentiation always proceeding from before backwards. If we now look at such a young Vertebrate as that shown in Fig. 80, Or, we see the typical Vertebrate structure, including alimentary canal (pay) extending right back practically to the tip of the tail: it is only at the extreme tip that the various organs merge together into unditl‘erentiated embryonic tissue. The only striking peculiarity is that the communication of the alimentary canal with the exterior, the anus, is not in the midst of the growing tissue of the tip, as it would be, for example, in a young Chaetopod worm, but well forwards on the ventral side.

This peculiarity, in the writer’s opinion, ﬁnds its explanation in the development from before backwards already alluded to. The appearance of the anus at a point relatively far forwards means that it and the organs related to it such as the excretory d11cts complete their development at an earlier period of time. As it is of functional importance that the organs in question should do so, in contradistinction to the purely motor arrangements farther back, we see a physiological reason why evolution should have brought about a development of the anal opening in its anterior position from the beginning, and the elimination of those stages in which it was situated farther back.

As regards the phyletic evolution of this part of the enteron, we may sum up probabilities as follows: that the alimentary canal with its surrounding splanchnocoele originally extended to the hind end of the body: that the anal opening came to be shifted on to the ventral wall of the canal: tliat; it then underwent; a. gradual shifting forwards a.long the ventral side: that as it did so the now

postanal portion with its sphmchiiocoelc gradually atrophied the position they occupied becoming filled mainly with muscle. '

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