Book - The development of the chick (1919) 11

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Lillie FR. The development of the chick. (1919) Henry Holt And Company New York, New York.

Lillie 1919: Introduction | Part 1 - 1 The Egg | 2 Development Prior to Laying | 3 Outline of development, orientation, chronology | 4 From Laying to Formation of first somite | 5 Head-fold to twelve somites | 6 From twelve to thirty-six somites | Part 2 - 7 External form of embryo and embryonic membranes | 8 Nervous system | 9 Organs of special sense | 10 Alimentary tract and appendages | 11 The body-cavities, mesenteries and septum transversum | 12 Later development of the vascular system | 13 Urinogenital system | 14 Skeleton | Appendix | Frank Lillie

Part II The Forth Day to Hatching, Organogeny, Development of the Organs

Chapter XI The Body-Cavities, Mesenteries and Septum Transversum

The development of these parts is one of the most difficult subjects in embryologA^ involving, as it does, complex relations between the viscera, vascular system, and primitive body-cavity, on which the definitive relations of the bodv-cavities and mesenteries depend.

The pericardial and pleuro peritoneal cavities are completely separated in all vertebrates excepting Amphioxus, cyclostomes and some Selachii and ganoids, in which narrow apertures exist between the two. The pleural and peritoneal divisions of the coelome of the trunk communicate widely in amphibia; among reptiles completely closed pleural cavities are found apparently only in Crococlilia; in birds and mammals they are completely closed.

As we have seen, in the early embryo of the chick there is free communication between all parts of the body-cavity. We have to consider, therefore, (1) the separation of the pericardial and pleuro peritoneal cavities, (2) the separation of pleural and peritoneal cavities, and (3) development of the mesenteries.

I. The Separation of the Pericardial and Pleuroperitoneal Cavities

The pericardial cavity proceeds from the cephalic division of the primitive coelome (parietal cavity of His). We may review its primitive relations as follows (stage of 10 somites; see Chap. V) : it contains the heart which divides it into right and left parts so long as the dorsal and ventral mesocardia persist; these, however, disappear very early. Laterally, the parietal cavity communicates with the extra-embryonic body-cavity (Figs. 53 and 54) ; posteriorly it is bounded by the wall of the anterior intestinal portal (Fig. 67), on which the heart is seated like a rider in his saddle, the body of the rider being represented by the heart, and his legs by the omphalomesenteric veins. On each side of this posterior wall the parietal cavity communicates with the coelome of the trunk. The floor of the parietal cavity comprises two parts meeting at the head-fold, the anterior part being composed of somatopleure, and the posterior part of splanchnopleure; the former is part of the definitive pericardial wall, the latter, known as the precardial plate, is provisional

(Fig! 67).

The lateral mesocardia also take part in boundmg the parietal cavity. It will be remembered that these arise as a fusion on each side between the somatopleure and the primitive omphalomesenteric veins, and that the ducts of Cuvier develop in them. As the blastoderm is spread out flat at the time that they form, they constitute at first a lateral boundary to the posterior part of the parietal cavity; but as the embryo becomes separated from the blastoderm they assume a frontal position between the sinus venosus and body-wall, tne original median face becoming dorsal and the lateral face ventral. Thus they come to form a dorsal wall for the posterior part of the parietal cavity (Fig. 119). The communication of the parietal cavity with the ccelome of the trunk is thus divided into two, known respectively as the dorsal parietal recess and the ventral parietal recess. The former is a passageway above the lateral mesocardia, communicating in front with the parietal (pericardial) cavity and behind with the trunk cavity; the latter is a communication on each side of the wall of the anterior intestinal portal ventral to the lateral mesocardia.

The completion of the posterior wall of the pericardium is brought about by the formation and development of the septum transversum.

Septum Transversum. The septum transversum arises from three originally distinct parts, viz., (1) a median mass, (2) the lateral mesocardia, and (3) lateral closing folds arising from the body-wall between the uml:)ilicus and the lateral mesocardia.

1. The median mass proceeds from the ventral mesentery of the fore-gut. The location of the heart and liver in the ventral mesentery divides it in three parts, viz., (a) a superior part, comprising the mesocardium and dorsal ligament of the liver (gastrohepatic ligament), uniting the floor of the fore-gut and the heart and Uver, (h) a median portion comprising the sinus venosus, ductus venosus and Hver, and (c) an inferior portion. Tlie superior part persists in the region of the sinus venosus and liver, and the inferior part only as the primary ventral ligament of the liver.

The median mass of the septum transversum thus includes the sinus venosus, liver, and dorsal and ventral ligaments of the liver.

At sixty hours the median mass includes chiefly the sinus and ductus venosus and their mesenteries. At eighty hours (Fig. 192) a constriction begins to appear between sinus and

Fig. 192. — Reconstruction of the septum transversum and associated mesenteries of a chick embryo of 80 hours. (After Ravn.) Ao., Aorta. Int., Intestine. Liv., Liver. PI. m'g., Plica

mesogastrica. S.V., Sinus venosus.

ductus venosus, and the walls of the latter are expanded by the formation of liver tissue, so that the cylindrical form characteristic of sixty hours is lost, and the lateral walls of the ductus venosus bulge considerably. The continued growth of the liver causes a rapid lateral expansion of this portion of the septum transversum (Fig. 193 A).

The primary ventral ligament of the liver is included within the wall of the anterior intestinal portal up to al)out eighty hours. But, as the volk-sac shifts farther back, this ligament appears as a separate membrane (inferior part of the primary ventral

Fig. 193. — Reconstruction of the septum transversum and associated mesenteries of a chick embryo of 5 to 6 days. (After


A. Entire.

B. After removal of the liver and sinus venosus.

A., Aorta, ac. M., Accessory mesentery. cav. F., Caval fold. coel. F., Coeliac fold. Her., Hiatus communis recessum. Int., Intestine. Lg., Lung. Liv., Liver, m. p., Pleuropericardial membrane, pvl., Primary ventral ligament of the hver. Sv., Sinus venosus.

mesentery), uniting the ventral and posterior face of the liver

to the body-wall just in front of the umbilicus (Fig. 193 A, pvl.).

For the purposes of these figures the body-wall is cut away.

Nevertheless, it can be seen that the pericardial cavity commiunicates with the peritoneal cavity around the median mass of the septum transversum beneath the kiteral mesocardia.

2. The lateral mesocardia constitute the second component of the septum transversum. At the stage of sixty hours they are nearly round in section. At eighty-six hours the substance posterior to the duct of Cuvier begins to thicken (Fig. 192) so that the section is no longer round but elongated towards the umbilicus. They still extend almost transversely to the lateral body-wall. However, the retreat of the heart backwards soon changes their direction (Fig. 193 A) so as to form a long oblique partition between the pericardium and the dorsal parietal recess, the direction of the ducts of Cuvier being changed at the same time. The lateral mesocardia are directly continuous with the anterior portion of the median mass of the septum transversum.

3. The lateral closing folds arise as ridges of the lateral bodywall extending obliquely from the primary ventral ligament of the liver upwards and forwards to the lateral mesocardia. They arise along the course of the umbilical veins which open at first into the ducts of Cuvier. As the lateral closing folds develop first at their anterior ends, they appear as direct backward prolongations of the lateral mesocardia. They fuse with the lateral ventral surface of the liver (median mass of the septum transversum), and when they are completed back to the primary ventral ligament of the liver, they completely close the ventral communication of the pericardium with the peritoneal cavity. They mark out a triangular area on the cephalic face of the liver with postero-ventral apex and antero-dorsal base, which forms the median portion of the posterior wall of the pericardium (cf. Fig. 193 A). At six days the ventral communication of the pericardium is reduced to a very small opening, and at eight days it is entirely closed.

Closure of the Dorsal Opening of the Pericardium. As already noted the pericardial cavity communicates with the peritoneal cavity above the lateral mesocardia by way of the dorsal parietal recesses, which are destined to form a large part of the pleural cavities. We have, therefore, to consider next the closure of the aperture between the pleural and pericardial cavities. We have already seen that the heart shifts backwards very rapidly between the third and sixth days, and this draws out the lateral mesocardia in an oblique plane directed from dorsal anterior to ventral posterior (Fig. 193); the ducts of Ciivier thus become oblique also, and the lateral mesocardia become converted into an oblique septum between the posterior parts of the incipient pleural cavities and the pericardial cavity (pleuro-pericardial membrane). In front of the sinus venosus, however, the pleural and pericardial cavities communicate with one another between the ducts of Cuvier, which form a projection from the lateral body-wall, and the bronchi which project laterally beneath the oesophagus. These apertures are gradually closed by fusion of the walls of the bronchi with the projecting duct of Cuvier, beginning in front and extending back to the sinus venosus. Thus the incipient pleural cavities come to end blindly in front, though they still communicate widely behind with the peritoneal cavity. The membrane thus established between pleural and pericardial cavities is know^n as the pleuro-pericardial membrane.

Establishment of Independent Pericardial Walls. With the formation of the ventral body-wall the precardial plate (a portion of the splanchnopleure, which at first forms part of the floor of the pericardial cavity) is gradually replaced by the ventral bodywall. The pericardial cavity is thus bounded ventrally and laterally by the body-wall and posteriorly by the median mass of the septum transversum. It has no independent walls at first. The definitive pericardium is, however, a membranous sac, and this is formed by two main processes: in the first place the membrane of the anterior face of the liver (median mass of the septum transversum) which forms the posterior boundary of the pericardium becomes much thickened, and gradually splits off from the liver (cf. Figs. 148 and 150), the peritoneal cavity extending pari passu between the liver and the membrana pericardiaco-peritoneale thus formed. The suspensory ligament of the liver, however, remains in the middle line, and the membrane is also directly continuous w^ith the liver dorsally around the roots of the great veins. Thus a membranous wall is established for the posterior part of the pericardium. In the second place the peritoneal cavity extends secondarily into the bodywall bounding the pericardium ventrally and laterally, and thus splits a membranous pericardial sac oE from the body-wall. In this process the liver appears to play an active role. At least its anterior lobes occupy the peritoneal spaces thus established (Fig. 194). In the mammals, on the other hand, it is the extension of the pleural cavities ventrally that splits the membranous pericardium from the body-wall.

Derivatives of the Septum Transversum. From the preceding account it will be seen that the following are derivatives of the septum transversum: (1) The posterior part of the pericardial membrane. (2) The pleuro-pericardial membrane. (3) The liver with its vessels and gastro-hepatic and primary ventral ligaments.

Fig. 194. — Photot;raph of a transverse section of an 8-day chick.

abd. A. S., Abdominal air-sac. A. coel., Coeliac artery. Ao., Aorta. A. o. m., Omphalomesenteric artery. Aiir. d., Right auricle. Cav. pc, Pericardial cavity. M. D., Miillerian duct. M. pc, Membranous pericardium. Msn., Mesonephros. Pr'v., Proventriculus. S., Septum ventriculorum. V. c. i., Vena cava inferior. V. h. d., Right hepatic vein. V. d., Right ventricle. V. s., Left ventricle.

(4) A small part of the heart (the sinus venosus). As regards the last, it should be noted that the anterior portion of the original septum transversum is gradually constricted from the major posterior portion and becomes established as the sinus venosus;

this subsequently becomes incorporated in the right auricle of the heart. (See Chap. XII).

II. Separation of Pleural and Peritoneal Cavities

Origin of the Septum Pleuro-peritoneale

The pleuro-peritoneal septum arises from the so-called accessory mesenteries, the origin of which must now be described. At first the septum transversum has only a median dorsal mesentery, viz., the superior part of the primary ventral mesentery that unites the septum transversum to the floor of the fore-gut, and so by way of the dorsal mesentery of the latter to the dorsal body-wall. Subsequently, however, there arises a pair of mesenteries extending from the lateral wall of the cesophagus to the septum transversum. These are the accessory mesenteries, and they arise as follows: about the sixtieth hour they appear as mesenchymatous outgrowths, forming elongated lobes, projecting from the side walls of the oesophagus opposite the hind end of the lung rudiments. The right and left lobes are practically the same size at first and they bend over ventrally and soon fuse with the median mass of the septum transversum, represented at this time by the sinus and meatus venosus (cf. Figs. 118-120, Chap. VI). Thus are produced a pair of bays of the peritoneal cavity ending blindly in front, bounded laterally by the accessory mesenteries, and in the median direction by the intestine and its mesenteries. These are the pneumato-enteric recesses.

These bays have received different names from the various authors: thus His named only the right one as recessus superior sacci omenti; the left one being practically absent in mammals; Stoss called both recessus pleuro-peritoneales ; :\Iall called them gastric diverticula; Hochstetter, recessus pulmo-hepatici ; Maurer, bursa hepatico-enterica ; Ravn, recessus superior for the right one and recessus sinister for the left. We may call them the pneumato-enteric recesses (recessus pneumato-enterici) , following Broman.

At seventy-two hours the entodermal lung-sacs extend to the base of the accessory mesenteries, ending at the anterior end of the pneumato-enteric recesses. On the left side at this time the recess is fully formed back to near the anterior end of the cephalic hepatic diverticulum, on the right side considerably farther back; that is, the accessory mesentery is already longer on the right than on the left side, and the mesenchymatous lobe


from which it arises (pUca mesogastrica, Broman) can be traced back, shifting its attachment to the dorsal mesentery, as far as the anterior intestinal portal and a little farther (Fig. 192, cf. also Fig. 120).

At ninety-six hours the entodermal lung-sacs extend far into the accessory mesenteries, and thus lie laterally to the pneumatoenteric recesses. On the left side the accessory mesentery ceases opposite the tip of the lung, but on the right side it is continued back by the mesentery of the vena cava as far as the middle of the stomach, and in this region its ventral attachment is to the superior lateral angle of the liver.

The growth of the lung-sacs into the accessory mesenteries divides the latter into three parts, viz., a superior portion uniting the lung to the dorsal mesentery, a median portion enclosing the lung, and an inferior portion uniting the lung-sacs to the median mass of the septum trans versum. Now, as the liver expands laterally the ventral attachment of the accessory mesentery is carried out towards the lateral body-wall, inasmuch as its attachment is to the lateral superior face of the liver (cf. Fig. 231, Chap. XIII). Thus the accessory mesenteries are gradually shifted from their original almost sagittal plane to a plane that is approximately frontal. The developing lungs project dorsally from the accessory mesenteries, which may now be called the pleuroperitoneal membranes, into the pleural cavities (Fig. 189); and the latter communicate with the peritoneal cavity onl}^ laterally to the liver. These communications are then soon closed by a fusion betw^een the lateral edges of the pleuro-peritoneal membrane and the lateral body-wall; this fusion is not completely established on the eighth day, but it is on the eleventh day.

In reptiles and mammals the so-called mesonephric mesentery plays an important part in the closure of the pleural cavities. It arises from the apex of the mesonephros at its cephalic end, and fuses with the septum transversum. It thus forms a partition between the hinder portion of the pleural cavity and the cranio-lateral recesses of the peritoneal cavity. Subsequently, in mammals, its posterior free border fuses with the caudal bounding folds of the pleural cavity that arise as forwardly directed projections from the accessory mesentery on the right side and the wall of the stomach on the left. Hochstetter states that such a mesonephric fold is found in the chick but that it does not appear to play any essential part in the formation of the septum pleuro-peritoneale.


I find it in the chick as a very minute vestige at the cranial end of the mesonephros associated with the funnel of the Miillerian duct. It aids in the final closure of the pleural cavity by bridging over the narrowchink between the lateral angle of the pleuro-peritoneal membrane and the lateral body-wall. (See Bertelli, 1898.)

The oblique septum of birds arises as a layer split off from the septum pleuro-peritoneale (pulmonary aponeurosis or pulmonary diaphragm of adult anatomy) by the expansion of the anterior and posterior thoracic air-sacs within it. This mode of formation is clearly seen, particularly on the right side, in a series of transverse sections of a chick embryo of eleven days (Fig. 190). Thus the cavity between the oblique septum and the pulmonary diaphragm (cavum sub-pulmonale of Huxley) is not a portion of the bodv-cavitv and bears no relation to it. The ingrowth of muscles into the pulmonary diaphragm can be observed in the same series of sections. It begins on the tenth day according to Bertelli.

HI. The Mesenteries

The dorsal mesentery is originally a vertical membrane formed by reduplication of the peritoneum from the mid-dorsal line of the body-cavity to the intestine; mesenchyme is contained from the outset between its peritoneal layers, and serves as the pathway for the development of the nerves and blood-vessels of the intestine. In the course of development, its lower edge elongates with the growth of the intestine, and is thrown into folds, or twisted and turned with the various folds and turnings of the intestine. Detailed studies of its later development in the chick have not been published, but the principal events in its history are as follows: For convenience of description the dorsal mesentery may be divided into three portions corresponding to the main divisions of the alimentary tract, viz., an anterior division belonging to the stomach and duodenum, sometimes known as the mesogastrium; an intestinal division belonging to the second loop of the embryonic intestine that descends into the umbilicus; and a posterior division belonging to the large intestine and rectum. Inasmuch as the duodeno-jejunal flexure (Figs. 179 and 180, X) retains from an early stage a short mesenterial attachment, there is quite a sharp boundary in the chick between the first and second divisions of the dorsal


mesentery. The mesogastriiim becomes modified b}- the displacement of the stomach, the outgrowth of the duodenal loop, the formation of the omentum, and by the development of the pancreas and spleen in it. (See below.)

The second division of the mesentery is related to the longest division of the intestine, but as this arises from a relatively very small part of the embryonic intestine, its dorsal attachment is short and the roots of the mesenteric arteries are grouped together. The third division is relatively long and not very deep; at its base it approaches near to the mesogastrium, to which it is attached by the root of the intermediate division.

The Origin of the Omentum (mainly after Broman). In a preceding section we saw that the accessory mesentery is continued back on the right side (at the stage of seventy-two hours) by a fold of the dorsal mesentery of the stomach known as the plica mesogastrica (Fig. 120). The stomach is already displaced somewhat to the left, hence the dorsal mesentery is bent also, and the plica mesogastrica arises from the angle of the bend (Fig. 120). The ventral mesentery of the stomach, including the meatus venosus and liver, remains in the middle line. Thus the bodv-cavitv on the right of the stomach is divided into two main divisions, viz., the general peritoneal cavity lateral to the plica mesogastrica and liver, and another cavity between the plica mesogastrica and liver on the one hand, and the stomach on the other; the latter cavity has two divisions, a dorsal one between the plica mesogastrica and upper half of the stomach (recessus mesenterico-entericus) and a ventral one between the liver (meatus venosus) and stomach (recessus hepatico-entericus), which are continued anteriorly into the pneumato-enteric recesses. Subsequently, they Ijecome entirely shut off from the peritoneal cavity, but at present (stage of Fig. 120) they communicate with it by a long fissure bounded by the accessory mesentery in front, by the plica mesogastrica above, and the meatus venosus below; this opening may be called the hiatus communis recessum; it corresponds to the foramen of Winslow of mammals (cf. Fig. 193 A).

As development proceeds, a progressive fusion of the right dorsal border of the liver with the plica mesogastrica takes place in a cranio-caudal direction, thus lessening the extent of the^ hiatus.


At about ninety-six hours, the pUca mesogastrica divides to form two longitudinal folds, in the lateral one of which the vena cava inferior develops (cf. Fig. 193 B) ; it is hence known as the caval fold; the more median division is the coeliac fold including the coeliac arter}^ Between them is a subdivision of the recesses known as the cavo-coeliac recess, which corresponds to the atrium burs£e omentalis of mammals. The fusion of the right lateral border of the liver continues along the course of the caval fold, and the vena cava inferior is soon completely enveloped in liver tissue. Behind the point where the vena cava inferior enters the liver, the latter fuses with the ventral edge of the right mesonephros, thus progressively diminishing the opening of the collective recesses into the peritoneal cavity. At about the one hundred and sixtieth hour, the fusion reaches the portal vein, and the recesses are thus completely shut off from the peritoneal cavity. Thus a lesser peritoneal cavity is completely separated on the right side of the body from the main cavity; and from the former both lesser and greater omental spaces develop on the right and left sides respectively of the coeliac fold. (Bursa omenti minoris and bursa omenti majoris of the bursa omentalis dextra.)

The communication of the lesser and greater omental spaces in front of the coeliac fold is closed by fusion of the latter with the right side of the proventriculus at about the one hundred and sixtieth hour, though it remains open throughout life in some birds. The two omental spaces are also elongated in a posterior direction by the caudal prolongation of the right lobe of the liver and of the gizzard respectively (Fig. 195). The lateral wall of the omentum minus is attached to the lateral dorsal border of the right lobe of the liver as already described, and it is therefore carried back by the elongation of this lobe; but as the vena cava inferior is inserted about the middle of this wall and cannot be drawn back, it results that there is a deep median indentation of the lateral wall of the omentum minus, at the bottom of which lies the vena cava inferior.

The condition of both right and left omental spaces at 154 hours is shown in Figures 195 and 196. Subsequently, about the eleventh day, the mesogastrium behind the spleen becomes perforated, and the greater omental space thus opens secondarily into the left side of the body-cavity. A true omental fold exists only for a short time in the development of the chick, and is



soon taken up by the caudal elongation of the stomach. Obliteration of the cavity of the omentum by fusion of its walls takes place at its caudal end. (Broman.)

Spaces corresponding to the omental cavities are also formed on the left side of the body, but they are of much less extent. (See Fig. 196.) The communication of these spaces with the greater peritoneal cavity is not, however, shut ofT as on the right side. However, a secondary and later fusion of the left lobe of the liver with the lateral body-wall, and of the gizzard with







Fig. 195. — Recon.struction of the omental space of a chick embryo of 154

hours from the right side. (After Broman.)

Bomaj., Bursa omenti majoris. Bomin., Bursa omenti minoris. Du., Duodenum. Giz., Gizzard. Her., Hiatus communis recessum. oe., (Esophagus, rBr., Right bronchus. Rpedx., Right pneumato-enteric recess.

the ventral body-wall does isolate a portion of the peritoneal cavity from the remainder on the left side. Into this the pneumato- and hepato-enteric cavities of the left side open; however, it is obvious that this space is not analogous to the omental spaces on the right.

Origin of the Spleen. The spleen arises as a proliferation from the peritoneum clothing the left side of the dorsal mesentery just above the extremity of the dorsal pancreas. This proliferation forms the angle of a cranio-caudal fold of the dorsal mesentery which is caused by the displacement of stomach and intestine to the left side of the body-cavity (Fig. 188), and which is exaggerated by the rapid growth of the dorsal pancreas (Choronschitzky). The spleen is thus genetically related to the wall of the great omentum, and lies outside the cavity of the latter. The cells of the spleen are proliferated from a peritoneal thickening, which may be compared in this respect to the germinal epithelium. It is recognizable at ninety-six hours, and the mass formed by its proliferation grows rapidly, forming a very considerable projection into the left side of the body-cavity above the stomach, at six days (cf. Fig. 197).

Fig. 196. — The same model from the left side. (After Broman.) Hrpesin., Hiatus recessus pneumato-entericus sinister. 1. Br., Left bronchus. Pr'v., Proventriculus. Rhesin., Recessus hepatoentericus sinister. Rpesin., Right pneumato-enteric recess. Other abbreviations as in Fig. 195.

According to Choronschitzky, the peritoneal cells invade the neighboring mesenchyme, and, spreading through it, form an illdefined denser area, the fundamental tissue of which is therefore mesenchymal. The meshes of the latter are in immediate continuity with the vena lienalis, but the vascular endothelium is not continued into these meshes. Thus free embryonic cells of the primordium of the spleen enter the venous circulation directly, and become transformed into blood-corpuscles.

On account of the intimate relation between the pancreas and spleen in early embryonic stages, certain authors (see esp. Woit) have asserted a genetic connection, deriving the spleen from the pancreas. There is, however, no good evidence that the relation is other than that of propinquity.

Fig. 197. — Photograph of transverse section through a chick embryo of 8 days. A. o. m., Omphalomesenteric artery. Du., Duodenum. Giz., Gizzard. Gon., Gonad. II., Ihum. M. D., Miillerian duct. Pc, Pancreas. V. umb., Umbilical vein.

It should also be noted that the absence of rotation of the chick's stomach (as contrasted with mammals) and the lesser development of the great omentum appear to be the causes of the more primitive position of the spleen in birds as contrasted with mammals.

Lillie 1919: Introduction | Part 1 - 1 The Egg | 2 Development Prior to Laying | 3 Outline of development, orientation, chronology | 4 From Laying to Formation of first somite | 5 Head-fold to twelve somites | 6 From twelve to thirty-six somites | Part 2 - 7 External form of embryo and embryonic membranes | 8 Nervous system | 9 Organs of special sense | 10 Alimentary tract and appendages | 11 The body-cavities, mesenteries and septum transversum | 12 Later development of the vascular system | 13 Urinogenital system | 14 Skeleton | Appendix | Frank Lillie

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