The Works of Francis Balfour 2-14

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Foster M. and Sedgwick A. The Works of Francis Balfour Vol. II. A Treatise on Comparative Embryology 1. (1885) MacMillan and Co., London.

The Ovum and Spermatozoon | The Maturation and Impregnation of the Ovum | The Segmentation of the Ovum | Dicyemae and Orthonectidae Dicyema | Porifera | Coelenterata | Platyhelminthes | Rotifera | Mollusca | Polyzoa | Brachiopoda | Chilopoda | Discophora | Gephyrea | Chaetognatha | Nemathelminthes | Tracheata | Crustacea | Pcecilopoda | Echinodermata | Enteropneusta | Bibliography
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This historic 1885 book edited by Foster and Sedgwick is the second of Francis Balfour's collected works published in four editions. Francis (Frank) Maitland Balfour, known as F. M. Balfour, (November 10, 1851 - July 19, 1882) was a British biologist who co-authored embryology textbooks.

The Works of Francis Balfour Foster M. and Sedgwick A. The Works of Francis Balfour Vol. I. Separate Memoirs (1885) MacMillan and Co., London.

Foster M. and Sedgwick A. The Works of Francis Balfour Vol. II. A Treatise on Comparative Embryology 1. (1885) MacMillan and Co., London.

Foster M. and Sedgwick A. The Works of Francis Balfour Vol. III. A Treatise on Comparative Embryology 2 (1885) MacMillan and Co., London.

Foster M. and Sedgwick A. The Works of Francis Balfour Vol. IV. Plates (1885) MacMillan and Co., London.

Modern Notes:

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Pages where the terms "Historic" (textbooks, papers, people, recommendations) appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms, interpretations and recommendations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

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Vol II. A Treatise on Comparative Embryology (1885)

Gephyrea is a now-dismantled taxon for a group of non-annulated worms, considered intermediate between annelids and holothurians, containing the three modern phyla Echiura, Sipuncula, and Priapulida.

Chapter XIV. Gephyrea

IT is convenient for the purposes of embryology to divide the Gephyrea into two groups, viz. (i) Gephyrea nuda or true Gephyrea; and (2) Gephyrea tubicola formed by the genus Phoronis.

GEPHYREA NUDA. Segmentation and formation of the layers.

An embolic or epibolic gastrula is characteristic of the Gephyrea, and the blastopore appears, in some cases at any rate (Phascolosoma, Thalassema), to become the mouth.

Bonellia. In Bonellia (Spengel, No. 370) the segmentation is unequal but complete, and, as in many Molluscs etc., the ovum exhibits before its commencement a distinction into a protoplasmic and a yoke pole. The ovum first divides into four equal segments, each of them formed of the same constituents as the original ovum. At the animal pole four small cells, entirely formed of protoplasm, are next formed by an equatorial furrow. They soon place themselves in the intervals between the large spheres. Four small cells are again budded off from the large spheres and the eight small cells then divide. By a further continuation of the division of the existing small cells, and the formation of fresh ones from the large spheres, a layer of small

1 The following scheme shews the classification of the Gephyrea adopted in the present chapter :

i. Gephyrea nuda. { ii. Gephyrea tubicola (Phoronis).




cells is eventually formed, which completely envelops the four large spheres except for a small blastopore at the vegetative pole of the ovum (fig. 160 A). The large spheres continue to give rise to smaller cells which however no longer take a superficial position but lie within the layer of small cells, and give rise to the hypoblast (fig. r6o B). The small cells become the epiblast, and at the blastopore they curl inwards (fig. 160 B) and give


A. Stage when the four hypoblast cells are nearly enclosed.

B. Stage after the formation of the mesoblast has commenced by an infolding of the lips of the blastopore.

ep. epiblast ; me. mesoblast ; bl. blastopore.

rise to a layer of cells, which appears to extend as an unbroken sheet between the epiblast and hypoblast, and to form the mesoblast. The blastopore now closes up, but its position in relation to the parts of the embryo has not been made out.

In Phascolosoma (Selenka, No. 369) the ovum, enclosed in a porous zona radiata, divides into two unequal spheres, of which the smaller next divides into two and then into four. An invagination takes place which is intermediate between the embolic and the epibolic types. The small cells, the number of which is increased by additions from the large sphere, divide, and grow round the large sphere. The latter in the meantime also divides, and the cells produced from it form on the one hand a small sack which opens by the blastopore, and on the other they fill up the segmentation cavity, and become the mesoblast and blood corpuscles. Tin- Mastoporc becomes the permanent mouth.



Larval forms and development of organs.

Amongst the Gephyrea armata the larva has as a rule (Thalassema, Echiurus) the characters of a trochosphere, and closely approaches the typical form characteristic of the larva of Polygordius, often known as Loven's larva. In Bonellia this larval form is less perfectly preserved.

Echiurus. In Echiurus (Salensky, No. 368) the youngest known larva has all the typical trochosphere characters (fig. 161). It is covered with cilia and divided into a prae-oral lobe and post-oral region of nearly equal dimensions. There is a double ciliated ring which separates the two sections of the body as in the larva of Polygordius : the mouth (m) opens between its two elements. The alimentary canal is divided into a stomodaeum with a ventral opening, a large stomach, and a short intestine opening by a terminal anus (an). Connecting the oesophagus with the apex of the prae-oral lobe is the usual contractile band, and at the insertion of this band -is a thickening of the epiblast which probably represents the rudiment of the supra-oesophageal ganglion. A ventral nerve cord is stated by Salensky to be present, but his observations on this point are not quite satisfactory.

The metamorphosis is accompanied by the loss of swimming power, and consists in the enlargement of the post-oral portion of the trunk, and in the simultaneous reduction of the prae-oral lobe, which remains however permanently as the cylindrical proboscis. A groove which terminates posteriorly at the mouth is very early formed on its ventral side. The ciliated rings gradually disappear during the metamorphosis.

FIG. 161. LARVA OF ECHIURUS. (After Salensky.)

_ m. mouth ; an. anus ; sg. supra-ceso

Of the further external phageal ganglion (?).



changes the most important are (i) the early appearance round the anal end of the body of a ring of bristles ; and (2) the appearance of a pair of ventral setae in the anterior part of the body. The anterior ring of bristles characteristic of the adult Echiurus does not appear till a late period.

Of the internal changes the earliest is the formation of the anal respiratory sacks. With the growth of the posterior part of the trunk the intestine elongates, and becomes coiled.

Bonellia. The embryo of Bonellia, while still within the egg, retains a spherical form and acquires an equatorial band of cilia, behind which a second narrower band is soon established, while in front of the first one a pair of eye-spots becomes


A. Larva with two ciliated bands and two eye-spots.

B. Ripe larva from the dorsal surface.

C. Young female Bonellia from the side.

a/, alimentary tract ; m. mouth ; sc. provisional excretory tube ; s. ventral hook ; an.-', anal vesicle.

formed (fig. 162 A). The embryo on becoming hatched rapidly elongates, while at the same time it becomes dorso-vcntrally flattened and acquires a complete coating of cilia (fig. 162 B). According to Spengel it resembles at this time in its form and habits a rhabdoccelous Turbcllarian. The anterior part is however somewhat swollen and presents an indication of a pre-oral lobe.


During the above changes important advances are made in the formation of the organs from the embryonic layers.

The epiblast acquires a superficial cuticula, which is perhaps directly derived from the vitelline membrane. The nervous system is also formed, probably from the epiblast. The band-like supra-cesophageal ganglion is the first part of the nervous system formed, and appears to be undoubtedly derived from the epiblast. The ventral cord arises somewhat later, but the first stages in its development have not been satisfactorily traced. It is continuous with the supra-cesophageal band which completely girths the oesophagus without exhibiting any special dorsal enlargement. After the ventral cord has become completely separated from the epiblast a central fibrous mass becomes differentiated in it, while the lateral parts are composed of ganglion cells. In the arrangement of its cells it presents indications of being composed of two lateral halves. It is, however, without ganglionic swellings.

The mesoblast, though at first very thin, soon exhibits a differentiation into a splanchnic and somatic layer though the two do not become distinctly separated by a body cavity. The somatic layer rapidly becomes thicker, and enlarges laterally to form two bands united dorsally and ventrally by narrow, thinner bands. The outermost parts of each of these bands become differentiated into an external circular and an internal longitudinal layer of muscles. In the pras-oral lobe the mesoblast assumes a somewhat vacuolated character.

The hypoblast cells form a complete layer round the four yolk cells from which they arise (fig. 162 B, al\ but at first no alimentary lumen is developed. The oesophagus appears during this period as an, at first solid, but subsequently hollow, outgrowth of the hypoblast towards the epiblast.

The metamorphosis of the larva into the adult female Bonellia commences with the conversion of many of the indifferent mesoblast cells into blood corpuscles, and the introduction into the body cavity of a large amount of fluid, which separates the splanchnic and somatic layers of mesoblast. The fluid is believed by Spengel to be sea-water, introduced by two anal pouches, the development of which is described below.

The body cavity is lined by a peritoneum, and very soon distinct vessels, formed by folds of the peritoneum, become established. Of these there are three trunks, two lateral and a median in the prae-oral lobe (proboscis), and in the body a ventral trunk above the nerve cord, and an intestinal trunk opening anteriorly into the ventral one. The vessels appear to communicate with the body cavity.

In the course of the above changes the two ciliated bands


disappear, the hinder one first. The cilia covering the general surface become atrophied, with the exception of those on the ventral side of the prae-oral lobe. The latter structure becomes more prominent ; the stellate mesoblast cells, which fill up its interior, become contractile, and it gives rise to the proboscis (fig. 162 C).

At the point where the cesophageal protuberance joined the epiblast at a previous stage the mouth becomes established (fig. 162 C, ;//), and though it is formed subsequently to the atrophy of the anterior ciliated band, yet there is evidence that it is potentially situated behind this band. The lumen of the alimentary canal becomes established by the absorption of the remains of the four central cells. The anus is formed on the ventral side of the posterior end of the body, and close to it the pouches already noticed grow out from the hindermost part of the alimentary tract (fig. 162 C, an.v\ They are at first simple blind pouches, but subsequently open into the body cavity 1 . They become the anal pouches of the adult. There is present when the mouth is first formed a peculiar process of the alimentary tract projecting into the prae-oral lobe, which appears to atrophy shortly afterwards.

After the formation of the mouth, there are formed on the ventral side of and slightly behind it (i) anteriorly a pair of tubes, which appear to be provisional excretory organs and soon disappear (fig. 162 C, sc}\ and (2) behind them a pair of bristles (s) which remain in the adult. The formation of the permanent excretory (?) organ (oviduct and uterus) has not been followed out. The ovary appears very early as a differentiation of the epithelium lining the ventral vessel.

The larvae, which become the minute parasitic males, undergo a very different and far less complete metamorphosis than those which become females. They attach themselves to the proboscis of an adult female, and lose their ciliated bands. Germinal cells make their appearance in the mesoblast, which form spherical masses, and, like the germinal balls in the female ovary, consist of a central cell, and an epithelium around it. The central cell becomes very large, while the peripheral cells give rise to the spermatozoa. A body cavity becomes developed in the larvae, into which the spermatic balls are dehisced. Neither mouth nor anus is formed. The further changes have not been followed out.

1 The fact that these pouches are outgrowths of the alimentary tract appears to preclude the possibility of their being homologous with excretory tubes of the Plalyelminthes and Rotifera.


The larval males make their way into the oesophagus of the female, where they no doubt live for some time, and probably become mature, though the seminal pouch of the adult is not found in many of the males living in the oesophagus. When mature the males leave the oesophagus, and pass into the uterus.

Phascolosoma. Cilia appear in Phascolosoma (Selenka, No. 369) while the ovum is still segmenting. After segmentation they form a definite band immediately behind the mouth, which divides the Jarva into two hemispheres a prae-oral and a postoral. A prae-oral band of cilia is soon formed close to the postoral band, and at the apex of the prae-oral lobe a tuft of cilia also appears.

The larva has now the characters of a trochosphere, but differs from the typical trochosphere in the post-oral part of the ciliated equatorial ring being more important than the prae-oral, and in the absence of an anus.

The metamorphosis commences very early. The trunk rapidly elongates, and the prae-oral lobe becomes relatively less and less conspicuous. The zona radiata becomes the larval cuticle.

Three pairs of bristles are formed on the trunk, of which the posterior pair appears first, then the anterior, and finally the middle pair : an order of succession which clearly proves they can have no connection with a true segmentation.

The tentacles become developed between the two parts of the ciliated ring, and finally the prse-oral lobe, unlike what takes place in the Gephyrea armata, nearly completely vanishes.

The anus appears fairly late on the dorsal surface, and the ventral nerve cord is established as an unganglionated thickening of the ventral epiblast.


The larva of Phoronis was known as Actinotrocha long before its connection with Phoronis was established by Kowalevsky (No. 372). There is a complete segmentation leading to the formation of a blastosphere, which is followed by an invagination, the opening of which is said by Kowalevsky to remain as


the mouth 1 . It is at first terminal, but on the development of a large prse-oral lobe it assumes a ventral position. The anus is formed at a later period at the posterior end of the body.


ACTINOTROCHA. (After Metschnikoff.)

A. Young larva.

H. Larva after the formation of post-oral ring of tentacles.

C. Larva with commencing invagination to form the body of Phoronis.

D. Invagination partially everted.

E. Invagination completely everted.

m. mouth ; an. anus; iv. invagination to form the body of Phoronis.

The youngest free larva observed by Metschnikoff (No. 373) was less developed than the oldest larva found by Kowalevsky.

1 Kowalevsky states that whnt I have called the mouth is the anus, but his subsequent descriptions shew that he has transposed the mouth and anus in the embryo, and that the opening, which he asserts to be the anus, is in reality the mouth.


It probably belongs to a different species. The body is uniformly ciliated (fig. 163 A). There is a large contractile prse-oral lobe, and the body ends behind in two processes. The mouth (m) is ventral, and the anus (an) dorsal, and not terminal as in Kowalevsky's larva.

The alimentary tract is divided into stomodseum, stomach and intestine. The two processes at the hind end of the body are the rudiments of the first-formed pair of the arms which are so characteristic of the fully developed Actinotrocha. A second pair of arms next become established on the dorsal side of the previously existing pair, and the region where the anus is placed grows out as a special process. New pairs of arms continue to be formed in succession dorsalwards and forwards, and soon constitute a complete oblique post-oral ring (fig. 163 B). They are covered by long cilia. Round the anal process a very conspicuous ciliated ring also becomes established.

At the period when five pairs of arms are present a delicate membrane becomes visible on the ventral side of the intestine which joins the somatic mesoblast anteriorly. This membrane is the rudiment of the future ventral vessel. The somatic mesoblast is present even before this period as a delicate layer of circular muscular fibres.

When six pairs of arms have become formed an involution (fig. 163 C, iv) appears on the ventral side, immediately behind the ring of arms. This involution consists both of the epiblast and somatic mesoblast. It grows inwards towards the intestine, and, increasing greatly in length, becomes at the same time much folded.

When it has reached its full development the critical period of the metamorphosis of Actinotrocha into Phoronis is reached, and is completed in about a quarter of an hour. The ventral involution becomes evoluted (fig. 163 D), just as one might turn out the finger of a glove which had been pulled inwards. When the involution has been to a certain extent everted, the alimentary canal passes into it, and at the same time the body of the larva becomes violently contracted. By the time the evagination is completed it forms (fig. 162 E) a long conical body, containing the greater part of the alimentary tract, and constituting the body of the young- Phoronis. The original anal process remains on the dorsal side as a small papilla (fig. 162 E, an).

364 \< T1NOTROCHA.

While these changes have been taking place the prae-oral lobe has become much contracted, and partly withdrawn into the stomodajum. At the same time the arms have become bent forward, so as to form a ring round the mouth. Their bases become much thickened. The metamorphosis is completed by the entire withdrawal of the prae-oral lobe within the oesophagus, and by the casting off of the ends of the arms, their bases remaining as the circumoral ring of tentacles, which form however a lophophore rather than a complete ring. The perianal ring of cilia is also thrown off, and the anal process withdrawn into the body of the young Phoronis. There are now three longitudinal vascular trunks, united anteriorly by a circular vessel which is prolonged into the tentacles.

General Considerations.

The development of Phoronis is so different from that of the other Gephyrea that further investigations are required to shew whether Phoronis is a true Gephyrean. Apart from its peculiar metamorphosis Actinotrocha is a very interesting larval form, in that it is without a prae-oral ciliated ring, and that the tentacles of the adult are derived from a true post-oral ring, prolonged into arm-like processes.

The other Gephyrea present in their development an obvious similarity to the normal Chaetopoda, but their development stops short of that of the Chaetopoda, in that they are clearly without any indications of a true segmentation. In the face of what is known of their development it is hardly credible that they can represent a degenerate Chaetopod phylum in which segmentation has become lost. Further than this the Gephyrea armata seem in one respect to be a very primitive type in that they retain through life a well-developed pra-oral lobe, which constitutes their proboscis. In almost all other forms, except Balanoglossus, the larval prae-oral lobe becomes reduced to a relatively insignificant anterior part of the head.

BIBLIOGRAPHY. Gephyrea nuda.

(366) A. Kowalevsky. Sitz. d. zool. Abth. d. III. Vcrsam. russ. Naturj. (Thalasscma). Zeit.f. wiss. Zool. Vol. xxn. 1872, p. 284.


(367) A. Krohn. "Ueb. d. Larve d. Sipunculus nudus nebst Bemerkungen," etc. Miiller's Archiv, 1857.

(368) M. Salensky. "Ueber die Metamorphose d. Echiurus." Morphologisches Jahrbuch, Bd. 11.

(369) E. Selenka. "Eifurchung u. Larvenbildung von Phascolosoma elongatum." Zeit.f. wiss. ZooL 1875, Bd. xxv. p. i.

(370) J. W. Spengel. "Beitrage z. Kenntniss d. Gephyreen (Bonellia)." Mittheil. a. d. zool. Station z. Neapel, Vol. I. 1879.

Gephyrea tubicola (Actinotrocha).

(371) A. Krohn. " Ueb. Pilidium u. Actinotrocha." Miiller's Archiv, 1858.

(372) A. Kowalevsky. "On anatomy and development of Phoronis," Petersbourg, 1867. 2 PI. Russian. Vide Leuckart's Bericht, 1866-7.

(373) E. Metschnikoff. " Ueber d. Metamorphose einiger Seethiere (Actinotrocha)." Zeit.f. wiss. Zool. Bd. xxi. 1871.

(374) J. Miiller. " Bericht lib. ein. Thierformen d. Nordsee." Miiller's Archiv, 1846.

(375) An. Schneider. "Ueb. d. Metamorphose d. Actinotrocha branchiata." Miiller's Arch. 1862.