Paper - Comparative development of the coelom (1901)
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Mall FP. Comparative development of the coelom. (1901) Ref. Handb. Med. Sci. 3: 166-171. PDF
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 See also: Mall FP. Development of the human coelom. (1901) Ref. Handb. Med. Sci. 3: 171-189. PDF
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Comparative Development of the Coelom
Introduction
In all vertebrates the primitive intestine forms two sets of diverticula which are destined to become permanent tissues, (1) one toward the medullary groove winch forms the chorda dorsalis, and (2) two lateral diverticula which form the body cavities. These latter are later on subdivided into pleural, pericardial, peritoneal, and other cavities. A detailed description of the theory of the formation may be found in Balfour's work, in Hertwig's "Embryologie," and in Minot's "'Human Embryology."
Fig. 1390. — Transverse Section thrrmpli tin: I'Dsterior Ri-sidn of a Chick, with Six Pairs of Jlyntonics. (After Wnhlcyei'. troiii Minot.) Kc, (^ctoiterrti ; Mes.^ mesoderm; Ent., entoderm; 3/'/., nu'diillary trroove.
When sections are made through very young embryos of higher vertebrates, just after tlie bhistodermic; nieniljranes are well formed, a solid mesoderm is found, as shown in Fig. 1390. Although in lower vertebrates the mesoderm is produced by lateral divertietda from the entoderm, which are hollow from the beginiiiug, in hi,i;lici- vertebrates the mesoderm is first laid down as a snlid mass of cells. Soon the cells of the mesoderm on either side of the chorda divide into two layers, the somatopleure and the splanclmopleure (Fig. 1391, Soin. and Spl.). From the two lateral cavities lietween these two layers the pen toneal cavity is formed.
The more accurate early forniaticin of the pleuro-perioneal cavity in its relation to the other organs, we find carefully studied by Budge, who by means of injection followed it in the chick. With a tine hypodermic syringe he filled the various spaces of the coelom as they appeared, thus showing very clearly the extent of this cavity in various embryos. The splanclmopleure, according to Budge, may be split into two layers, a dorsal or lymphatic and a ventral or vascular. As the first blood-vessels are formed, lymph vessels appear on their dorsal side, which flow together to form networks and accompany the primitive veins to the axial part of the germinal area. Here the lymphatics form two spaces, one on either side of the body, which are soon united by a bridge, or rather duct, on the ventral side of the heart. Therefore, in birds at least, the primitive pleuro-peritoneal cavity appears somewhat as an H, the uprights of which are on either side of the body, and the cross-piece on the oral side of the sinus venosus. In its further development the sinus venosus grows to the dorsal side of the cross piece, thus reversing the relation of the vascular system to the lymphatic, or rather codomic system. The uprights of the H fall to the outside of the body and are swallowed \i\) in the foiniationof the aiimion. Fig. 1392 is a ei-oss-section fnim a ehiek at tliis si age, :uhI shows that tlie greater portion of the cavity is now on the outside of tlie body. The ci'oss-piecc of the H is immediately on the ventral side of the heart, and forms the cavity of the pericardium Ijy the heart growing into it. Its communication with the remaining coelomic cavity is later on cut oil in higher vertebrates, wliile in lower vertebrates it may remain open.
According to Budge lv.n diverticula grow from the cross-piece, one on either side of the chorda, toward the tail of the body, and form the primitive pleuro-peritoneal cavities. Budge's paper was published from fragmentary notes after his death, and I am certain that the above statement is not correct. Professor His has placed before me Budge's specimens, which I think show conclusively that the interpretation of his injections is not correct. Most of his injections were made into the amniotic fold as the amnion was forming. Cross-sections of embryos show that on either side there is a large cavity (Fig. 1392, Som.) which communicates freely with the iDleftro-peritoneal (6'«!). Before the amnion is complete we have lateral cavities on either side of the body, communicating with each other only by means of the cross-piece on the ventral side of the heart. This is the freest portion of the communication, which also communicates most freely with the pleuro-peritoneal cavities (Pig. 1393, Coe). In many embryos the injection passed from the cross-piece into the pleuro-peritoneal cavity and would not extend out into tlie amniotic portion of the ccelom, thus malcing it appear as if the pleuro - peritoneal cavities were, so to speali, diverticula projecting directly from tlie cross-piece or pericardial cavity. Transverse sections, however, give the picture of Fig. 1393. Surface views could not decide that these two cavities united directly, and these sections were made no doubt after the writing of a rough draft of his manuscript. Therefore, instead of stating that the two pleuro-peritoneal cavities arise as independent diverticula, we must say that they are pinched off from the coelomic cavity after the amnion is formed
Fig. 1391. — Transverse Section of a Chick of the Second Day. (Alter Waldeyer, from Minot.) Sum., Somatic mesoderm ; Sp(.. splanchnic mesoderm ; jEc, eitoderm ; Kiit., entoderm ; VJ'.. vein ; jr., Wolfllan duct ; Md., medullary canal : Au., aorta; C/i., chorda; M.S., myotome.
Fig. 1392. — Section throueh the Body of a Chick of the Third Day. (After Minot.) Cli., Chorion ; ,4m., amnion ; Som., somatopleure ; v., hlood vessels ; Coc, coelom; Spl., splanchnopleure ; In., intestine; au.. aorta; Wd., Wolffian duct; Year., vena cardinalis ; (li.d., chorda dorsalis ;" My., myotome ; Md., medullary canal.
Fig. 1393. — Section of a Chick, to show that the Plea-peritoneal cavity is cut off of the coelomic leaving a portion in the Amnion. Tbe embryo has been injected, but the fluid of the two cavities has not flowea together.
The coelomic cavities which are so intimately united with the lymphatic system unite and again divide into sections, thus forming the various compartments of the visceral cavity of higlier vertebrates. In all of tlie vertebrates the heart, as it is developing, hangs into the ventral transverse portion of the cavity, or the primitive pericardial cavitv. This is shown diagrammatically in Figs. 1394, 1395, "1396, and 1397, P.
Figs. 1394 to 1397 show the very early condition of things; the coelomic cavities are united by the cross-piece or the primitive pericardial cavity. The dotted lines (Fig. 1394) mark what portion of the cavity is taken up in the amnion (A. P.), while the remaining middle portion (P. P.) becomes the pleuro-peritoneal. Figs 1395, 1396 and 1397 show in succession the more advanced stages. In higher vertebrates the pericardial cavity is completely closed olT from the pleuro-peritoneal, but in elasmobranch fishes a communication between tlicm exists in the adult. The separation of the pericardial cavity from the pleuroperitoneal is aided materially by the heart growing over to the ventral side of the body, as shown in Fig. 139S. Sections through various parts of the same embryo, from which Fig. 1398 is taken, are shown in Figs. 1399" to 1404. In none of these sections is the communication between the pericardial and pleural cavities shown, but sections nearer the head contain it.
A cast of the coelomic cavity of this same embryo is given in Fig. 1405. There is only a slight communication between the pericardial cavity and the pleuro-peritoneal. The groove in the cast marked M indicates the position of the simple mesentery. Its relation to these organs is better shown in the sections (Figs. 1 399 to 1404). Fig. 1400 represents a section through a chick at an earlier stage of development, in which the duct (Dmniiinicating bel ween tlie pericardial and pleural cavities is cut longitudinally.
Thus it is seen that the heart first grows into the primitive pericardial cavity, which is nothing else than the cross-piece of the H already spoken of. The pericardial coelom grows larger and larger, at the same time hanging as it were over the ventral side of the body, and is soon connected with the pleuro-peritoneal cavity only by two ducts, which later on become closed in the higher vertebrates.
In early embryos the veins enter the lieart behind, and not in front, as is the case in higher animals. The heart in its whole development undergoes a half-revolution, and in this way the twists, etc., are formed. Before the pericardial cavity is shut ofE from the pleuro-peritoneal the large vessels enter front behind. They are embedded in a mass of mesoblastic tissue which is encroaching upon the pleuro-peritoneal cavity, and has been termed by His the transverse septum. This, by its further growth, forms the diaphragm of higher animals (Figs. 1395, 1396, 1397). In lower animals only a rudimentary diaphragm, or none at all, is present. By the formation of Ibe diaphragm the pleuro-peritoneal cavity is divided into a smaller anterior portion, the pleural, and a larger posterior portion, the peritoneal. The lungs now grow into the iileural, as shown in an early stage in Fig. 1406, and in a somewhat later stage in Fig. 1399. The peritoneal cavity is at first composed of two distinct portions, one oil either side of the intestine, which in lower animals is quite a straight tube, lying in the middle line of the body. Soon, however, two communications are found between the two lialves, one in front and one behind the omphalo-mesenteric vessels (Fig. 1399, 0). These openings enlarge more and more as the intestine becomes more convoluted, and soon flow together, severing completely the omphalo-mesenteric vessels and duct. A portion of the duct may, however, remain in connection with the small intestine to form the diverticulum of Meckel.
Figs. 1394, 1395, 1396, and 1397.— Diagrams to Show the Development of the Coelomic Cavitv. P.P., Pleuro-peritoneal cHvlty ; A. P., portion of the coelomic cavity swallowed up In the amnion ; P., t.ericajflial amty ; L., i)leunil cavity ; O.N.. gastric diverticula, right and left ; D., position of itie diapiiragiii ; L.d.lK. left gastric diverticulum ; H.G.D., right gastric divprtii'uUiin 111' lesser peritnncal cavity ; F.W., foramen of Wlnslow ; G.P.C greater peritoneal cavity ; T., tuuica vaginalis.
Fig. 1398. — Reconstruction of a Human Embryo. (Enlarged 16 times, viewed from the left side.) P., Pericardial cavity ; 1, 2, 3. and 4, branchial pockets; A.D., descending aorta; A., auricle; V., ventricle ; 1/., lung ; S., stomach ; P., pancreas ; M., mesentery ; Jv., kidney ; W.D.. Wolffian duct ; O., openings through which the right and left peritoneal cavities communicate.
As the organs grow the peritoneal cavity surrounds them more or less completely, until the condition of things as seen in the adult is produced.
In lower vertebrates the peritoneal cavity remains quite simple, but in reptiles, birds, and mammals it may become (luite complex. Especially is this true regarding the birds, in which these divisions are greatly complicated by the growth of the air sacs from the lungs.
The first trace of the lesser peritoneal cavity is seen in the reptiles. Ravn has shown that in the lizard there are two diverticula from the peritoneum, one on either side of the stomach. From the one on the right side the lesser peritoneal cavity of mammals arises. In general the relation of the lesser peritoneal cavity to the greater is much like what is shown in Fig. 139,^. In the true sense of the term there is no lesser cavity, but only the two pouches. These are already present in the embryo, and in the adult they retain their embryonic appearance.
In birds the conditions become more complex. They appear in the chick during the third day of incubation. A section of the chick at this stage is given in Fig. 1406, G.D., making the lesser cavities, or, as they may better be termed, the right and loft gastric diverticula. At the beginning of the f(nirth day the gastric diverticula become larger, and on transverse section semicircular. Figs. 1407 and 1408 are from casts of the cavities about the stomach of a chick of eighty-eight hours. The right is larger than the left and is markedly cup-shaped, and connects by means of a narrowed opening with the right pleuro-peritoneal cavity (Fig. 1407, F. W.). The two together enclose the proventriculus. On account of the relations of the opening of the right diverticulum with the blood-vessels, stomach, and liver, and also for reasons whicli find their basis in comparative anatoni}' and embryology, the opening can be nothing else than the foramen of Winslow.
Figs. 1399-1400. — Sections through a Human Embryo Twenty-six Days Old. (Y. 2.5 tlmes.l O., CEsophaffus ; S., stomach; I., intestine; P., pancreas B., bile duct ; A., aorta ; r., coeliac axis ; G., right gastric diverticulum ; F., foramen oj Winslow ; M., mesentery ; L., liver ; P portal vein U , umbilical vein ; H.. heart ; X.. bulb of the aorta. The pleuro-peritoneal cavity is colored blacif throughout.
On the left side the gastric diverticulum is much smaller, and in older embryos it disappears altogether.
In a chick of five days and sixteen hours (Pig. 1409) the right gastric diverticulum has about doubled all its dimensions, while the embryonic foramen of Winslow has become much more sliarply defined. At this time the liver has greatly increased in size, the right lobe being larger than the left, both lying auterioi- to the foramen of Winslow. The original position of the liver being behind the foramen, its rotation necessarily earries the hepatic artery and the portal vein around the foramen of Winslow — its adult position. "With the growth of the gizzard a space extends from behind the right gastric diverticulum along the dorsal side of this origan, and marks the beginning of the cavity of the g'reat omentum (0.). Nearly the whole of the right diverticulum now lies on the left side of the body; the same position is held by the proventriculus and the gizzard. The domestic fowl possesses three peritoneal cavities, completely sepafated from one another, and from one of them the lesser cavity ai'iscs. The communication i's by means of the foi-amen of Winslow. After the anterior abdominal walls are removed, two ventral cavities are exposed, separated from each other by a vertical longitudinal septiun. Into each of'tlic cavities hangs a lobe of the liver, while into the left the ventral surface of the gizzard projects. On the doisal side of the liver then; are, on each side, thiee air sacs — an anterior, a middle, and a posterior. The middle one is the smallest, and the posterior the largest, exlending as it d.>es thi-ougliout the postei'ior portion of the abdominal cavity. Each sac communicates by means of a special opening dire'etlv into the hnigs. By allowing tile .sacs to collapse we tind that a very distinct meniliranc pnijccls 'hackM-ard from the gizzard and cuts oil the portion of the abdominal cavity containing the intestines I Ins IS the " pscudo-eiiiplodn " described by Weldou ami followed more extensively by Bed are separated from the posterior sac on the same side, a slit is shown which extends anterior and dorsal to the hepatic veins. Here it communicates by means of a round opening, about 1 cm. in diameter." with a large cavity lying on the median and dorsal side of the proventriculus and extending to the spleen. The cavity does not extend on the dorsal side of the gizzard. In all repects it corresponds with the right gastric diverticulum of embryos and with the lesser peritoneal cavity of mammals.
The relation of the embrvonic omentum with the "pseudo-epiploön" is as yet unknown. However I think it probable that the one is changed into the other and that the "pseudo-epiploön " will prove to be the true epiploon homologous with the same in mammals We
Fig. 1405. — Corrosion Preparation of the Pleuro-perltoneal Cavity of an EmbiTO Twenty-six Days Old. (X 22 times. I P., Pericardial cavity ; ^1., opening for the aorta ; V., opening for the vein • L space over the Uver ; 21., slit for mesentery ; Tl'.B., space for lYolQlan body.
Flc. lirili.— Section thronph tlic l(cf;i(,n of tlic Heart (,f a ciiic k of Seventy ii,,iirs
'■:i.. limes.) Tlicseetinn
strikes 11 nil i.,„| i,f III,.
n-astrlcrtlverticulumi; It and tliB tips of tlie imil mnnm-y buils, L. A few .sections deepeithe Kastric ■ di\erticula I'oinminiieate with the pleuiij-iicritoneal cavity. H., Iieart; /) r ductus Ciivii-ri ; B i ' bultius aorUe. ' "
derd. A similar membrane is present in the crocodile. In all respects, this mcmbniue is situated in the same position as is the c]iiploou in mammals, with the difference that it is adherent to the abdominal walls along its free border. On the dorsal side of the gizzard the air sacs fill all the space, thus closing off the communication between the cavity in which the intestines lie and the ventral cavities. When the anterior and middle air sacs on the right .side
Figs. UO? and 14( is. —Corrosion Preparations of the Rlpht and Left Gastnc Diverticula of a Chii/k Eiglitv-eieht Hours (lid. ( ■ Zi times ) P.P., Plenro-peritoneal cavity ; R.d.T).. right gastric diverticulum • -L.Cr.£)., left gastric diverticulum; L., position of lung; FW foramen of Winslow.
Fir.. IKBl.-Corrosion Preparation of the Right Gastric Diverticiiliim
Fig. Uin.— Corrosion Preparation of tiie (iastrio nivertlL-uliun ol a Huiiian Emliryo, T iiim. long. (X 35 timns.) !>.['., Plem-n-peritoneal oavlty: F.W., fmaniea of Wiuslow ; G.D., gastric diverticulum.
imist imagine cmly tlie embrvdiiic omeutiim attachiiia: itself Oil the sides (if tlie abddiueii followed by a lo.ss u'f the epiploouic cavity. A subsequent growth of the air
sacs backward fioni the doi'.sal side of the stomach will produce the condition found in the adult.
In mammalian embryos, while the stomach is still upri.t;'ht, oidy one gastric diverliculum is found. It is on the right side in Figs. 13119 to 1-101, which are taken fi-om a young human embryo. In each drawing the cadomic cavity is colored black and the position of the section can be made out by the organs which are cut across in the section. A east of the cavity is shown in Fig. 140.5. The portion of the cavity on the right side of the stomach and the liver IS shown in Fig. 1410, which is taken from a cast also. Figs. 1399, 1400, and 1401 show .sections through the gastric diverticulum of Fig. 1410. Fig. 1401 being through the foramen of Winslow.
The general form of the cavities is shown in Fig. 1410, which is taken fi-om a rescoustruction of a human embryo. The peritoneal cavity suri-ounds the Wolffian body, intestine, oraphalo-mesenteric vessels, stomach, hver, and lungs, with the addition of the right gastric diverticulum.
In lower mammals, according to Ravn, there are two diverticula; so the symmetric'al arrangement of these cavities in reptiles, is still indicated in the mammals. It is so insigniUcant, however, that we need not take it into considei'ation.
The fate of the right gastric diverticulum of mammals has been studied in the dog, and it has been found that it is converted directly into the lesser peritoneal cavity, much as is shown in Figs. 1396 and 1397. In a dog's embryo, li mm. long, the diverticulum is much like what it is in the human embryo of about the same .size (Fig. 1410). Adogembiyo, lb mm. long, shows a picture more advanced, much like what is seen iu the chick of five days (Fig. 1409). In a later stage (Fig. 1411) the stomach has been twisted about, holding in great part the adult 5.D.
Fio. 1411.— Corrosion Preparation of the Stomach, Intestines, and Lesser- Peritoneal Cavity of a Dog, i:3.5 mm. Long, Viewed from the Left Wide. (X 15 times.) The lesser peritoneal cavity has been filled with metal. B.D., Bile duct; P., pancreas; C, caecum ; O., omentum; F.JV., foramen of Winslow ; L.S., position of lobus Spigelii.
position. The liver, which before lay on the ventral side of the stomach, now^ lies in front, and to a great extent on the dorsal side of it. A model of these parts from a 10-mm. embryo, simply rotated to throw the stomach away from the mouth, gives the condition of things as they exist in the embryo 13 mm. long.
Fig. 1411 shows the lesser peritoni-al cavity as a cast stuck m behind the stonuich. The inb-stiiie is composed of two loojis, one from the stomach, I'Xb'nding inio (he pelvis, and the other from the ca'Cuni into the "imibi Ileal cord. The rapiil growth of the lai-ge inlestinehas thrcjwn the ca'cum as high as the stomach and to the riglit of it The fold of mesogastrium coming fi-om the dorsal side of the stomach passes over the large inlestine to form the omentum (Fig. 1411, 0.). The general shape of the lesser
Fig. 1413. — Section through the Foramen of Winslow and Lobus Spigelii of a Dog, 13.5 ram. long. (X :36 times.) A., Aorta; ,'^., stomach ; P., portal vein ; C., umbilical vein ; L.S., lobus Spigelii ; o., omental i.-avity ; LJ., large intestine.
peritoneal cavity is shown in transverse section in Fig. 14ia, which can be compared with Fig. 1401. The Sshaped loop of intestine is cut acro.ss three times, and the lesser peritoneal cavity with the foramen of "Winslow is shown throughout its w hole extent.
The omentum from now on rapidly grows over the wiiole ventral wall of the abdominal cavity, and iu man adheres to the colon as tirst described by Sleckel.
A resume of the comparative development of the coelom of the embryo is given in Figs. 1394 to 1397.
Franklin P. Mall.
See also the following paper: Mall FP. Development of the human coelom. (1901) Ref. Handb. Med. Sci. 3: 171-189. PDF
Bibliographical References
1 Reichert: Abhandl. d. kgl. Akad. d. Wiss., Berlin, 1873.
2 Von Spee ; His's Archiv, 1889 ; Mall : Anatom. Anzeiger, 1893 ; Johns Hopkins Hospital Bulletin, 1893 ; von Spee : Hls's Archiv, 1896 ; Siegenbeek von Henkelom : Hls's Archiv, 1898 ; and Peters ; Einbtttung des mensch. Eies, 1899.
3 Bischoff: Entwicklungsgeschlchte des Hundes Eies, Braunschweig,
BischoiI: Entwicklungsgeschlchte des Kanincheu Eies, Braunschweig, 1843. » Selenka : Studien liber Entwicklungsgeschlchte der Thiere, Heft . 5, Wiesbaden, 1893.
• Mall : Anatom. Anz. viii.
' Mall : Journ. of Morph., vol. v.
8 Mall : His's Archiv, Supplement Band, 189/.
» Hoen ; Johns Hopkins Hospital Bulletin, 1896.
1" Mall : Journ. of Morph., vol. xli.
11 Bischoff : Entwlckl. d. Meerschweinschens, Giessen, 1853.
12 Rauber- Sitzungsber. d. Naturforscher (iesellsch,, Leipzig, 1875.
13 Selenka : Studien iiber Entwlckl. d. Thiere, Heft 3. 1884- ,^^ n Selenka : Studien, etc.. Heft .5, Erste und Zweite Halfte, 1891, 1892. 15 His's Archiv, 1889 and 1896.
"Selenka : Studien, 1891, p. 201.
" Graf Spee : His's Archiv, 1896, Taf. 1., Fig. 1.
8 His : Anat. mensch. Embryonen, Theil i., p. 171.
i» Selenka: Studien, 1893, p. 209.
" Duval : Jour, de I'Anatomle et de la Physiologic, 1895.
= 1 Gohre : Selenka's Studien. etc., 1893, p. 218.
2'^ (iral Spee : His's Archiv, B«0 and 1896.
S3 Mall • A Human Embrvo of the Second Week, Anatom. Anz., Bd. 8 and Early Human Embryos and the Mo(Je of their Preservation, Johns Hopkins Hospital Bulletin, 1893.
21 His Anatomie mensch. Embryonen, Heft 3, 1883, and Interna^ tionale Beitriige zur wissenschaftllchen Medicin, Bd. 1, 1891.
25 Giacomini : Ergebnisse der Anatomie und Entwicklungsgeschlchte, Bd. 4, 1895. The original papei-s of Giacomini are in the Archives Ital'iennes de Biologle, vols, xvtii.-xxli.
2« Mall : Contributions to the Medical Sciences, Johns Hopkins Hospital Reports, vol. ix., Baltimore, ISIOO. ^ x,., , a
" Giacomini : Ergebnisse d. Anat. u. Entwicklungsgesch., Bd. 4, S. 636.
2" Mall : Anatom. Anz., 1893, and Jdhns Hopkins Hospital Bulletin,
2» Von Spee : His's Archiv, IWIIJ, PL i.. Figs. 4, 5, S, and 10.
=»GratSpee: His's .Archiv, 1KHI).
" Bonnet: His's Archiv, IWi).
^-Selenka: Stiidien, etc., Taf. xxxviii.. Fig. 3.5.
=' Drasch : Anatom. Anz., Bd. 9.
" Budge : His's Archiv, 1887.
^= Kollmann : His's Archiv, Supplement Bd., 1&S9, PI. v.. Figs. 1 and 3 ; von Lenhossek : His's Archiv, 1891, PI. i. ; Kollmann : His's Archiv, 1891, PI. lii.. Fig. 3.
^* Froriep : His's Arciiiv, 188;i and 188(5.
^' Piatt : Bulletin ot the Museum of Comparative Zoology, vol. xvli.
3" Dexter: Anatonj. Anz., 189(1.
»» Bonnet: His's Archiv, 1889.
■I" His : Abhandl. d. siich. (Jesellsch. d. Wiss., Bd. xxiv.
■'^ See also Mall ; -lourn. of Morph., vol. v.
^' His : Anat. nu-nsch. Eniljryonen, PI. vi.
■" Minot : Human f;iiil)ryi>logy. New York, Fig. 169.
'^'^ His : Anat. mensch. Euihryonen, i., p. l~(i.
'• His: Anat. mensch. Emhryonen, i., p. 126.
•"His: His's Archiv, 1881, PI. xii.. Fig. 9. Also Anat. mensch. Emhryonen, PI. ix.. Figs. Hi-13, 11.
" Bonnet : His's Archiv, 1889.
■" Uadiat : Jour, de I'Anat. et de la Physiol., 18*^ PI. v.. Figs. 1, 3.
^"The exceptions have been published by Waldeyer : Studien des physiol. Inst, zu Breslau, 180,5 ; Janosfk : Arch. f. mik. Anat., Bd. :Hi : His; Anat. mensch. Emhryonen, PI. viii.. Figs. A 1-4 ; Mall: Journ. of Morph., vol. V.
" His : Anat. mensch. Embrv(men, PI. vi.. Fig. 3, No. 10.
^'Kollmann : His's Archiv, 1891, PI. ill.. Figs. 3, 3, 4. V. umbil.
"•^ Mall : Journ. of Morph., vol. v.
^^ Mall : Journ. of Morph., vol. v.
" Budge : His's Archiv, 18«0 and 1887.
^^ Drasch : Anatom. Anz., Bd. 9.
'^« Cadiat : Jour, de I'Anat. et de la Physiol., 1883, PI. v., Figs. 1 and 3.
^' Duval : Atlas d'Embryologie, PI. xxli., Fig. 354.
»* Von Baer : Entwlcklungsgeschichte, 1837. •
«» Cadiat : Journ. de I'Anat. et de la Physiol., 1878.
" His : Anat. mensch. Emhryonen, Th. i., 1880. " Uskow : Arch. f. mik. Anat., 1883.
«= Ravn : His's Archiv, 1889.
" Hochstetter : Morph. Jahr., Bd. 20, p. 5a3.
^ Mall : Journ. of Morph.. vol. v., p. 472. «= Kavn : His's Archiv, 1889, PI. x.. Fig. 16.
"* Minot : Human Embryology, p. 483. " Mall : Journ. of Morph., vol. v.
- Franklin Mall Links: Franklin Mall | 1891 26 Day Human Embryo | 1905 Blood-Vessels of the Brain | 1906 Human Ossification | 1910 Manual of Human Embryology 1 | 1912 Manual of Human Embryology 2 | 1911 Mall Human Embryo Collection | 1912 Heart Development | 1915 Tubal Pregnancy | 1916 Human Magma in Normal and Pathological Development | 1917 Frequency Human Abnormalities | 1917 Human Embryo Cyclopia | 1918 Embryo Age | 1918 Appreciation | 1934 Franklin Mall biography PDF | Mall photograph | Mall painting | Mall painting | Carnegie Stages | Carnegie Embryos | Carnegie Collection | Category:Franklin Mall
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