Paper - On the development of the pericardiaco-peritoneal canals in selachians (1918)

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Goodrich ES. On the development of the pericardiaco-peritoneal canals in selachians. (1918) J Anat. 53(1): 1-13. PMID 17103854

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This 1918 paper by Goodrich describes development of the pericardiaco-peritoneal canals in selachians.

Modern Notes: respiratory | coelomic cavity

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On the Development of the Pericardiaco-Peritoneal Canals in Selachians

By Edwin S. Goodrich, F.R.S.,

Fellow of Merton College, Oxford


It is well known that in the Selachians the pericardial cavity in the adult communicates with the coelom of the trunk or peritoneal cavity by a pericardiaco-peritoneal canal. This canal, first described and figured by Monro() in the skate, starts from a median opening in the hinder wall of the pericardium, between the oesophagus and the sinus venosus, and passing into the ventral wall of the oesophagus soon divides into two branches which have right and left slit-like apertures leading into the peritoneal coelom.

Balfour, in his monograph, “On the Development of Elasmobranch Fishes” (1), wrote that “Immediately in front of the liver the splanchnic and somatic walls of the body come into very close contact, and I believe unite over the greater part of their extent. The septum so formed divides the. original body-cavity into an anterior section or pericardial cavity, and a posterior section or true body-cavity. There is left, however, on each side dorsally a rather narrow passage which serves to unite the pericardial cavity in front with the true body-cavity behind... .The two lateral passages spoken of above probably unite in the adult to form the passage connecting the pericardial with the peritoneal cavity, which, though provided with but a single orifice into the pericardial cavity, divides into two limbs before opening into the peritoneal cavity.” To this statement he added in his text-book “The origin of these communications has not however been satisfactorily worked out’’(2). Balfour’s view of the origin of the canal was generally accepted until Hochstetter, in 1900, published an elaborate paper on the subject (3) in which he claimed to prove that the early communication between the two cavities becomes completely closed, and that the canal opening from one to the other in the adult is a new formation. No other meaning can be given to the statement made in the above-mentioned paper and repeated later in Hertwig’s Handbuch(4) that the pericardiaco-peritoneal canal of the adult ‘sist somit nicht der Rest einer urspriinglich bestehenden Kommunication zwischen den beiden in Betracht kommenden Leibeshéhlenabschnitten, sondern eine sekundare Bildung.’ According ‘to Hochstetter, then, the paired passages of the embryo (ductus pericardiaco-peritoneales) situated dorsally to the ductus Cuvieri, and separated from each other by the median mesentery enclosing the oesophagus, are closed up by the fusion of the splanchnic layer of the oesophagus with the somatic wall, “‘so sind auch die Ductus_ pericardiaco-peritoneales verschlossen.”” The adult canal, on the other hand, he states, is developed from a backwardly growing diverticulum of the pericardial wall, which, passing between the oesophagus and the sinus venosus, gives rise by a very complicated process of growth to a bifurcating passage leading into the peritoneal cavity. Yet I have sought in vain in Hochstetter’s somewhat confused and obscure description and in his figures for any definite evidence either of the complete obliteration of the dorsal openings, or of the formation of new openings from the diverticulum.

As the matter seemed to me of some interest I examined the very large collection of sections now available in the Department of Comparative Anatomy of the University Museum in Oxford, not only of Acanthias, the species studied by Hochstetter, but also and more particularly of Scyllium canicula, as well as of other forms. A few gaps in quite late stages leading to the adult structure I have been able to fill from some excellent series kindly lent by my friend Professor J. P. Hill, and for the loan of one series of Acanthias I am indebted to Professor A. Dendy.

It may be said at once that the result of these researches is to show that Hochstetter is mistaken in his interpretation, and that Balfour’s original view is essentially correct.

First Subdivision of the Primitive Coelom

The first indication of a division of the coelom into pericardial and peritoneal regions appears about Stage J of Balfour, figs. 1 and 2. Here, before the longitudinal somatic veins (future cardinals) have established a communication with the suboesophageal vein (future sinus venosus), the somatic wall is seen in transverse sections to be closely applied to the splanchnic wall at the sides of the oesophagus, cutting off two passages above from two passages below. The former are separated by the dorsal mesentery, the latter by the remains of the ventral mesentery or mesohepatic ligament. Moreover the splanchnic mesoblast is already forming paired longitudinal ventro-lateral ridges running forwards for a short distance on the dorsal surface of the sinus. These ridges vanish in front, but merge behind with the broad mesentery where the ventral wall of the oesophagus joins the posterior end of the developing heart. Later on, when fusion of the somatic and splanchnic walls allows the ductus Cuvieri to become established across the coelom, in what Balfour called the horizontal septum and Koelliker the mesocardium laterale, the ridges grow into pronounced upstanding folds extending from the sides of the oesophagus to the sinus. The ductus Cuvieri develops about the level of the 5th metaotic myotome (Somite 9). Figs. 3, 4 and 5 show these structures reconstructed from transverse sections at Stage L.

Fig. 1. Transverse section of an embryo Scyllium canicula, Stage I, in the posterior pericardial region, showing the origin of the lateral mesenterial folds, /f.

Fig. 2. Transverse section of the same embryo in the region of the sinus venosus, sv, showing the formation of the horizontal septum (mesocardia lateralia).

Figs. 3, 4, and 5. Embryo Scyllium canicula, Stage L. Transverse sections viewed from in front. Fig. 3, section through the median pericardial depression, dp, between the two lateral mesenterial folds. Fig. 4, section farther back through the mesocardia lateralia and ductus Cuvieri. Fig. 5, reconstructed thick section of same region, beginning in front of that drawn in fig. 3. .

The further development of the anterior mesenterial folds is illustrated in fig. 7 or Stage N and in fig. 6 reconstructed from transverse sections of an embryo Torpedo 14 mm. in length. The folds may be considered as merely right and left outgrowths of the front edge of the suboesophageal mesentery (omentum minus, ligamentum hepato-entericum) forming here the hinder wall of the pericardium. There is necessarily a depression between them, ending blindly behind but open to the pericardium in front. It is this depres 1-2 ‘ys Fic. 6 Fie. 7

Fig. 6. Reconstructed thick transverse section through the posterior pericardial region of an embryo Torpedo ocellata, 14 mm. long. Anterior view; heart removed.

Fig. 7. Similar section of an embryo Scyllium canicula, Stage N, 20 mm. long; showing the mesohepatic Hgament, m.h., and the anterior face of the liver, J.

Figs. 8 and 9. Reconstructed thick transverse sections of an embryo Scyllium canicula, 25 mm. long; anterior views. The dotted line in fig. 8 fits on to the front of fig. 9. The dotted line in fig. 9 represents the most posterior section.

sion, erroneously labelled liver by Balfour in his figure (fig. 852, 2), that Hochstetter held to be the rudiment of the adult pericardiaco-peritoneal canal. It does not really grow backwards to open into the peritoneal cavity, as that author believed; but, owing to the relative shifting of parts in the process of growth, comes to lie behind the ductus Cuvieri, which itself has by this time shifted backwards from the level of the 5th to that of the 7th myotome. The enlargement of the heart and gills is probably to a large extent responsible for the shifting.

Development of the Septum Transversum and Closure of the Ventral Coelomic Passages

Concerning the formation of the septum transversum cutting off the pericardium from the peritoneal cavity below the ductus Cuvieri there is now little difference of opinion. Briefly it may be described as follows. Of the primitive ventral mesentery, originally complete in very early stages, there remains in this pericardial region at stage I only a narrow strip passing obliquely backwards from the oesophagus to the ventral body-wall and known as the mesohepaticum anterius (future posterior wall of the pericardium and falciform ligament). The sinus venosus lies on its front face, the liver on its posterior face, and the hepatic veins pass through it from one to the other (figs. 9 and 12). This mesohepaticum is a triangular mass of connective tissue with its apex pointing downwards. As the liver enlarges the connective tissue spreads over its anterior surface, and with the help of corresponding somatic ridges growing inwards from fi the body-wall and described by Hochstetter as the ‘Schlussfalte,’ gradually Fis. 10. Posterior view of a portion of a recon structed thick transverse section of an embryo closes the passage between the body- Scyllium canicula, 33 mm. long. The section wall and the edge of the liver (figs. 8 passes just in front of the liver, and shows and 9). The two holes shown in fig. 14 are the last remains of the communication persisting at this stage O appears through the septum transversum. (about 28 mm.) of Scyllium. the pericardiaco-peritoneal openings, pp, and suspensory ligaments of the liver, lig. The

outline of the ductus Cuvieri and sinus venosus

Meanwhile the liver becomes so to speak peeled off at the sides from the septum transversum by an ingrowth of the peritoneum, leaving it attached only in the neighbourhood of the hepatic veins above and the falciform ligament in the middle (figs. 10 and 16).

Development of the Suspensory Ligaments of the Liver

A dorsal hepatic ligament or suspensory fold (cranial hepatic ligament of Hochstetter(1)) is formed at each side as a ridge passing up just on the outside of the pericardiaco-peritoneal aperture, and on the inner or medial side of the descending Millerian funnel (figs. 10 and 14). Thus these ridges run on to the body-wall along the hinder surface of the mesocardium laterale; and become transformed into the suspensory folds of the adult liver, variously developed in different Selachians. Owing to their presence a right

Fig. 11. Reconstructed thick longitudinal section of an embryo Scyllium canicula, Stage N, 20 mm. long. Dorsal view. The oesophagus is almost entirely cut away leaving its ventral splanchnic mesoblast, sp; an arrow passes below it in the posterior pericardial region. On the left side the pericardial cavity is completely exposed; its posterior wall, formed by

- the diverging folds of the suboesophageal mesentery, is seen between the two arrows.

and a left hepato-enteric recess become cut off above the liver, blind in front but widely open to the general peritoneal coelom behind. In the embryo these recesses are at first separated from each other by the median suboesophageal mesentery; a condition I find persisting in Chlamydoselachus. In other forms. examined they are found to be continuous owing to the disappearance of the mesentery below the oesophagus (Cestracion, Acanthias, Torpedo); while in the Seylliidae a peculiar condition obtains, which will be described below *. 1

sf Fia. 13 Figs. 12 and 13. Inner views of the right half of the pericardial region of an embryo Scyllium canicula, 26 mm. long. In fig. 12 the section is cut to the left of the median mesentery through which a window has been cut to expose the Miillerian funnel, mf, and the root of the vitelline artery, ca. Behind the pericardiaco-peritoneal opening, pp, is seen the beginning of the left mesenterial fold. An arrow passes behind the mesohepatic ligament from the pericardial to the peritoneal cavity. In fig. 13 the section is taken to the right of the median mesentery and a part of the liver has been cut away exposing the somatic fold, sf. An arrow passes through the pericardiaco-peritoneal opening.

1 The suspensory folds here described. must not be confused with the pulmo-hepatic ligaments which pass on the inner side of the pericardiaco-peritoneal passages in air-breathing vertebrates.

Obliteration of the Dorsal Pericardial, Coelom, and Formation of the Definitive Pericardiacoperitoneal Openings

From figs. 14, 10, 8, it will easily be understood that, as has already been described by previous authors, the dorsal region of the pericardial cavity becomes obliterated from before backwards by the fusion of the dorsal and lateral wall of the oesophagus with the roof of the pericardium. In later stages the concrescence of oesophagus and somatic wall extends backwards beyond the pericardial region (fig. 16). But the concrescence does not completely close the original communication above the mesocardium laterale. This opening persists on either side, though reduced in extent, as a passage between the body-wall and the anterior mesenteric fold (figs. 8, 10,16).

Development of the Pericardiaco-Peritoneal Canals of the Adult

We have seen that at first the anterior mesenterial folds have between them a deep depression (figs. 5 to 9). During later growth, as the relative shifting of organs takes place, the front edge of the suboesophageal mesentery, together with the lateral folds, is dragged backwards with the lengthening oesophagus, and the folds which always form the inner and posterior limit of the pericardiaco-peritoneal openings are continually receding from the pericardium (fig. 11).

The next, and perhaps the most difficult point to determine, is how the anterior region of the suboesophageal mesentery with its diverging folds and ridges becomes converted into the ventral sheet of connective tissue, the ” ‘Verbindungsplatte’ of Hochstetter, which later constitutes the floor of the pericardiaco-peritoneal canal.

Already at Stage N the folds extend well behind the ductus Cuvier, and the openings come to assume a position at the sides of the oesophagus, almost exactly opposite and below the Miillerian funnels (figs. 7, 18, 14, 15). The development of the canals of the adult will be easier to understand if we first take the case of Acanthias where the conditions are much simpler than in Scyllium. It will be remembered that in Acanthias the median suboesophageal mesentery disappears in the adult, so that the suspensory folds of the liver enclose a single coelomic space. The pericardiaco-peritoneal canal passes backwards in the ventral wall of the oesophagus for a considerable distance, then divides into two branches which open on either side into the space just mentioned between the liver and the oesophagus a long way behind the limit of the short suspensory folds. Now the tissue in the fork at the junction of the branches of the canal represents the original posterior wall of the embryonic pericardium. In other words the anterior edge of the suboesophageal mesentery has shifted back from its original position above the septum transversum as the median canalelongated. Turning again to Scyllium, we find that the depression seen between the two anterior mesenterial folds at Stage L (fig. 8) becomes transversely drawn out (fig. 7) and finally extends over the lateral edge of the folds themselves. Meanwhile the ridge-like forward continuations of the folds mark off a median plate of tissue closely applied to the sinus venosus in front and the dorsal surface of the liver further back (figs. 10, 11, 14, 15). Thus the original floor of the depression becomes transformed into a nearly horizontal sheet running from the sinus backwards to the oesophagus, and destined to form the ventral wall of the canals. But we have still to account for the restriction of the pericardiaco-peritoneal openings to comparatively small narrow apertures situated far back in the adult at the ends of the two branch canals. At first the openings are bounded externally merely by the somatic wall (fig. 7); later by the developing hepatic ligament (fig. 14). Still later, as the openings are carried backwards, their antero-external margins are formed by a thin membrane growing from the septum transversum just on the medial side of the hepatic ligament (figs. 11 and 17). This membrane extends as the opening recedes on each side of the oesophagus in Acanthias.

Figs. 14 and 15. Posterior views of reconstructed thick transverse sections of an embryo ' Seyllium canicula, Stage O, about 28 mm. long, showing the obliteration of the dorsal coelom and the formation of the septum transversum. The posterior face of the section in fig. 14 passes just in front of the liver, and the dotted line in fig. 15 fits on to it. The top corners of the liver have been cut away.

Fig. 16. Posterior view of a reconstructed thick transverse section passing behind the septum transversum, st, of an embryo Scyllium canicula, 37 mm. long. The ventral region of the liver has been cut away.

Now, in the adult Scyllium the right branch of the pericardiaco-peritoneal canal is said by Hochstetter to be blind. Such, however, is not really the case, and his failure to find the right aperture is probably due to his having searched for it in the wrong place. For in Scyllium there is a marked asymmetry in. the relation of the mesentery and hepatic ligaments. On the left side are found the suspensory fold of the liver and the left branch of the pericardiaco-peritoneal canal with its slit-like opening as usual; but on the right side the suspensory fold appeats to be absent and the right canal opening to be suppressed. On the other hand the original median suboesophageal mesentery or lesser omentum is seen to persist, though passing up well on the right side of the oesophagus and apparently running on to the right lobe of the liver. The fact is that in Scyllium this mesentery, bent very much to the right by the gastric loop of the alimentary canal, has fused with the right suspensory fold. The opening of the right branch of the canal is consequently carried on to the outer lateral surface of the combined sheet of tissue so formed, where it is represented by a deep notch on the outer side of the membrane in front of the coeliac artery. The right branch of the canal is long and very narrow; but I have satisfied myself by means of injections that its opening persists even in the adult. It leads, then, not as on the left side into the suboesophageal region of the coelom, but directly into the lateral region of the general body-cavity. Steps in the development of this strange asymmetry are shown in figs. 11 and 17; they lead to a structure whereby the Scylliidae differ from many, perhaps from all, other Selachians. A comparative study of these membranes in the Selachii would probably yield results of considerable importance. The relation of the hepatic suspensory ligaments to the suboesaphageal mesentery and pericardiaco-peritoneal canals in Acanthias on the one hand, and in Scyllium on the other, is shown in the diagrams 4 and B of fig. 18.

Fig. 17. Dorsal view of a reconstructed thick longitudinal section of an embryo Scyllium canicula. about 35 mm. long, passing between the sinus venosus and oesophagus in front.

Summary and Conclusion

Balfour’s suggestion that the canal leading in the adult Selachii from the pericardial to the peritoneal coelom, and opening into the latter by paired apertures, is a remnant of the wide communication between these cavities in the embryo is correct. The canal openings are not new formations as Hochstetter maintained, but are derived from the pericardiaco-peritoneal passages above the mesocardia lateralia. The pericardium. is first of all delimited by the mesocardia lateralia, enclosing the ductus Cuvieri, and leaving two passages above and two passages below. The pericardium becomes cut off from the peritoneal cavity below the mesocardia by a complete septum transversum formed by the junction of paired somatic ridges with the mesohepatic ligament. The dorsal passages become restricted by the obliteration of the dorsal pericardial coelom, owing to the concrescence of the oesophagus with the roof and sides of the pericardium. They remain, however, as small pericardiaco-peritoneal openings situated at first opposite and below the Mullerian funnels.

Fig. 18. Diagrams showing the relation of the suspensory ligaments of the liver to the mesenteries and pericardiaco-peritoneal canals in an adult Acanthias, A, and Scyllium, B. Dorsal view in which the canals below the oesophagus are represented by dotted lines.

Between the oesophagus and the sinus venosus the hind wall of the pericardium is formed by the anterior edge of the ventral hepatoenteric mesentery, which hére divides into two diverging folds passing forwards as ridges on to the sinus venosus. The deep depression between these folds does not give rise to the adult pericardiaco-peritoneal canal, nor does it break through into the peritoneal coelom, giving rise to new openings as described by Hochstetter. Folds and depression are together carried backwards, and delimit the posterior margins of the openings throughout development. As the oesophagus lengthens they come to occupy a position on its ventro-lateral surface far behind the septum transversum. The anterolateral margin of the opening is at first formed by the body-wall, then by the hepatic suspensory ligament, and lastly by a membrane growing out from the surface of the somatic wall at the base of these ligaments. The floor of the canals is derived from the plate of tissue below the original depression in conjunction with the folds and ridges reaching on to the sinus. The fork of the two branches of the canal in the adult represent the original anterior edge of the suboesophageal mesentery in the embryo; while the anterior median canal is merely the posterior narrowed region of the pericardium between the sinus and the oesophagus.

While in Acanthias the development of these structures is approximately bilaterally symmetrical, and the mesentery disappears between the oesophagus and the liver, in Scyllium there is a marked asymmetry. For in this fish the right suspensory ligament of the liver combines with the persistent hepatoenteric mesentery in such a way as to bring the much reduced opening of the branch canal of the right side on to the outer surface of the mesentery. Hence this opening leads not into the suboesophageal coelom but directly into the lateral region of the peritoneal cavity, and seems on that account to have been missed by Hochstetter. The disposition of the mesenteries and suspensory ligament varies considerably in the different families of the Selachii, and a careful comparative study of these structures would probably yield results of taxonomic value.


a. aorta; a.c. anterior cardinal; b.d. bile duct; b.w. body-wall; c. conus arteriosus;,c.a. coeliac artery or root of vitelline artery; d. somatic veins or future ductus Cuvieri; d.c. dorsal coelom; d.c.p. dorsal coelomic passage; ductus Cuvieri; d.m. median dorsal mesentery ; dp. depression between diverging mesenterial folds; fl. floor of pericardiaco-peritoneal canal; g. ganglion; g.b. gall-bladder; g.s. gill-slit; 4.s. horizontal septum or mesocardium laterale; ht. heart; h.v. hepatic vein; J. right lobe of liver; J.f. left mesenteric fold; lig. suspensory ligament of liver; 1.1. left lobe of liver; .o. left. opening of pericardiaco-peritoneal canal; /..v. left somatic vein or future cardinal vein; J.v. lateral vein; m.d. Miillerian duct; m.f. Miillerian funnel; m.h. mesohepaticum anterius or falciform ligament; m.l. mesocardium laterale; ms.d. mesonephric duct; m.t. mesonephric tubule; .c. nerve cord; nt. notochord; 0. opening in septum transversum; oe. oesophagus; pa. pancreas; pe. posterior cardinal vein; pc.c. pericardial cavity; pc.w. pericardial wall; pf. pectoral fin; p.g. pectoral girdle; ph. pharynx; p.o. median pericardiaco-peritoneal opening into pericardium; p.p. lateral pericardiaco-peritoneal opening; p.p.c. median pericardiaco-peritoneal canal; r. ridge-like prolongation of mesenterial fold; r.f. right mesenterial fold; r.lig. right suspensory ligament of liver; r.o. right opening of pericardiaco-peritoneal canal; r.p.c. right pericardiaco-peritoneal canal; r.s.v. right somatic vein or future cardinal; s. somite; s.f. somatic fold or ridge of septum transversum; 8.g. sympathetic ganglion; s.m. suboesophageal lesser or hepatoenteric mesentery; sp. splanchnic wall of oesophagus; spl. pancreas; s.t. septum transversum; stm. stomach; 8.v. sinus venosus; v.g. vagus ganglion; v.a. vitelline artery; v.p.p. ventral pericardiaco-peritoneal passage; v.v. vitelline vein; y.d. yolk duct; y.s. yolk stalk.

List of References

(1) Baxrour, F. M. “A Monograph on the development of Elasmobranch Fishes.” Journ. Anat. and Phys. 1876-8.

(2) A Treatise on Comparative Embryology. London, 1881.

(3) Hocustetrer, F. “Ueber die Entstehung der Scheidewand zw. Pericardial- und Peritonealhohle u. iiber die Bildung des Canalis Pericardiaco-peritonealis bei Embryonen von Acanthias vulgaris.” Morph. Jahrb. n. 29, 1900.

(4) —— “Die Entw. des Blutgefass-systems,” Hertwig’s Handbuch d. Entw. der Wirbeltiere.

(5) Monro, A. Structure and Physiology of Fishes. Edinburgh, 1783.

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