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

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This historic 1885 book edited by Foster and Sedgwick is the third 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. 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. III. A Treatise on Comparative Embryology 2 (1885)

CHAPTER V. CYCLOSTOMATA

PETROMYZON is the only type of this degenerated but primitive group of Fishes the development of which has been as yet studied 2 .

The development does not however throw any light on the relationships of the group. The similarity of the mouth and other parts of Petromyzon to those of the Tadpole probably indicates that there existed a common ancestral form for the Cyclostomata and Amphibia. Embryology does not however add anything to the anatomical evidence on this subject. The fact of the segmentation being complete was at one time supposed to indicate an affinity between the two groups ; but the discovery that the segmentation is also complete in the Ganoids deprives this feature in the development of any special weight. In the formation of the layers and in most other developmental characters there is nothing to imply a special relationship with the Amphibia, and in the mode of formation of the nervous system Petromyzon exhibits a peculiar modification, otherwise only known to occur in Teleostei and Lepidosteus.

Dohrn 3 was the first to bring into prominence the degenerate character of the Cyclostomata. I cannot however assent to his view that they are

1 The following classification of the Cyclostomata is employed in the present chapter :

I. Hyperoartia ex. Petromyzon. II. Hyperotreta ex. Myxine, Bdellostoma.

2 The present chapter is in the main founded upon observations which I was able to make in the spring of 1880 upon the development of Petromyzon Planeri. Mr Scott very kindly looked over my proof-sheets and made a number of valuable suggestions, and also sent me an early copy of his preliminary note (No. 87), which I have been able to make use of in correcting my proof-sheets.

3 Der Ursprung d. Wirbelthiere, etc. Leipzig, 1875.

62

8 4

FORMATION OF THE LAYERS.

descended from a relatively highly-organized type of Fish. It appears to me almost certain that they belong to a group of fishes in which a true skeleton of branchial bars had not become developed, the branchial skeleton they possess being simply an extra-branchial system; while I see no reason to suppose that a true branchial skeleton has disappeared. If the primitive Cyclostomata had not true branchial bars, they could not have had jaws, because jaws are essentially developed from the mandibular branchial bar. These considerations, which are supported by numerous other features of their anatomy, such as the character of the axial skeleton, the straightness of the intestinal tube, the presence of a subintestinal vein etc., all tend to prove that these fishes are remnants of a primitive and praegnathostomatous group. The few surviving members of the group have probably owed their preservation to their parasitic or semiparasitic habits, while the group as a whole probably disappeared on the appearance of gnathostomatous Vertebrata.

The ripe ovum of Petromyzon Planeri is a slightly oval body of about i mm. in diameter. It is mainly formed of an

opaque nearly white yolk, TTI& ,

invested by a membrane composed of an inner perforated layer, and an outer structureless layer. There appears to be a pore perforating the inner layer at the formative pole, which may be called a micropyle (KupfTer and Benecke, No. 79). Enclosing the eggmembranes there is present a mucous envelope, which causes the egg, when laid, to adhere to stones or other objects.

Impregnation is effected by the male attaching itself by its suctorial mouth to the female. The attached couple then shake together ; and, as they do so, they respectively emit from their abdominal pores ova and spermatozoa which pass into a hole previously made 1 .

U

FIG. 37. LONGITUDINAL VERTICAL SECTION THROUGH AN EMBRYO OF PETROMYZON

PLANERI OF 136 HOURS.

me. mesoblast ; yk. yolk-cells ; al. alimentary tract ; bl. blastopore ; s.c. segmentation cavity.

1 Artificial impregnation may be effected without difficulty by squeezing out into the same vessel the ova and spermatozoa of a ripe female and male. The fertilized eggs are easily reared. Petromyzon Planeri breeds during the second half of April.

CYCLOSTOMATA.

The segmentation is total and unequal, and closely resembles that in the Frog's egg (Vol. II. p. 96). The upper pole is very slightly whiter than the lower. A segmentation cavity is formed very early, and is placed between the small cells of the upper pole and the large cells of the lower pole. It is proportionately larger than in the Frog ; and the roof eventually thins out so as to be formed of a single row of small cells. At the sides of the segmentation cavity there are always several rows of small cells,

FIG. 38. TRANSVERSE SECTION THROUGH A PETROMYZON EMBRYO 160 HOURS

AFTER IMPREGNATION. ep. epiblast ; al. mesenteron ; yk. yolk-cells ; ms. mesoblast.

which gradually merge into the larger cells of the lower pole of the egg. The segmentation is completed in about fifty hours.

The segmentation is followed by an asymmetrical invagination (fig. 37) which leads to a mode of formation of the hypoblast fundamentally similar to that in the Frog. The process has been in the main correctly described by M. Schultze (No. 81).

On the border between the -large and small cells of the embryo, at a point slightly below the segmentation cavity, a small circular pit appears ; the roof of which is formed by an infolding of the small cells, while the floor is formed of the large cells. This pit is the commencing mesenteron. It soon grows deeper (fig. 37, al} and extends as a well-defined tube (shewn in transverse section in fig. 38, al} in the direction of the segmentation cavity. In the course of the formation of the mesenteron the segmentation cavity gradually becomes smaller, and is

86 FORMATION OF THE LAYERS.

finally (about the 2ooth hour) obliterated. The roof of the mesenteron is formed by the continued invagination of small cells, and its floor is composed of large yolk-cells. The wide external opening is arched over dorsally by a somewhat prominent lip the homologue of the embryonic rim. The opening persists till nearly the time of hatching ; but eventually becomes closed, and is not converted into the permanent anus. On the formation of the mesenteron the hypoblast is composed of two groups of cells, (i) the yolk-cells, and (2) the cells forming the roof of the mesenteron.

While the above changes are taking place, the small cells, or as they may now be called the epiblast cells, gradually spread over the large yolk-cells, as in normal types of epibolic invagination. The growth over the yolk-cells is not symmetrical, but is most rapid in the meridian opposite the opening of the alimentary cavity, so that the latter is left in a bay (cf. Elasmobranchii, p. 63). The epibolic invagination takes place as in Molluscs and many other forms, not simply by the division of pre-existing epiblast cells, but by the formation of fresh epiblast cells from the yolk-cells (fig. 37) ; and till after the complete enclosure of the yolk-cells there is never present a sharp line of demarcation between the two groups of cells. By the time that the segmentation cavity is obliterated the whole yolk is enclosed by the epiblast. The yolk-cells adjoining the opening of the mesenteron are the latest to be covered in, and on their enclosure this opening constitutes the whole of the blastopore. The epiblast is composed of a single row of columnar cells.

Mesoblast and notochord. During the above changes the mesoblast becomes established. It arises, as in Elasmobranchs, in the form of two plates derived from the primitive hypoblast. During the invagination to form the mesenteron some of the hypoblast cells on each side of the invaginated layer become smaller, and marked off as two imperfect plates (fig. 38, ms). It is difficult to say whether these plates are entirely derived from invaginated cells, or are in part directly formed from the pre-existing yolk-cells, but I am inclined to adopt the latter view ; the ventral extension of the mesoblast plates undoubtedly takes place at the expense of the yolk-cells. The mesoblast plates soon become more definite, and form (fig. 39, ms) well

CYCLOSTOMATA.

defined structures, triangular in section, on the two sides of the middle line.

At the time the mesoblast is first formed the hypoblast cells, which roof the mesenteron, are often imperfectly two layers thick (fig. 38). They soon however become constituted of a single layer only. When the mesoblast is fairly established, the lateral parts of the hypoblast grow inwards underneath the axial part, so that the latter (fig. 39, c/i) first becomes isolated as an axial cord, and is next inclosed between the medullary cord (nc) (which has by this time been formed) and a continuous sheet of hypoblast below (fig. 40). Here its cells divide and it becomes the notochord. The notochord is thus bodily formed out of the axial portion of the primitive hypoblast. Its mode of origin may be compared with that in Amphioxus, in which an axial fold of the archenteric wall is constricted off as the notochord. The above features in the development of the notochord were first established by Calberla 1 (No. 78).

General history of the development. Up to about the time when the enclosure of the hypoblast by the epiblast is completed, no external traces are visible of any of the organs of the embryo ; but about this time, i.e. about 180 hours after impregnation, the rudiment of

FIG. 39. TRANSVERSE SECTION THROUGH AN EMBRYO OF PETROMYZON PLANERI OF

208 HOURS.

The figure illustrates the formation of the neural cord and of the notochord.

ms. mesoblast ; nc. neural cord ; ch. notochord ; yk. yolk-cells ; al. alimentary canal.

m C.

FIG. 40. TRANSVERSE SECTION THROUGH PART OF AN EMBRYO OF PETROMYZON PLANERI OF 256 HOURS.

m.c. medullary cord ; ch. notochord ; al. alimentary canal ; ms. mesoblastic plate.

1 In Calberla's figure, shewing the development of the notochord, the limits of mesoblast and hypoblast are wrongly indicated.

88 GENERAL DEVELOPMENT.

the medullary plate becomes established, as a linear streak extending forwards from the blastopore over fully one half the circumference of the embryo. The medullary plate first contains a shallow median groove, but it is converted into the medullary cord, not in the usual vertebrate fashion, but, as first shewn by Calberla, in a manner much more closely resembling the formation of the medullary cord in Teleostei. Along the line of the median groove the epiblast becomes thickened and forms a kind of keel projecting inwards towards the hypoblast (fig. 39, nc]. This keel is the rudiment of the medullary cord. It soon becomes more prominent, the median groove in it disappears, and it becomes separated from the epiblast as a solid cord (fig. 40, me}.

By this time the whole embryo has become more elongated, and on the dorsal surface is placed a ridge formed by the projection of the medullary cord. At the lip of the blastopore the medullary cord is continuous with the hypoblast, thus forming the rudiment of a neurenteric canal.

Calberla gives a similar account of the formation of the neural canal to that which he gives for the Teleostei (vide p. 72.)

He states that the epiblast becomes divided into two layers, of which the outer is involuted into the neural cord, a median slit in the involution representing the neural groove. The eventual neural canal is stated to be lined by the involuted cells. Scott (No. 87) fully confirms Calberla on this point, and, although my own sections do not clearly shew an involution of the outer layer of epiblast cells, the testimony of these two observers must no doubt be accepted on this point.

Shortly after the complete establishment of the neural cord the elongation of the embryo proceeds with great rapidity. The processes in this growth are shewn in fig. 41, A, B, and C. The cephalic portion (A, c] first becomes distinct, forming an anterior protuberance free from yolk. About the time it is formed the mesoblastic plates begin to be divided into somites, but the embryo is so opaque that this process can only be studied in sections. Shortly afterwards an axial lumen appears in the centre of the neural cord, in the same manner as in Teleostei.

The general elongation of the embryo continues rapidly, and, as shewn in my figures, the anterior end is applied to the

CYCLOSTOMATA.

8 9

ventral surface of the yolk (B). With the growth of the embryo the yolk becomes entirely confined to the posterior part. This part is accordingly greatly dilated, and might easily be mistaken for the head. The position of the yolk gives to the embryo a very peculiar appearance. The apparent difference between it and the embryos of other Fishes in the position of the yolk is due in the main to the fact that the post-anal portion of the tail is late in developing, and always small. As the embryo grows longer it becomes spirally coiled within the eggshell. Before hatching the mesoblastic somites become distinctly marked (C).

The hatching takes place at between 13 21 days after impregnation ; the period varying according to the temperature.

During the above changes in the external form of the

FlG. 41. FOUR STAGES IN THE DEVELOPMENT OF PETROMYZON.

(After Owsjannikoff.)

c. cephalic extremity ; bl. blastopore ; op. optic vesicle ; au.v. auditory vesicle ; br.c. branchial clefts.

embryo, the development of the various organs makes great progress. This is especially the case in the head. The brain becomes distinct from the spinal cord, and the auditory sacks and the optic vesicles of the eye become formed. The branchial region of the mesenteron becomes established, and causes a

GENERAL DKVKLOl'MKNT.

dilatation of the anterior part of the body, and the branchial pouches grow out from the throat. The anus becomes formed, and a neurenteric canal is also established (Scott). The nature of these and other changes will best be understood by a description of the structure of the just-hatched larva. The general appearance of the larva immediately after hatching is shewn in fig. 41, D. The body is somewhat -curved ; the posterior extremity being much dilated with yolk, while the anterior is very thin. All the cells still contain yolk particles, which render the embryo very opaque. The larva only exhibits slow movements, and is not capable of swimming about.

The structure of the head is shewn in figs. 42 and 43. Fig. 42 is a section through a very young larva, while fig. 43 is taken from a larva three days after hatching, and shews the parts with considerably greater detail.

On the ventral side of the head is placed the oral opening (fig. 43, m) leading into a large stomodaeum which is still without a communication with the mesenteron. Ventrally the stomodaeum is prolonged for a considerable distance under the anterior part of the mesenteron. Immediately behind the sto

FIG. 42. DIAGRAMMATIC VERTICAL SECTION OF A JUST-HATCHED LARVA OF

PETROMYZON. (From Gegenbaur ; after Calberla.)

o. mouth ; o ' . olfactory pit ; v. septum between stomodaeum and mesenteron ; h. thyroid involution ; n. spinal cord ; ch. notochord ; c. heart ; a. auditory vesicle.

modaeum is placed the branchial region of the mesenteron. Laterally it is produced on each side into seven or perhaps eight branchial pouches (fig. 43, br.c}, which extend outwards nearly to the skin but are not yet open. Between the successive pouches are placed mesoblastic segments, of the same nature and structure as the walls of the head cavities in the embryos of Elasmobranchs, and like them enclosing a central cavity. A

CYCLOSTOMATA. 91

similar structure is placed behind the last, and two similar structures in front of the first persistent pouch. This pouch is situated in the same vertical line as the auditory sack (au.v), and would appear therefore to be the hyo-branchial cleft ; and this identification is confirmed by the fact of two head cavities being present in front of it At the front end of the branchial region of the mesenteron is placed a thickened ridge of tissue,

pn

FIG. 43. DIAGRAMMATIC VERTICAL SECTION THROUGH THE HEAD OF A LARVA OF PETROMYZON.

The larva had been hatched three days, and was 4 '8 mm. in length. The optic and auditory vesicles are supposed to be seen through the tissues. The letter tv pointing to the base of the velum is where Scott believes the hyomandibular cleft to be situated.

c.h. cerebral hemisphere; th. optic thalamus; in, infundibulum; pn. pineal gland ; mb. mid-brain; cl>. cerebellum; md. medulla oblongata ; au.v. auditory vesicle; op. optic vesicle ; ol. olfactory pit ; m. mouth; br.c. branchial pouches; th. thyroid involution ; v.ao. ventral aorta ; ht. ventricle of heart ; ch. notochord.

which, on the opening of the passage between the stomodseum and the mesenteron, forms a partial septum between the two, and is known as the velum (fig. 43, tv).

According to Scott (No. 87) a hyomandibular pouch forming the eighth pouch is formed in front of the pouch already defined as the hyobranchial. It disappears early and does not acquire gill folds 1 . The tissue forming the

1 Scott informs me that he has been unable to find the hyomandibular pouch in larvae larger than 4-8 mm. My material of the stages when it should be present is somewhat scanty, but I have as yet, very likely owing to the imperfection of my material, been unable to find Scott's hyomandibular pouch either in my sections or surface-views. Huxley describes this pouch as present in the form of a cleft in later stages; I have failed to find his cleft also. The vessel interpreted below as the branchial artery of the mandibular arch was only imperfectly investigated by me, and I was not sure of my interpretations about it. Scott however informs me by letter that it is undoubtedly present.

9 2

GENERAL DEVELOPMENT.

line of insertion of the velum appears to me to represent the mandibular arch. The grounds for this view are the following :

(1) The structure in question has exactly the position usually occupied by the mandibular arch.

(2) There is present in late larvae (about 20 days after hatching) an arterial vessel, continued from the ventral prolongation of the bulbus arteriosus along the insertion of the velum towards the dorsal aorta, which has the relations of a true branchial artery.

On the ventral aspect of the branchial region is placed a sack (figs. 42, h, and 43, ///), which extends from the front end of the branchial region to the fourth cleft. At first it constitutes a groove opening into the throat above (fig. 44), but soon the opening becomes narrowed to a pore placed between the second and third of the permanent branchial pouches (fig. 43, tJi). In Ammoccetes 1 the simple tube becomes divided, and assumes a very complicated form, though still retaining its opening into the branchial region of the throat. In the adult it forms a glandular mass underneath the branchial region of the throat equivalent to the thyroid gland of higher Vertebrates.

On the ventral aspect of the head, and immediately in front of the mouth, is placed the olfactory pit (fig. 43, of}. It is from the first unpaired, and in just-hatched larvae simply forms a shallow groove of thickened epiblast at the base of the front of the brain. By the stage represented in fig. 43 the ventral part of the original groove is prolonged into a pit, extending backwards beneath the brain nearly up to the infundibulum.

On the side of the head, nearly on a level with the front end of the notochord, is placed the eye (fig. 43, op}. It is constituted (figs. 45 and 46) of a very shallow optic cup with a thick outer (retinal) layer, and a thin inner choroid layer. In contact with the retinal layer is placed the lens. The latter is formed as an invagination of the

FIG. 44. DIAGRAMMATIC TRANSVERSE SECTIONS THROUGH THE BRANCHIAL REGION

OF A YOUNG LARVA OK PETBOMYZON. (From Gegenbaur ; after Calberla.)

d. branchial region of throat.

1 Schneider (No. 85) states that in the full-grown Ammoccetes the opening is situated between the third and fourth pouches. This is certainly not true for the young larva.

CYCLOSTOMATA.

93

skin ; to which it is still attached in the just-hatched larva (fig. 45). The eye only differs at this stage from that of other Vertebrata in its extraordinarily small size, and the rudimentary character of its constituent parts.

The auditory sack is a large vesicle (fig. 43, au.v}, placed at the side of the brain opposite the first persistent branchial pouch.

The brain is formed of the usual vertebrate parts 1 , but is characterized by the very slight cranial flexure. The fore-brain consists (fig. 43) of a thalamencephalon (t/i) and an undivided cerebral rudiment (ch}. To the roof of the thalamencephalon is attached a flattened sack (pn} which is probably the pineal gland. The floor is prolonged into an infundibulum (in} which contains a prolongation of the third ventricle. The lateral walls of the cerebral rudiment are much thickened.

Behind the thalamencephalon follows the mid-brain (mb], the sides of which form the optic lobes, and behind this again the hind-brain (ind} ; the front border of the roof of which is thickened to form the cerebellum (cb}. The medulla passes without any marked line of demarcation into the spinal cord.

The histological differentiation of the brain has already proceeded to some extent ; and it has in the main the same character as the spinal cord. Before the larva has been hatched very long a lateral investment of white matter is present throughout. The notochord (ck] is continued forwards in the head to the hinder border of the infundibulum. It is slightly flexed anteriorly.

From the hinder border of the auditory region to the end of the branchial region the mesoblast is dorsally divided into

1 Max Schultze's statements as to the structure and histology of the brain are very inadequate in the present state of our knowledge.

FIG. 45. HORIZONTAL SECTION THROUGH THE HEAD OF A JUST-HATCHED LARVA OF PETROMYZON SHEWING THE DEVELOPMENT OF THE LENS OF THE EYE.

th.c. thalamencephalon ; op.v. optic vesicle ; /. lens of eye ; h.c. head cavity.

94

GENERAL DEVELOPMENT.

myotomes, which nearly, though number with the branchial pouches.

not quite, correspond in

FIG. 46. EYE OF A LARVA OF PETROMYZON NINE DAYS AFTER HATCHING.

/. lens; r. retina.

The section passes through one side of the lens.

The growth of the myotomes would seem, as might be anticipated from their independent innervation, not to be related to that of the branchial pouches, so that there is a want of correspondence between these parts, the extent of which varies at different periods of life. The relation between the two in an old larva is shewn in fig. 47.

The head of the larva of Petromyzon differs very strikingly in general appearance from that of the normal Vertebrata. This is at once shewn by a comparison of fig. 43 with fig. 29. The most important difference between the two is due to the absence of a pronounced cranial flexure in Petromyzon ; an absence which is in its turn probably caused by the small development of the fore-brain.

The stomodaeum of Petromyzon is surprisingly large, and its size and structure in this type militate against the view of some embryologists that the stomodaeum originated from the coalescence of a pair of branchial pouches.

In the region of the trunk there is present an uninterrupted dorsal fin continuous with a ventral fin round the end of the tail.

There is a well-developed body cavity, which is especially dilated in front, in the part which afterwards becomes the pericardium. In this region is placed the nearly straight heart, divided into an auricle and ventricle (figs. 42 and 43), the latter continued forwards into a bulbus arteriosus.

The myotomes are now very numerous (about 57, including those of the head, in a three days' larva). They are separated by septa, but do not fill up the whole space between the septa, and have a peculiar wavy outline. The notochord is provided with a distinct sheath, and below it is placed a subnotochordal rod.

The alimentary canal consists of a narrow anterior section free from yolk, and a posterior region, the walls of which arc

CYCLOSTOMATA.

95

largely swollen with yolk. The anterior section corresponds to the region of the oesophagus and stomach, but exhibits no distinction of parts. Immediately behind this point the alimentary canal dilates considerably, and on the ventral side is placed the opening of a single large sack, which forms the commencement of the liver. The walls of the hepatic sack are posteriorly united to the yolk-cells. At the region where the hepatic sack opens into the alimentary tract the latter dilates considerably.

The posterior part of the alimentary tract still constitutes a kind of yolk-sack, the ventral wall being enormously thick and formed of several layers of yolk-cells. The dorsal wall is very thin.

The excretory system is composed of two segmental ducts, each connected in front with a well-developed pronephros (headkidney), with about five ciliated funnels opening into the pericardial region of the body cavity. The segmental ducts in the larvae open behind into the cloacal section of the alimentary tract.

The development of the larva takes place with considerable rapidity. The yolk becomes absorbed and the larva becomes accordingly more transparent. It generally lies upon its side, and resembles in general appearance and habit a minute Am

tl

FIG. 47. HEAD OF A LARVA OF PETROMYZON six WEEKS OLD.

(Altered from Max Schultze.)

au.v. auditory vesicle ; op. optic vesicle ; ol. olfactory pit ; ul. upper lip ; //. lower lip ; or.p. papillae at side of mouth ; v. velum ; br.s. extra branchial skeleton ; i 7. branchial clefts.

phioxus. It is soon able to swim with vigour, but usually, unless disturbed, is during the day quite quiescent, and chooses by

96 GENERAL DEVELOPMENT.

preference the darkest situations. It soon straightens out, and, with the disappearance of the yolk, the tail becomes narrower than the head. A large caudal fin becomes developed.

When the larva is about twenty days old, it bears in most anatomical features a close resemblance to an Ammoccetes ; though the histological differences between my oldest larva (29 days) and even very young Ammoccetes are considerable.

The mouth undergoes important changes. The upper lip becomes much more prominent, forming of itself the anterior end of the body (fig. 47, /). The opening of the nasal pit is in this way relatively thrown back, and at the same time is caused to assume a dorsal position. This will be at once understood by a comparison of fig. 43 with fig. 47. On the inner side of the oral cavity a ring of papillae is formed (fig. 47, or.p). Dorsally these papilla; are continued forward as a linear streak on the under side of the upper lip. A communication between the oral cavity and the branchial sack is very soon established.

The gill pouches gradually become enlarged ; but it is some time before their small external openings are established. Their walls, which are entirely lined by hypoblast, become raised in folds, forming the branchial lamellae. The walls of the head cavities between them become resolved into the contractors and dilators of the branchial sacks. The extra-branchial basketwork becomes established very early (it is present in the larva of 6 millimetres, about 9 days after hatching) and is shewn in an older larva in fig. 47, br.s. It is not so complicated in these young larvae as in the Ammoccetes, but in Max Schultze's figure, which I have reproduced, the dorsal elements of the system are omitted. On the dorsal wall of the branchial region a ciliated ridge is formed, which may be homologous with the ridge on the dorsal wall of the branchial sack of Ascidians. It has been described by Schneider in Ammoccetes.

With reference to the remainder of the alimentary canal there is but little to notice. The primitive hepatic diverticulum rapidly sprouts out and forms a tubular gland. The opening into the duodenum changes from a ventral to a lateral or even dorsal position. The duct leads into a gallbladder imbedded in the substance of the liver. Ventrally the liver is united with the abdominal wall, but laterally passages are left by which the pericardial and body cavities continue to communicate.

The greater part of the yolk becomes employed in the formation of the intestinal wall. This part of the intestine in a nine days' larva (67 mm.) has the form of a cylindrical tube with very thick columnar cells entirely filled with yolk particles. The dorsal wall is no longer appreciably thinner than the ventral. In the later stages the cells of this part of the intestine become gradually less columnar as the yolk is absorbed.

The fate of the yolk-cells in the Lamprey is different from that in most other Vertebrata with an equally large amount of yolk. They no doubt

CYCLOSTOMATA. 97

supply nutriment for the growth of the embryo, and although in the anterior part of the intestine they become to some extent enclosed in the alimentary tract and break up, yet in the posterior part they become wholly transformed into the regular epithelium of the intestine.

On the ninth day a slight fold filled with mesoblastic tissue is visible on the dorsal wall of the intestine. This fold appears to travel towards the ventral side ; at any rate a similar but better-marked fold is visible in a ventro-lateral position at a slightly later period. This fold is the commencement of the fold which in the adult makes a half spiral, and is no doubt equivalent to the spiral valve of Elasmobranchs and Ganoids. It contains a prolongation of the cceliac artery, which constitutes at first the vitelline artery.

The nervous system does not undergo during the early larval period changes which require a description.

The op-Mii.^ of the olfactory sack becomes narrowed and ciliated (fig. 47, 0/). It is carried by the process already mentioned to the dorsal surface of the head. The lumen of the sack is well developed ; and lies in contact with the base of the fore part of the brain.

The vascular system presents no very remarkable features. The heart is two-chambered and straight. The ventricle is continued forwards as a bulbus arteriosus, which divides into two arteries at the thyroid body. From the bulbus and its continuations eight branches are given off to the gills ; and, as mentioned above, a vessel, probably of the same nature, is given off in the region of the velum. The blood from the branchial sacks is collected into the dorsal aorta. Some of it is transmitted to the head, but the greater part flows backwards under the notochord.

The venous system consists of the usual anterior and posterior cardinal veins which unite on each side into a ductus Cuvieri, and of a great subintestinal vessel of the same nature as that in embryo Elasmobranchs, which persists however in the adult. It breaks up into capillaries in the liver, and constitutes therefore the portal vein. From the liver the blood is brought by the hepatic vein into the sinus venosus. In addition to these vessels there is a remarkable unpaired sub-branchial vein, which brings back the blood directly to the heart from the ventral part of the branchial region.

Metamorphosis. The larva just described does not grow directly into the adult, but first becomes a larval form, known as Ammoccetes, which was supposed to be a distinct species till Aug. Miiller (No. 80) made the brilliant discovery of its nature.

The Ammoccetes does not differ to any marked extent from the larva just described. The histological elements become more differentiated, and a few organs reach a fuller development.

The branchial skeleton becomes more developed, and capsules for the olfactory sack and auditory sacks are established.

B. III. 7

9 8

METAMORPHOSIS.

The olfactory sack is nearly divided into two by a ventral septum. The eye (fig. 48) is much more fully developed, but lies a long way below the surface. The optic cup forms a deep pit, in the mouth of which is placed the lens. The retinal layers are well developed (cf. Langerhans), and the outer layer of the optic cup or layer of retinal pigment (rp} contains numerous pigment granules, especially on its dorsal side. At the edge of the optic cup the two layers fall into each other. They constitute the commencement of the pigment layer of the iris ; but at this stage they are not pigmented. The mesoblast of the iris is hardly differentiated. The lens (/) has the normal structure of the embryonic lens of Vertebrata. The inner wall is thick and doubly convex, while the outer wall, which will form the anterior epithelium, is very thin. There is a large space between the lens and the retina containing the vitreous humour (v.h\ There is no aqueous humour, and the tissues in front of the lens bear but little resemblance to those in higher Vertebrata. The cornea is represented by (i) the epidermis (<?/) ; (2) the dermis (d.c) ; (3) the sub-dermal connective tissue (s.d.c) which passes without any sharp line of demarcation into the dermis ; (4) a thick membrane continuous with the choroid which represents Descemet's membrane. The sub-dermal connective tissue is continued as an investment round the whole eye. There is no specially differ

s.d.c

cfm

entiated sclerotic, and a choroid is only imperfectly indicated 1 . The peculiar features of the eye of the young larva of the Ammoccetes are probably due to degeneration.

In the brain the two cerebral hemispheres lie one on each side of the anterior end of the thalamencephalon. There are welldefined olfactory lobes, and two distinct olfactory nerves are present.

The excretory system has undergone great changes. A series of segmental tubes, which first appear in a larva of about 9 mm.,

FIG. 48. EYE OF AN AMMOCCETES LYING BENEATH THE SKIN.

ep. epidermis ; d.c. dermal connective tissue continuous with the sub-dermal connective tissue (s.d.c), which is also shaded. There is no definite boundary to this tissue where it surrounds the eye.

m. muscles ; dm. membrane of Descemet; /. lens; v.h. vitreous humour ; r. retina; rp. retinal pigment.

1 Langerhans loc. cit. describes the eye of the Ammoccetes in some respects very differently from the above. Very probably his description applies to an older Ammoccetes. The most important points of difference appear to be (i) that the vitreous humour is all but obliterated ; (2) that the iris is much better developed.

CYCLOSTOMATA.

99

becomes established behind the pronephros, and in an Ammoccetes of 65 mm. the pronephros has begun to atrophy. The generative organs are formed in a larva of about 35 mm. Shortly before the metamorphosis the portion of the cloaca into which the segmental tubes open becomes separated off as a distinct urinogenital sinus, the walls of which become perforated by the two abdominal pores.

The Ammoccetes of Petromyzon Planeri lives in the mud in streams. Without undergoing any marked changes in structure it gradually grows larger, and after three or four years undergoes a metamorphosis. The full-grown larva may be as large or even larger than the adult. The metamorphosis takes place from August till January. The breeding season sets in during the second half of April ; and shortly after depositing its generative products the Lamprey dies. The changes which take place in the metamorphosis are of a most striking kind.

The dome-shaped mouth of the larva is replaced (fig. 47) by a more definitely suctorial mouth with horny cuticular teeth (fig. 49). The eyes appear on the surface ; and the dorsal fin becomes more prominent, and is divided into two parts.

Besides these obvious external changes very great modifications are effected in almost all the organs, which may be very briefly enumerated.

1. Very profound changes take place in the skeleton. An elaborate system of cartilages is developed in connection with the mouth ; the cranium itself undergoes important modifications; and neural arches become formed.

2. Considerable changes are effected in the gill pouches, and, according to Schneider, whose statements must however be received with some caution, the branchial sack becomes detached posteriorly from the oesophagus, the oesophagus then sends forwards a prolongation above the branchial sack which is at first solid. This prolongation forms the anterior part of the

72

FIG. 49. MOUTH OF PETROMYZON MARINUS WITH ITS HORNY TEETH. (From Gegenbaur; after Heckel and Kner.)

100 METAMORPHOSIS.

oesophagus of the adult, and joins the primitive oral cavity at the velum. The so-called bronchus of the adult is thus the whole branchial region of the Ammoccetes, and the anterior part of the oesophagus of the adult is an entirely new formation.

3. The posterior part of the alimentary tract of the Ammoccetes undergoes partial atrophy. The gall-bladder of the liver is absorbed ; and the liver itself ceases to communicate with the intestine.

4. The eye undergoes important changes in that it travels to the surface, and acquires all the characters of the normal vertebrate eye.

5. The brain becomes relatively larger but more compact, and the optic lobes (corpora bigemina) become more distinct.

6. The pericardial cavity becomes completely separated from the body cavity, and a distinct pericardium is formed.

7. The mesonephros of the larva disappears, and a fresh posterior part is formed.

Myxine. The ovum of Myxine when ready to be laid is inclosed, as shewn by Allen Thomson 1 , in an oval horny shell in many respects similar to that of Elasmobranchii ; from its ends there project a number of trumpet-shaped tubular processes, which no doubt serve to attach it to marine objects. No observations have been made on the development.

BIBLIOGRAPHY.

(77) E. Calberla. " Der Befruchtungsvorgang beim Petromyzon Planeri." Zeit.f. wiss. Zool., Vol. xxx. 1877.

(78) E. Calberla. "Ueb. d. Entwicklung d. Medullarrohres u. d. Chorda dorsalis d. Teleostier u. d. Petromyzonten." Morpholog. Jahrbuch, Vol. in. 1877.

(79) C. Kupffer u. B. Benecke. Der Vorgang d. Befruchtung am Ei d. Nennangen. Konigsberg, 1878.

(80) Aug. Miiller. " Ueber die Entwicklung d. Neunaugen." Muller's Archiv, 1856.

(81) Aug. Miiller. Beobachtungen iib. d. Befruchtungserscheinungen im Ei d. Neunaugen, Konigsberg, 1864.

1 Cyclopedia of Anat. and Phys. Article 'Ovum.'

CYCLOSTOMATA. IOI

(82) W. Miiller. "Das Urogenitalsystem d. Amphioxus u. d. Cyclostomen." Jenaische Zeitschrift, Vol. IX. 1875.

(83) Ph. Owsjannikoff. " Die Entwick. von d. Flussneunaugen." Vorlauf. Mittheilung. Melanges Biologiques tires du Bulletin de VAcad. Imp. St Petersbourg, Vol. vn. 1870.

(84) Ph. Owsjannikoff. On the development of Petromyzon fluviatilis (Russian).

(85) Anton Schneider. Beitrdge z. vergleich. Anat. u. Entwick. d. Wirbelthiere. Quarto. Berlin, 1879.

(86) M. S. Schultze. "Die Entwickl. v. Petromyzon Planeri." Gekronte Preisschrift. Haarlem, 1856.

(87) \V. B. Scott. " Vorlaufige Mittheilung lib. d. Entwicklungsgeschichte d. Petromyzonten." Zoologischer Anzeiger, Nos. 63 and 64. ill. Jahrg. 1880.

The Works of Francis Balfour 3-5

Vol. III. A Treatise on Comparative Embryology 2 (1885)

CHAPTER V. CYCLOSTOMATA