Opening
THE WORKS OF FRANCIS MAITLAND BALFOUR.
VOL. III.
Memorial Edition.
Cambridge:
PRINTED BY C. J. CLAY, M.A. AND SON, AT THE UNIVERSITY PRESS.
Memorial Edition.
THE WORKS
OF
FRANCIS MAITLAND BALFOUR,
M.A., LL.D., F.R.S.,
FELLOW OF TRINITY COLLEGE, AND PROFESSOR OF ANIMAL MORPHOLOGY IN THE UNIVERSITY OF CAMBRIDGE.
EDITED BY
M. FOSTER, F.R.S.,
PROFESSOR OF PHYSIOLOGY IN THE UNIVERSITY OF CAMBRIDGE;
AND
ADAM SEDGWICK, M.A.,
FELLOW AND LECTURER OF TRINITY COLLEGE, CAMBRIDGE.
VOL. III.
A TREATISE ON COMPARATIVE EMBRYOLOGY.
Vol. II. Vertebrata.
London: MACMILLAN AND CO. 1885
[The Right of Translation is reserved.]
PREFACE TO VOLUME II.
The present volume completes my treatise on Comparative Embryology. The first eleven chapters deal with the developmental history of the Chordata. These are followed by three comparative chapters completing the section of the work devoted to Systematic Embryology. The remainder of the treatise, from Chapter XIV. onwards, is devoted to Organogeny. For the reasons stated in the introduction to this part the organogeny of the Chordata has been treated with much greater fulness than that of the other groups of Metazoa.
My own investigations have covered the ground of the present volume much more completely than they did that of the first volume; a not inconsiderable proportion of the facts recorded having been directly verified by me.
The very great labour of completing this volume has been much lightened by the assistance I have received from my friends and pupils. Had it not been for their co-operation a large number of the disputed points, which I have been able to investigate during the preparation of the work, must have been left untouched.
My special thanks are due to Mr Sedgwick, who has not only devoted a very large amount of time and labour to correcting the proofs, but has made for me an index of this volume, and has assisted me in many other ways.
Dr Allen Thomson and Professor Kleinenberg of Messina have undertaken the ungrateful task of looking through my proof-sheets, and have made suggestions which have proved most valuable. To Professors Parker, Turner, and Bridge, I am also greatly indebted for their suggestions with reference to special chapters of the work.
CONTENTS OF VOLUME II.
I. CEPHALOCHORDA. Pp. 1-8
Segmentation and formation of the layers, pp. 1-3. Central nervous system, pp. 3, 4. Mesoblast, p. 5. General history of larva, pp. 6-8.
II. UROCHORDA. Pp. 9-39
Solitaria, pp. 9-23. Development of embryo, pp. 9-15. Growth and structure of free larva, pp. 15-19. Retrogressive metamorphosis, pp. 19-23. Sedentaria, p. 23. Natantia, pp. 23-28. Doliolidæ, pp. 28, 29. Salpidæ, pp. 29-34. Appendicularia, p. 34. Metagenesis, pp. 34-38.
III. ELASMOBRANCHII. Pp. 40-67
Segmentation and formation of the layers, pp. 40-47. Epiblast, p. 47. Mesoblast, pp. 47-51. Hypoblast and notochord, pp. 51-54. General features of the embryo at successive stages, pp. 55-62. The yolk-sack, pp. 62-66.
IV. TELEOSTEI. Pp. 68-82
Segmentation and formation of the layers, pp. 68-73. General history of the layers, pp. 73-75. General development of the embryo, pp. 76-81.
V. CYCLOSTOMATA. Pp. 83-101
Segmentation and formation of the layers, pp. 83-86. Mesoblast and notochord, pp. 86, 87. General history of the development, pp. 87-97. Metamorphosis, pp. 97-100. Myxine, p. 100.
VI. GANOIDEI. Pp. 102-119
Acipenser, pp. 102-110. Segmentation and formation of the layers, pp. 102-104. General development of the embryo and larva, pp. 104-110. Lepidosteus, pp. 111-119. Segmentation, pp. 111, 112. General development of embryo and larva, pp. 112-119. General observations on the embryology of Ganoids, p. 119.
VII. AMPHIBIA. Pp. 120-144
Oviposition and impregnation, pp. 120, 121. Formation of the layers, pp. 121-124. Epiblast, pp. 125-127. Mesoblast and notochord, pp. 128, 129. Hypoblast, pp. 129-131. General growth of the embryo, pp. 131-143. Anura, pp. 131-141. Urodela, pp. 141-143. Gymnophiona, p. 143.
VIII. AVES. Pp. 145-201
Segmentation and formation of the layers, pp. 145-166. General history of the germinal layers, pp. 166-169. General development of the embryo, pp. 169-180. Foetal membranes, pp. 185-199. Amnion, pp. 185-191. Allantois, pp. 191-193. Yolk-sack, pp. 193-199.
IX. REPTILIA. Pp. 202-213
Lacertilia, pp. 202-209. Segmentation and formation of the layers, pp. 202-207. General development of the embryo, p. 208. Embryonic membranes and yolk-sack, pp. 208-210. Ophidia, p. 210. Chelonia, pp. 210-212.
X. MAMMALIA. Pp. 214-274
Segmentation and formation of the layers, pp. 214-227. General growth of the embryo, pp. 227-232. Embryonic membranes and yolk-sack, pp. 232-239. Comparative history of the Mammalian foetal membranes, pp. 239-257. Comparative histology of the placenta, pp. 257-259. Evolution of the placenta, pp. 259-261. Development of the Guinea-pig, pp. 262-265. The human embryo, pp. 265-270.
XI. COMPARISON OF THE FORMATION OF THE GERMINAL LAYERS AND OF THE EARLY STAGES IN THE DEVELOPMENT OF VERTEBRATES. Pp. 275-310
Formation of the gastrula, pp. 275-292. The formation of the mesoblast and of the notochord, pp. 292-300. The epiblast, pp. 300-304. Formation of the central nervous system, pp. 301-304. Formation of the organs of special sense, p. 304. Summary of organs derived from the three germinal layers, pp. 304-306. Growth in length of the Vertebrate embryo, pp. 306-309. The evolution of the allantois and amnion, pp. 309, 310.
XII. OBSERVATIONS ON THE ANCESTRAL FORM OF THE CHORDATA. Pp. 311-330
General considerations, pp. 311-316. The medullary canal, pp. 316, 317. The origin and nature of the mouth, pp. 317-321. The cranial flexure, pp. 321, 322. The postanal gut and neurenteric canal, pp. 322-325. The body-cavity and mesoblastic somites, p. 325. The notochord, pp. 325, 326. Gill clefts, pp. 326, 327. Phylogeny of the Chordata, pp. 327-329.
XIII. GENERAL CONCLUSIONS. Pp. 331-388
I. Mode of origin and homologies of the germinal layers, pp. 331-360. Formation of the primary germinal layers, pp. 332, 333. Invagination, pp. 333-335. Delamination, pp. 335-338. Phylogenetic significance of delamination and invagination, pp. 338-345. Homologies of the germinal layers, pp. 345, 346. The origin of the mesoblast, pp. 346-360.
II. Larval forms: their nature, origin, and affinities. Preliminary considerations, pp. 360-362. Types of larvæ, pp. 363-384. Phylogenetic conclusions, pp. 384, 385. General conclusions and summary, pp. 385, 386.
II. ORGANOGENY
INTRODUCTION. Pp. 391, 392.
XIV. THE EPIDERMIS AND ITS DERIVATIVES. Pp. 393-399
Protective epidermic structures, pp. 393-397. Dermal skeletal structures, p. 397. Glands, pp. 397, 398.
XV. THE NERVOUS SYSTEM. Pp. 400-469
The origin of the nervous system, pp. 400-405. Nervous system of the Invertebrata, pp. 405-414. Central nervous system of the Vertebrata, pp. 415-447. Spinal chord, pp. 415-419. General development of the brain, pp. 419-423. Hind-brain, pp. 424-427. Mid-brain, pp. 427, 428. General development of fore-brain, pp. 428-430. Thalamencephalon, pp. 430-435. Pituitary body, pp. 435-437. Cerebral Hemispheres, pp. 437-444. Olfactory lobes, pp. 444, 445. General conclusions as to the central nervous system of the Vertebrata, pp. 445-447. Development of the cranial and spinal nerves, pp. 448-466. Spinal nerves, pp. 448-455. Cranial nerves, pp. 455-466. Sympathetic nervous system, pp. 466-468.
XVI. ORGANS OF VISION. Pp. 470-511
Coelenterata, pp. 471, 472. Mollusca, pp. 472-479. Chætopoda, p. 479. Chætognatha, p. 479. Arthropoda, pp. 479-483. Vertebrata general, pp. 483-490. Retina, pp. 490-492. Optic nerve, pp. 492, 493. Choroid fissure, p. 493. Lens, pp. 494, 495. Vitreous humour, pp. 494, 495. Cornea, pp. 495-497. Aqueous humour, p. 497. Comparative development of Vertebrate eye, pp. 497-506. Ammocoete eye, pp. 498, 499. Optic vesicles, p. 499. Lens, p. 499. Cornea, p. 500. Optic nerve and choroid fissure, pp. 500-505. Iris and ciliary processes, p. 506. Accessory organs connected with the eye, p. 506. Eyelids, p. 506. Lacrymal glands, p. 506. Lacrymal duct, pp. 506, 507. Eye of the Tunicata, pp. 507-509. Accessory eyes in the Vertebrata, pp. 509, 510.
XVII. AUDITORY ORGAN, OLFACTORY ORGAN, AND SENSE ORGANS OF THE LATERAL LINE. Pp. 512-541
Auditory organs, pp. 512-531. General structure of auditory organs, pp. 512, 513. Auditory organs of the Coelenterata, pp. 513-515. Auditory organs of the Mollusca, pp. 515, 516. Auditory organs of the Crustacea, p. 516. Auditory organs of the Vertebrata, pp. 516-530. Auditory vesicle, pp. 517-524. Organ of Corti, pp. 524-527. Accessory structures connected with the organ of hearing of terrestrial vertebrata, pp. 527-530. Auditory organ of the Tunicata, pp. 530, 531. Bibliography of Auditory organs, p. 531.
Olfactory organs, pp. 531-538. Bibliography of Olfactory organs, p. 538. Sense organs of the lateral line, pp. 538-540. Bibliography of sense organs of lateral line, pp. 540, 541.
XVIII. THE NOTOCHORD, THE VERTEBRAL COLUMN, THE RIBS, AND THE STERNUM. Pp. 542-563
Introductory remarks on the origin of the skeleton, pp. 542-544. Bibliography of the origin of the skeleton, pp. 544, 545. The notochord and its cartilaginous sheath, pp. 545-549. The vertebral arches and the vertebral bodies, pp. 549-559. Cyclostomata, p. 549. Elasmobranchii, pp. 549-553. Ganoidei, p. 553. Teleostei, p. 553. Amphibia, pp. 553-556. Reptilia, pp. 556, 557. Aves, pp. 557, 558. Mammalia, pp. 558, 559. Bibliography of the notochord and vertebral column, p. 560. Ribs, pp. 560-562. Sternum, pp. 562, 563. Bibliography of the ribs and sternum, p. 563.
XIX. THE SKULL. Pp. 564-598
Preliminary remarks, pp. 564, 565. The cartilaginous cranium, pp. 565-571. The parachordals and notochord, pp. 566, 567. The trabeculæ, pp. 567-570. The sense capsules, pp. 570, 571. The branchial skeleton, pp. 572-591. General structure of, pp. 572-575. Mandibular and hyoid arches, pp. 575-591. Elasmobranchii, pp. 576-579. Teleostei, pp. 579-581. Amphibia, pp. 581-588. Sauropsida, pp. 588, 589. Mammalia, pp. 589-591. Membrane bones and ossifications of the cranium, pp. 592-597. Membrane bones, pp. 592-595. Ossifications of the cartilaginous cranium, pp. 595-597. Labial cartilages, p. 597. Bibliography of the skull, p. 598.
XX. PECTORAL AND PELVIC GIRDLES AND THE SKELETON OF THE LIMBS. Pp. 599-622
The Pectoral girdle, pp. 599-606. Pisces, pp. 599-601. Amphibia and Amniota, pp. 601, 602. Lacertilia, p. 603. Chelonia, p. 603. Aves, pp. 603, 604. Mammalia, p. 604. Amphibia, p. 605. Bibliography of Pectoral girdle, pp. 605, 606.
The Pelvic girdle, pp. 606-608. Pisces, pp. 606, 607. Amphibia and Amniota, pp. 606, 607. Amphibia, p. 607. Lacertilia, p. 607. Mammalia, p. 608. Bibliography of Pelvic girdle, p. 608. Comparison of pectoral and pelvic girdles, pp. 608, 609.
Limbs, pp. 609-622. The piscine fin, pp. 609-618. The cheiropterygium, pp. 618-622. Bibliography of limbs, p. 622.
XXI. THE BODY CAVITY, THE VASCULAR SYSTEM AND THE VASCULAR GLANDS. Pp. 623-666
The body cavity, pp. 623-632. General, pp. 623, 624. Chordata, pp. 624-632. Abdominal pores, pp. 626, 627. Pericardial cavities, pleural cavities and diaphragm, pp. 627-632. Bibliography of body cavity, p. 632.
The vascular system, pp. 632-663. General, pp. 632, 633. The heart, pp. 633-643. Bibliography of the heart, p. 643. Arterial system, pp. 643-651. Bibliography of the arterial system, p. 651. Venous system, pp. 651-663. Bibliography of the venous system, p. 663. Lymphatic system and spleen, p. 664. Bibliography of spleen, p. 664. Suprarenal bodies, pp. 664-666. Bibliography of suprarenal bodies, p. 666.
XXII. THE MUSCULAR SYSTEM. Pp. 667-679
Evolution of muscle-cells, pp. 667, 668. Voluntary muscular system of the Chordata, pp. 668-679. Muscular fibres, pp. 668, 669. Muscular system of the trunk and limbs, pp. 673-676. The somites and muscular system of the head, pp. 676-679. Bibliography of muscular system, p. 679.
XXIII. EXCRETORY ORGANS. Pp. 680-740
Platyelminthes, pp. 680, 681. Mollusca, pp. 681, 682. Polyzoa, pp. 682, 683. Branchiopoda, p. 683. Chætopoda, pp. 683-686. Gephyrea, pp. 686, 687. Discophora, pp. 687, 688. Arthropoda, pp. 688, 689. Nematoda, p. 689. Excretory organs and generative ducts of the Craniata, pp. 689-737. General, pp. 689, 690. Elasmobranchii, pp. 690-699. Cyclostomata, pp. 700, 701. Teleostei, pp. 701-704. Ganoidei, pp. 704-707. Dipnoi, p. 707. Amphibia, pp. 707-713. Amniota, pp. 713-727. General conclusions and summary, pp. 728-737. Pronephros, pp. 728, 729. Mesonephros, pp. 729-732. Genital ducts, pp. 732-736. Metanephros, pp. 736, 737. Comparison of the excretory organs of the Chordata and Invertebrata, pp. 737, 738. Bibliography of Excretory organs, pp. 738-740.
XXIV. GENERATIVE ORGANS AND GENITAL DUCTS. Pp. 741-753
Generative organs, pp. 741-748. Porifera, p. 741. Coelenterata, pp. 741-743. Chætopoda and Gephyrea, p. 743. Chætognatha, pp. 743-745. Polyzoa, p. 745 Nematoda, p. 745. Insecta, p. 745. Crustacea, pp. 745, 746. Chordata, pp. 746-748. Bibliography of generative organs, p. 748. Genital ducts, pp. 748-753.
XXV. THE ALIMENTARY CANAL AND ITS APPENDAGES IN THE CHORDATA. Pp. 754-780
Mesenteron, pp. 754-774. Subnotochordal rod, pp. 754-756. Splanchnic mesoblast and mesentery, pp. 756-758. Respiratory division of the Mesenteron, pp. 758-766. Thyroid body, pp. 759-762. Thymus gland, pp. 762, 763. Swimming bladder and lungs, pp. 763-766, The middle division of the Mesenteron, pp. 766-771. Cloaca, pp. 766, 767. Intestine, pp. 767, 768. Liver, pp. 769, 770. Pancreas, pp. 770, 771. Postanal section of the Mesenteron, pp. 771-774.
The stomodæum, pp. 774-778. Comparative development of oral cavity, pp. 774-776. Teeth, pp. 776-778.
The proctodæum, pp. 778-780. Bibliography of alimentary canal, p. 780.
EMBRYOLOGY.
I. CEPHALOCHORDA
The developmental history of the Chordata has been studied far more completely than that of any of the groups so far considered; and the results which have been arrived at are of striking interest and importance. Three main subdivisions of this group can be recognized: (1) the Cephalochorda containing the single genus Amphioxus; (2) the Urochorda or Tunicata; and (3) the Vertebrata[1]. The members of the second and probably of the first of these groups have undergone degeneration, but at the same time the members of the first group especially undergo a less modified development than that of other Chordata.
[1] The term Vertebrata is often used to include the Cephalochorda. It is in many ways convenient to restrict its use to the forms which have at any rate some indications of vertebræ; a restriction which has the further convenience of restoring to the term its original limitations. In the first volume of this work the term Craniata was used for the forms which I now propose to call Vertebrata.
CEPHALOCHORDA.
Our knowledge of the development of Amphioxus is mainly due to Kowalevsky (Nos. 1 and 2). The ripe eggs appear to be dehisced into the branchial or atrial cavity, and to be transported thence through the branchial clefts into the pharynx, and so through the mouth to the exterior. (Kowalevsky, No. 1, and Marshall, No. 5.)
[FIG. 1. THE SEGMENTATION OF AMPHIOXUS. (Copied from Kowalevsky.)
B. Stage with four equal segments. C. Stage after the four segments have become divided by an equatorial furrow into eight equal segments. D. Stage in which a single layer of cells encloses a central segmentation cavity. E. Somewhat older stage in optical section.
sg. segmentation cavity.]
When laid the egg is about 0.105 mm. in diameter. It is invested by a delicate membrane, and is somewhat opaque owing to the presence of yolk granules, which are however uniformly distributed through it, and proportionately less numerous than in the ova of most Chordata. Impregnation is external and the segmentation is nearly regular (fig. 1). A small segmentation cavity is visible at the stage with four segments, and increases during the remainder of the segmentation; till at the close (fig. 1 E) the embryo consists of a blastosphere formed of a single layer of cells enclosing a large segmentation cavity. One side of the blastosphere next becomes invaginated, and during the process the embryo becomes ciliated, and commences to rotate. The cells forming the invaginated layer become gradually more columnar than the remaining cells, and constitute the hypoblast; and a structural distinction between the epiblast and hypoblast is thus established. In the course of the invagination the segmentation cavity becomes gradually obliterated, and the embryo first assumes a cup-shaped form with a wide blastopore, but soon becomes elongated, while the communication of the archenteron, or cavity of invagination, with the exterior is reduced to a small blastopore (fig. 2 A), placed at the pole of the long axis which the subsequent development shews to be the hinder end of the embryo. The blastopore is often known in other Chordata as the anus of Rusconi. Before the invagination is completed the larva throws off the egg-membrane, and commences to lead a free existence.
[FIG. 2. EMBRYOS OF AMPHIOXUS. (After Kowalevsky.)
The parts in black with white lines are epiblastic; the shaded parts are hypoblastic. A. Gastrula stage in optical section. B. Slightly later stage after the neural plate np has become differentiated, seen as a transparent object from the dorsal side. C. Lateral view of a slightly older larva in optical section. D. Dorsal view of an older larva with the neural canal completely closed except for a small pore (no) in front. E. Older larva seen as a transparent object from the side.
bl. blastopore (which becomes in D the neurenteric canal); ne. neurenteric canal; np. neural or medullary plate; no. anterior opening of neural canal; ch. notochord; so^I, so^{II}. first and second mesoblastic somites.]
Up to this stage the larva, although it has acquired a cylindrical elongated form, has only the structure of a simple two-layered gastrula; but the changes which next take place give rise on the one hand to the formation of the central nervous system, and on the other to the formation of the notochord and mesoblastic somites[2]. The former structure is developed from the epiblast and the two latter from the hypoblast.
[2] The protovertebræ of most embryologists will be spoken of as mesoblastic somites.
The formation of the central nervous system commences with the flattening of the dorsal surface of the embryo. The flattened area forms a plate (fig. 2 B and fig. 3 A, np), extending backwards to the blastopore, which has in the meantime passed round to the dorsal surface. The sides of the plate become raised as two folds, which are most prominent posteriorly, and meet behind the blastopore, but shade off in front. The two folds next unite dorsally, so as to convert the previous groove into a canal[3]--the neural or medullary canal. They unite first of all over the blastopore, and their line of junction extends from this point forwards (fig. 2 C, D, E). There is in this way formed a tube on the floor of which the blastopore opens behind, and which is itself open in front. Finally the medullary canal is formed for the whole length of the embryo. The anterior opening persists however for some time. The communication between the neural and alimentary tracts becomes interrupted when the caudal fin appears and the anus is formed. The neural canal then extends round the end of the notochord to the ventral side, but subsequently retreats to the dorsal side and terminates in a slight dilatation.
[3] The details of this process are spoken of below.
In the formation of the medullary canal there are two points deserving notice--viz. (1) the connection with the blastopore; (2) the relation of the walls of the canal to the adjoining epiblast. With reference to the first of these points it is clear that the fact of the blastopore opening on the floor of the neural canal causes a free communication to exist between the archenteron or gastrula cavity and the neural canal; and that, so long as the anterior pore of the neural canal remains open, the archenteron communicates indirectly with the exterior (vide fig. 2 E). It must not however be supposed (as has been done by some embryologists) that the pore at the front end of the neural canal represents the blastopore carried forwards. It is even probable that what Kowalevsky describes as the carrying of the blastopore to the dorsal side is really the commencement of the formation of the neural canal, the walls of which are continuous with the lips of the blastopore. This interpretation receives support from the fact that at a later stage, when the neural and alimentary canals become separated, the neural canal extends round the posterior end of the notochord to the ventral side. The embryonic communication between the neural and alimentary canals is common to most Chordata; and the tube connecting them will be called the neurenteric canal. It is always formed in fundamentally the same manner as in Amphioxus. With reference to the second point it is to be noted that Amphioxus is exceptional amongst the Chordata in the fact that, before the closure of the neural groove, the layer of cells which will form the neural tube becomes completely separated from the adjoining epiblast (fig. 3 A), and forms a structure which may be spoken of as the medullary plate; and that in the closure of the neural canal the lateral epiblast forms a complete layer above this plate before the plate itself is folded over into a closed canal. This peculiarity will be easily understood from an examination of fig. 3 A, B and C.
[FIG. 3. SECTIONS OF AN AMPHIOXUS EMBRYO AT THREE STAGES. (After Kowalevsky.)
A. Section at gastrula stage. B. Section of an embryo slightly younger than that represented in fig. 2 D. C. Section through the anterior part of an embryo at the stage represented in fig. 2 E.
np. neural plate; nc. neural canal; mes. archenteron in A and B, and mesenteron in C; ch. notochord; so. mesoblastic somite.]
The formation of the mesoblastic somites commences, at about the same time as that of the neural canal, as a pair of hollow outgrowths of the walls of the archenteron. These outgrowths, which are shewn in surface view in fig. 2 B and D, so, and in section in fig. 3 B and C, so, arise near the front end of the body and gradually extend backwards as wing-like diverticula of the archenteric cavity. As they grow backwards their dorsal part becomes divided by transverse constrictions into cubical bodies (fig. 2 D and E), which, with the exception of the foremost, soon cease to open into what may now be called the mesenteron, and form the mesoblastic somites. Each mesoblastic somite, after its separation from the mesenteron, is constituted of two layers, an inner one--the splanchnic--and an outer--the somatic, and a cavity between the two which was originally continuous with the cavity of the mesenteron. Eventually the dorsal parts of the outgrowths become separated from the ventral, and form the muscle-plates, while their cavities atrophy. The cavity of the ventral part, which is not divided into separate sections by the above described constrictions, remains as the true body cavity. The ventral part of the inner layer of the mesoblastic outgrowths gives rise to the muscular and connective tissue layers of the alimentary tract, and the dorsal part to a section of the voluntary muscular system. The ventral part of the outer layer gives rise to the somatic mesoblast, and the dorsal to a section of the voluntary muscular system. The anterior mesoblastic somite long retains its communication with the mesenteron, and was described by Max Schultze, and also at first by Kowalevsky, as a glandular organ. While the mesoblastic somites are becoming formed the dorsal wall of the mesenteron develops a median longitudinal fold (fig. 3 B, ch), which is gradually separated off from before backwards as a rod (fig. 3 C, ch), underlying the central nervous system. This rod is the notochord. After the separation of those parts the remainder of the hypoblast forms the wall of the mesenteron.
With the formation of the central nervous system, the mesoblastic somites, the notochord, and the alimentary tract the main systems of organs are established, and it merely remains briefly to describe the general changes of form which accompany the growth of the larva into the adult. By the time the larva is but twenty-four hours old there are formed about seventeen mesoblastic somites. The body, during the period in which these are being formed, remains cylindrical, but shortly afterwards it becomes pointed at both ends, and the caudal fin appears. The fine cilia covering the larva also become replaced by long cilia, one to each cell. The mesenteron is still completely closed, but on the right side of the body, at the level of the front end of the mesenteron, the hypoblast and epiblast now grow together, and a perforation becomes formed through their point of contact, which becomes the mouth. The anus is probably formed about the same time if not somewhat earlier[4].
[4] The lateral position of the mouth in the embryo Amphioxus has been regarded as proving that the mouth represents a branchial cleft, but the general asymmetry of the organs is such that no great stress can, I think, be laid on the position of the mouth.
[FIG. 4. SECTIONS THROUGH TWO ADVANCED EMBRYOS OF AMPHIOXUS TO SHEW THE FORMATION OF THE PERIBRANCHIAL CAVITY. (After Kowalevsky.)
In A are seen two folds of the body wall with a prolongation of the body cavity. In B the two folds have coalesced ventrally, forming a cavity into which a branchial cleft is seen to open.
mes. mesenteron; br.c. branchial cavity; pp. body cavity.]
Of the subsequent changes the two most important are (1) the formation of the gill slits or clefts; (2) the formation of the peribranchial or atrial cavity.
The formation of the gill slits is, according to Kowalevsky's description, so peculiar that one is almost tempted to suppose that his observations were made on pathological specimens. The following is his account of the process. Shortly after the formation of the mouth there appears on the ventral line a coalescence between the epiblast and hypoblast. Here an opening is formed, and a visceral cleft is thus established, which passes to the left side, viz. the side opposite the mouth. A second and apparently a third slit are formed in the same way. The stages immediately following were not observed, but in the next stage twelve slits were present, no longer however on the left side, but in the median ventral line. There now appears on the side opposite the mouth, and the same therefore as that originally occupied by the first three clefts, a series of fresh clefts, which in their growth push the original clefts over to the same side as the mouth. Each of the fresh clefts becomes divided into two, which form the permanent clefts of their side.
The gill slits at first open freely to the exterior, but during their formation two lateral folds of the body wall, containing a prolongation of the body cavity, make their appearance (fig. 4 A), and grow downwards over the gill clefts, and finally meet and coalesce along the ventral line, leaving a widish cavity between themselves and the body wall. Into this cavity, which is lined by epiblast, the gill clefts open (fig. 4 B, br.c). This cavity--which forms a true peribranchial cavity--is completely closed in front, but owing to the folds not uniting completely behind it remains in communication with the exterior by an opening known as the atrial or abdominal pore.
The vascular system of Amphioxus appears at about the same time as the first visceral clefts.
BIBLIOGRAPHY.
(1) A. Kowalevsky. "Entwicklungsgeschichte des Amphioxus lanceolatus." Mém. Acad. Impér. des Sciences de St Pétersbourg, Series VII. Tom. xi. 1867.
(2) A. Kowalevsky. "Weitere Studien über die Entwicklungsgeschichte des Amphioxus lanceolatus." Archiv f. mikr. Anat., Vol. XIII. 1877.
(3) Leuckart u. Pagenstecher. "Untersuchungen über niedere Seethiere." Müller's Archiv, 1858.
(4) Max Schultze. "Beobachtung junger Exemplare von Amphioxus." Zeit. f. wiss. Zool., Bd. III. 1851.
(5) A. M. Marshall. "On the mode of Oviposition of Amphioxus." Jour. of Anat. and Phys., Vol. X. 1876.
II. UROCHORDA[5]
[5] The following classification of the Urochorda is adopted in the present chapter.
I. Caducichordata. {Solitaria ex. Ascidia. A. SIMPLICIA {Socialia ex. Clavellina. {Sedentaria ex. Botryllus. B. COMPOSITA {Natantia ex. Pyrosoma. {Salpidæ. C. CONSERTA {Doliolidæ. II. Perennichordata. Ex. Appendicularia.
In the Solitaria, except Cynthia, the eggs are generally laid, and impregnation is effected sometimes before and sometimes after the eggs have left the atrial cavity. In Cynthia and most Caducichordata development takes place within the body of the parent, and in the Salpidæ a vascular connection is established between the parent and the single foetus, forming a structure physiologically comparable with the Mammalian placenta.
Solitaria. The development of the Solitary Ascidians has been more fully studied than that of the other groups, and appears moreover to be the least modified. It has been to a great extent elucidated by the splendid researches of Kowalevsky (Nos. 18 and 20), whose statements have been in the main followed in the account below. Their truth seems to me to be established, in spite of the scepticism they have met with in some quarters, by the closeness of their correspondence with the developmental phenomena in Amphioxus.
The type most fully investigated by Kowalevsky is Ascidia (Phallusia) mammillata; and the following description must be taken as more especially applying to this type.
The segmentation is complete and regular. A small segmentation cavity appears fairly early, and is surrounded, according to Kowalevsky, by a single layer of cells, though on this point Kupffer (No. 27) and Giard (No. 11) are at variance with him.
[FIG. 5. TRANSVERSE SECTION THROUGH THE FRONT END OF AN EMBRYO OF PHALLUSIA MAMMILLATA. (After Kowalevsky.)
The embryo is slightly younger than that represented in fig. 8 III.
mg. medullary groove; al. alimentary tract.]
The segmentation is followed by an invagination of nearly the same character as in Amphioxus. The blastosphere resulting from the segmentation first becomes flattened on one side, and the cells on the flatter side become more columnar (fig. 8 I.). Very shortly a cup-shaped form is assumed, the concavity of which is lined by the more columnar cells. The mouth of the cup or blastopore next becomes narrowed; while at the same time the embryo becomes oval. The blastopore is situated not quite at a pole of the oval but in a position which subsequent development shews to be on the dorsal side close to the posterior end of the embryo. The long axis of the oval corresponds with the long axis of the embryo. At this stage the embryo consists of two layers; a columnar hypoblast lining the central cavity or archenteron, and a thinner epiblastic layer. The dorsal side of the embryo next becomes flattened (fig. 8 II.), and the epiblast covering it is shortly afterwards marked by an axial groove continued forwards from the blastopore to near the front end of the body (fig. 5, mg). This is the medullary groove, and it soon becomes converted into a closed canal--the medullary or neural canal--below the external skin (fig. 6, n.c). The closure is effected by the folds on each side of the furrow meeting and coalescing dorsally. The original medullary folds fall into one another behind the blastopore so that the blastopore is situated on the floor of the groove, and, on the conversion of the groove into a canal, the blastopore connects the canal with the archenteric cavity, and forms a short neurenteric canal. The closure of the medullary canal commences at the blastopore and is thence continued forwards, the anterior end of the canal remaining open. The above processes are represented in longitudinal section in fig. 8 III, n. When the neural canal is completed for its whole length, it still communicates by a terminal pore with the exterior. In the relation of the medullary canal to the blastopore, as well as in the closure of the medullary groove from behind forwards, the Solitary Ascidians agree closely with Amphioxus.
[FIG. 6. TRANSVERSE OPTICAL SECTION OF THE TAIL OF AN EMBRYO OF PHALLUSIA MAMMILLATA. (After Kowalevsky.)
The section is from an embryo of the same age as fig. 8 IV.
ch. notochord; n.c. neural canal; me. mesoblast; al. hypoblast of tail.]
The cells of the dorsal wall of the archenteron immediately adjoining the front and sides of the blastopore have in the meantime assumed a somewhat different character from the remaining cells of the archenteron, and give rise to a body which, when viewed from the dorsal surface, has somewhat the form of a horseshoe. This body was first observed by Metschnikoff. On the elongation of the embryo and the narrowing of the blastopore the cells forming this body arrange themselves as a broad linear cord, two cells wide, underlying about the posterior half of the neural canal (fig. 7, ch). They form the rudiment of the notochord, which, as in Amphioxus, is derived from the dorsal wall of the archenteron. They are seen in longitudinal section in fig. 8 II. and III. ch.
With the formation of the notochord the body of the embryo becomes divided into two distinct regions--a posterior region where the notochord is present, and an anterior region into which it is not prolonged. These two regions correspond with the tail and the trunk of the embryo at a slightly later stage. The section of the archenteric cavity in the trunk dilates and constitutes the permanent mesenteron (figs. 7, al, and 8 III. and IV. dd). It soon becomes shut off from the slit-like posterior part of the archenteron. The nervous system in this part also dilates and forms what may be called the cephalic swelling (fig. 8 IV.), and the pore at its anterior extremity gradually narrows and finally disappears. In the region of the tail we have seen that the dorsal wall of the archenteron becomes converted into the notochord, which immediately underlies the posterior part of the medullary canal, and soon becomes an elongated cord formed of a single or double row of flattened cells. The lateral walls of the archenteron (fig. 7, me) in the tail become converted into elongated cells arranged longitudinally, which form powerful lateral muscles (fig. 8 IV. m). After the formation of the notochord and of the lateral muscles there remains of the archenteron in the tail only the ventral wall, which according to Kowalevsky forms a simple cord of cells (fig. 6, al). It is however not always present, or else has escaped the attention of other observers. It is stated by Kowalevsky to be eventually transformed into blood corpuscles. The neurenteric canal leads at first into the narrow space between the above structures, which is the remnant of the posterior part of the lumen of the archenteron. Soon both the neurenteric canal and the caudal remnant of the archenteron become obliterated.
[FIG. 7. OPTICAL SECTION OF AN EMBRYO OF PHALLUSIA MAMMILLATA. (After Kowalevsky.)
The embryo is of the same age as fig. 8 III, but is seen in longitudinal horizontal section.
part of body; ch. notochord; me. mesoblast.]
During the above changes the tail becomes considerably elongated and, owing to the larva being still in the egg-shell, is bent over to the ventral side of the trunk.
[FIG. 8. VARIOUS STAGES IN THE DEVELOPMENT OF PHALLUSIA MAMMILLATA. (From Huxley; after Kowalevsky.)
The embryos are represented in longitudinal vertical section. I. Commencing gastrula stage. fh. segmentation cavity. II. Late gastrula stage with flattened dorsal surface. eo. blastopore; ch. notochord; dd. hypoblast. III. A more advanced embryo with a partially-formed neural tube. ch. and dd. as before; n. neural tube; c. epiblast. IV. Older embryo in which the formation of the neural tube is completed. dd. hypoblast enclosing persistent section of alimentary tract; dd´. hypoblast in the tail; m. muscles. V. Larva just hatched. The end of the tail is not represented. a. eye; gb. dilated extremity of neural tube with otolith projecting into it; Rg. anterior swelling of the spinal division of the neural tube; f. anterior pore of neural tube; Rm. posterior part of neural tube; o. mouth; Chs. notochord; kl. atrial invagination; dd. branchial region of alimentary tract; d. commencement of oesophagus and stomach; dd´. hypoblast in the tail; m. muscles; hp. papilla for attachment. VI. Body and anterior part of the tail of a two days' larva. klm. atrial aperture; en. endostyle; ks. branchial sack; 1ks. 2ks. branchial slits; bb. branchial vessel between them; ch. axial portion of notochord; chs. peripheral layer of cells. Other reference letters as before.]
The larva at this stage is represented in a side view in fig. 8 IV. The epidermis is formed throughout of a single layer of cells. In the trunk the mesenteron is shewn at dd and the dilated part of the nervous system, no longer communicating with the exterior, at n. In the tail the notochord is shewn at ch, the muscles at m, and the solid remnant of the ventral wall of the archenteron at dd´. The delicate continuation of the neural canal in the tail is seen above the notochord at n. An optical section of the tail is shewn in fig. 6. It is worthy of notice that the notochord and muscles are formed in the same manner as in Amphioxus, except that the process is somewhat simplified. The mode of disappearance of the archenteric cavity in the tail, by the employment of the whole of its walls in the formation of various organs, is so peculiar, that I feel some hesitation in accepting Kowalevsky's statements on this head[6].
[6] It is more probable that this part of the alimentary tract is equivalent to the postanal gut of many Vertebrata, which is at first a complete tube, but disappears later by the simple absorption of the walls.
The larva continues to grow in length, and the tail becomes further curled round the ventral side of the body within the egg-membrane. Before the tail has nearly reached its full length the test becomes formed as a cuticular deposit of the epiblast cells (O. Hertwig, No. 13, Semper, No. 37). It appears first in the tail and gradually extends till it forms a complete investment round both tail and trunk, and is at first totally devoid of cells. Shortly after the establishment of the test there grow out from the anterior end of the body three peculiar papillæ, developed as simple thickenings of the epidermis. At a later stage, after the hatching of the larva, these papillæ develop glands at their extremities, secreting a kind of glutinous fluid[7]. After these papillæ have become formed cells first make their appearance in the test; and there is simultaneously formed a fresh inner cuticular layer of the test, to which at first the cells are confined, though subsequently they are found in the outer layer also. On the appearance of cells in the test the latter must be regarded as a form, though a very abnormal one, of connective tissue. When the tail of the larva has reached a very considerable length the egg-membrane bursts, and the larva becomes free. The hatching takes place in Asc. canina about 48-60 hours after impregnation. The free larva (fig. 8 V.) has a swollen trunk, and a very long tail, which soon becomes straightened out. It has a striking resemblance to a tadpole (vide fig. 10).
[7] It is probable that these papillæ are very primitive organs of the Chordata. Structures, which are probably of the same nature, are formed behind the mouth in the larvæ of Amphibia, and in front of the mouth in the larvæ of Ganoids (Acipenser, Lepidosteus), and are used by these larvæ for attaching themselves.
In the free larval condition the Ascidians have in many respects a higher organization than in the adult state. It is accordingly convenient to divide the subsequent development into two periods, the first embracing the stages from the condition represented in fig. 8 V. up to the full development of the free larva, and the second the period from the full development of the larva to the attainment of the fixed adult condition.
Growth and Structure of the free larva.
The nervous system. The nervous system was left as a closed tube consisting of a dilated anterior division, and a narrow posterior one. The former may be spoken of as the brain, and the latter as the spinal cord; although the homologies of these two parts are quite uncertain. The anterior part of the spinal cord lying within the trunk dilates somewhat (fig. 8 V. and VI. Rg) and there may thus be distinguished a trunk and a caudal section of the spinal cord.
[FIG. 9. LARVA OF ASCIDIA MENTULA. (From Gegenbaur; after Kupffer.) Only the anterior part of the tail is represented.
N´. anterior swelling of neural tube; N. anterior swelling of spinal portion of neural tube; n. hinder part of neural tube; ch. notochord; K. branchial region of alimentary tract; d. oesophageal and gastric region of alimentary tract; O. eye; a. otolith; o. mouth; s. papilla for attachment.]
The original single vesicle of the brain becomes divided by the time the larva is hatched into two sections (fig. 9)--(1) an anterior vesicle with, for the most part, thin walls, in which unpaired auditory and optic organs make their appearance, and (2) a posterior nearly solid cephalic ganglion, through which there passes a narrow continuation of the central canal of the nervous system. This ganglion consists of a dorsal section formed of distinct cells, and a ventral section formed of a punctated material with nuclei. The auditory organ[8] consists of a 'crista acustica' (fig. 9), in the form of a slight prominence of columnar cells on the ventral side of the anterior cerebral vesicle; to the summit of which a spherical otolith is attached by fine hairs. In the crista is a cavity containing clear fluid. The dorsal half of the otolith is pigmented: the ventral half is without pigment. The crista is developed in situ, but the otolith is formed from a single cell on the dorsal side of the cerebral vesicle, which forms a projection into the cavity of the vesicle, and then travels (in a manner not clearly made out) round the right side of the vesicle till it comes to the crista; to which it is at first attached by a narrow pedicle. The fully developed eye (figs. 8 VI. and 9, O) consists of a cup-shaped retina, which forms a prominence slightly on the right side of the posterior part of the dorsal wall of the anterior cerebral vesicle, and of refractive media. The retina is formed of columnar cells, the inner ends of which are imbedded in pigment. The refractive media of the eye are directed towards the cavity of the cerebral vesicle, and consist of a biconvex lens and a meniscus. Half the lens is imbedded in the cavity of the retina and surrounded by the pigment, and the other half is turned toward a concavo-convex meniscus which corresponds in position with the cornea. The development of the meniscus and lens is unknown, but the retina is formed (fig. 8 V. a) as an outgrowth of the wall of the brain. At the inner ends of the cells of this outgrowth a deposit of pigment appears.
[8] For a fuller account of the organs of sense vide the chapters on the eye and ear.
The trunk section of the spinal cord (fig. 9, N) is separated by a sharp constriction from the brain. It is formed of a superficial layer of longitudinal nervous fibres, and a central core of ganglion cells. The layer of fibres diminishes in thickness towards the tail, and finally ceases to be visible. Kupffer detected three pairs of nerves passing off from the spinal cord to the muscles of the tail. The foremost of these arises at the boundary between the trunk and the tail, and the two others at regular intervals behind this point.
The mesoblast and muscular system. It has already been stated that the lateral walls of the archenteron in the tail give rise to muscular cells. These cells lie about three abreast, and appear not to increase in number; so that with the growth of the tail they grow enormously in length, and eventually become imperfectly striated. The mesoblast cells at the hinder end of the trunk, close to its junction with the tail, do not become converted into muscle cells, but give rise to blood corpuscles; and the axial remnant of the archenteron undergoes a similar fate. According to Kowalevsky the heart is formed during larval life as an elongated closed sack on the right side of the endostyle.
The notochord. The notochord was left as a rod formed of a single row of cells, or in As. canina and some other forms of two rows, extending from just within the border of the trunk to the end of the tail.
According to Kowalevsky, Kupffer, Giard, etc. the notochord undergoes a further development which finds its only complete parallel amongst Chordata in the doubtful case of Amphioxus.
There appear between the cells peculiar, highly refractive discs (fig. 8 V. Chs). These become larger and larger, and finally, after pushing the remnants of the cells with their nuclei to the sides, coalesce together to form a continuous axis of hyaline substance. The remnants of the cells with their nuclei form a sheath round the hyaline axis (fig. 8 VI. ch.). Whether the axis is to be regarded as formed of an intercellular substance, or of a differentiation of parts of the cells is still doubtful. Kupffer inclines to the latter view: the analogy of the notochord of higher types appears to me to tell in favour of the former one.
The alimentary tract. The anterior part of the primitive archenteron alone retains a lumen, and from this part the whole of the permanent alimentary tract (mesenteron) becomes developed. The anterior part of it grows upwards, and before hatching an involution of the epiblast on the dorsal side, just in front of the anterior extremity of the nervous system, meets and opens into this upgrowth, and gives rise to the permanent mouth (fig. 8 V. o).
Kowalevsky states that a pore is formed at the front end of the nervous tube leading into the mouth (fig. 8 V. and VI. f) which eventually gives rise to the ciliated sack, which lies in the adult at the junction between the mouth and the branchial sack. Kupffer however was unable to find this opening; but Kowalevsky's observations are confirmed by those of Salensky on Salpa.
From the hinder end of the alimentary sack an outgrowth directed dorsalwards makes its appearance (figs. 8 V. and 9, d), from which the oesophagus, stomach and intestine become developed. It at first ends blindly. The remainder of the primitive alimentary sack gives rise to the branchial sack of the adult. Just after the larva has become hatched, the outgrowth to form the stomach and oesophagus, etc. bends ventralwards and to the right, and then turns again in a dorsal and left direction till it comes close to the dorsal surface, somewhat to the left of and close to the hinder end of the trunk. The first ventral loop of this part gives rise to the oesophagus, which opens into the stomach; from this again the dorsally directed intestine passes off.
On the ventral wall of the branchial sack there is formed a narrow fold with thickened walls, which forms the endostyle. It ends anteriorly at the stomodæum and posteriorly at the point where the solid remnant of the archenteron in the tail was primitively continuous with the branchial sack. The whole of the alimentary wall is formed of a single layer of hypoblast cells.
A most important organ connected with the alimentary system still remains to be dealt with, viz. the atrial or peribranchial cavity. The first rudiments of it appear at about the time of hatching, in the form of a pair of dorsal epiblastic involutions (fig. 8 V. kl), at the level of the junction between the brain and the spinal cord. These involutions grow inwards, and meet corresponding outgrowths of the branchial sack, with which they fuse. At the junction between them is formed an elongated ciliated slit, leading from the branchial sack into the atrial cavity of each side. The slits so formed are the first pair of branchial clefts. Behind the first pair of branchial clefts a second pair is formed during larval life by a second outgrowth of the branchial sack meeting the epiblastic atrial involutions (fig. 8 VI. 1ks and 2ks). The intestine at first ends blindly close to the left atrial involution, but the anus becomes eventually formed by an opening being established between the left atrial involution and the intestine.
During the above described processes the test remains quite intact, and is not perforated at the oral or the atrial openings.
The retrogressive metamorphosis of the larva.
The development of the adult from the larva is, as has already been stated, in the main a retrogressive metamorphosis. The stages in this metamorphosis are diagrammatically shewn in figs. 10 and 11. It commences with the attachment of the larva (fig. 10 A) which takes place by one of the three papillæ. Simultaneously with the attachment the larval tail undergoes a complete atrophy (fig. 10 B), so that nothing is left of it but a mass of fatty cells situated close to the point of the previous insertion of the tail in the trunk.
FIG. 10. DIAGRAM SHEWING THE MODE OF ATTACHMENT AND SUBSEQUENT RETROGRESSIVE METAMORPHOSIS OF A LARVAL ASCIDIAN. (From Lankester.)
The nervous system also undergoes a very rapid retrogressive metamorphosis; and the only part of it which persists would seem to be the dilated portion of the spinal cord in the trunk (Kupffer, No. 28).
The three papillæ, including that serving for attachment, early disappear, and the larva becomes fixed by a growth of the test to foreign objects.
An opening appears in the test some time after the larva is fixed, leading into the mouth, which then becomes functional. The branchial sack at the same time undergoes important changes. In the larva it is provided with only two ciliated slits, which open into the, at this stage, paired atrial cavity (fig. 10).
The openings of the atrial cavity at first are shut off from communication with the exterior by the test, but not long after the larva becomes fixed, two perforations are formed in the test, which lead into the openings of the two atrial cavities. At the same time the atrial cavities dilate so as gradually to embrace the whole branchial sack to which their inner walls attach themselves. Shortly after this the branchial clefts rapidly increase in number[9].
[9] The account of the multiplication of the branchial clefts is taken from Krohn's paper on Phallusia mammillata (No. 24), but there is every reason to think that it holds true in the main for simple Ascidians.
The increase of the branchial clefts is somewhat complicated. Between the two primitive clefts two new ones appear, and then a third appears behind the last cleft. In the interval between each branchial cleft is placed a vascular branchial vessel (fig. 8 VI. bb). Soon a great number of clefts become added in a row on each side of the branchial sack. These clefts are small ciliated openings placed transversely with reference to the long axis of the branchial sack, but only occupying a small part of the breadth of each side. The intervals dorsal and ventral to them are soon filled by series of fresh rows of slits, separated from each other by longitudinal bars. Each side of the branchial sack becomes in this way perforated by a number of small openings arranged in rows, and separated by transverse and longitudinal bars. The whole structure forms the commencement of the branchial basketwork of the adult; the arrangement of which differs considerably in structure and origin from the simple system of branchial clefts of normal vertebrate types. At the junction of the transverse and longitudinal bars papillæ are formed projecting into the lumen of the branchial sack.
[FIG. 11. DIAGRAM OF A VERY YOUNG ASCIDIAN. (From Lankester.)]
After the above changes are far advanced towards completion, the openings of the two atrial sacks gradually approximate in the dorsal line, and finally coalesce to form the single atrial opening of the adult. The two atrial cavities at the same time coalesce dorsally to form a single cavity, which is continuous round the branchial sack, except along the ventral line where the endostyle is present. The atrial cavity, from its mode of origin as a pair of epiblastic involutions[10], is clearly a structure of the same nature as the branchial or atrial cavity of Amphioxus; and has nothing whatever to do with the true body cavity.
[10] In the asexually produced buds of Ascidians the atrial cavity appears, with the exception of the external opening, to be formed from the primitive branchial sack. In the buds of Pyrosoma however it arises independently. These peculiarities in the buds cannot weigh against the embryonic evidence that the atrial cavity arises from involutions of the epiblast, and they may perhaps be partially explained by the fact that in the formation of the visceral clefts outgrowths of the branchial sack meet the atrial involutions.
It has already been stated that the anus opens into the original left atrial cavity; when the two cavities coalesce the anus opens into the atrial cavity in the median dorsal line.
Two of the most obscure points in the development are the origin of the mesoblast in the trunk, and of the body cavity. Of the former subject we know next to nothing, though it seems that the cells resulting from the atrophy of the tail are employed in the nutrition of the mesoblastic structures of the trunk.
The body cavity in the adult is well developed in the region of the intestine, where it forms a wide cavity lined by an epithelioid mesoblastic layer. In the region of the branchial sack it is reduced to the vascular channels in the walls of the sack.
Kowalevsky believes the body cavity to be the original segmentation cavity, but this view can hardly be regarded as admissible in the present state of our knowledge. In some other Ascidian types a few more facts about the mesoblast will be alluded to.
With the above changes the retrogressive metamorphosis is completed; and it only remains to notice the change in position undergone in the attainment of the adult state. The region by which the larva is attached grows into a long process (fig. 10 B), and at the same time the part carrying the mouth is bent upwards so as to be removed nearly as far as possible from the point of attachment. By this means the condition in the adult (fig. 11) is gradually brought about; the original dorsal surface with the oral and atrial openings becoming the termination of the long axis of the body, and the nervous system being placed between the two openings.
The genus Molgula presents a remarkable exception amongst the simple Ascidians in that, in some if not all the species belonging to it, development takes place (Lacaze Duthiers 29 and 30, Kupffer 28) quite directly and without larval metamorphosis.
The ova are laid either singly or adhering together, and are very opaque. The segmentation (Lacaze Duthiers) commences by the formation of four equal spheres, after which a number of small clear spheres are formed which envelope the large spheres. The latter give rise to a closed enteric sack, and probably also to a mass of cells situated on the ventral side, which appear to be mesoblastic. The epiblast is constituted of a single layer of cells which completely envelopes the enteric sack and the mesoblast.
While the ovum is still within the chorion five peculiar processes of epiblast grow out; four of which usually lie in the same sectional plane of the embryo. They are contractile and contain prolongations of the body cavity. Their relative size is very variable.
The nervous system is formed on the dorsal side of the embryo before the above projections make their appearance, but, though it seems probable that it originates in the same manner as in the more normal forms, its development has not been worked out. As soon as it is formed it consists of a nervous ganglion similar to that usually found in the adult. The history of the mass of mesoblast cells has been inadequately followed, but it continuously disappears as the heart, excretory organs, muscles, etc. become formed. So far as can be determined from Kupffer's descriptions the body cavity is primitively parenchymatous--an indication of an abbreviated development--and does not arise as a definite split in the mesoblast.
The primitive enteric cavity becomes converted into the branchial sack, and from its dorsal and posterior corner the oesophagus, stomach and intestine grow out as in the normal forms. The mouth is formed by the invagination of a disc-like thickening of the epidermis in front of the nervous system on the dorsal side of the body; and the atrial cavity arises behind the nervous system by a similar process at a slightly later period. The gill clefts opening into the atrial cavity are formed as in the type of simple Ascidians described by Krohn.
The embryo becomes hatched not long after the formation of the oral and atrial openings, and the five epiblastic processes undergo atrophy. They are not employed in the attachment of the adult.
The larva when hatched agrees in most important points with the adult; and is without the characteristic provisional larval organs of ordinary forms; neither organs of special sense nor a tail becoming developed. It has been suggested by Kupffer that the ventrally situated mesoblastic mass is the same structure as the mass of elements which results in ordinary types from the degeneration of the tail. If this suggestion is true it is difficult to believe that this mass has any other than a nutritive function.
The larva of Ascidia ampulloides described by P. van Beneden is regarded by Kupffer as intermediate between the Molgula larva and the normal type, in that the larval tail and notochord and a pigment spot are first developed, while after the atrophy of these organs peculiar processes like those of Molgula make their appearance.
Sedentaria. The development of the fixed composite Ascidians is, so far as we know, in the main similar to that of the simple Ascidians. The larvæ of Botryllus sometimes attain, while still in the free state, a higher stage of development with reference to the number of gill slits, etc. than that reached by the simple Ascidians, and in some instances (Botryllus auratus Metschnikoff) eight conical processes are found springing in a ring-like fashion around the trunk. The presence of these processes has led to somewhat remarkable views about the morphology of the group; in that they were regarded by Kölliker, Sars, etc. as separate individuals, and it was supposed that the product of each ovum was not a single individual, but a whole system of individuals with a common cloaca.
The researches of Metschnikoff (No. 32), Krohn (No. 25), and Giard (No. 12), etc. demonstrate that this paradoxical view is untenable, and that each ovum only gives rise to a single embryo, while the stellate systems are subsequently formed by budding.
Natantia. Our knowledge of the development of Pyrosoma is mainly due to Huxley (No. 16) and Kowalevsky (No. 22). In each individual of a colony of Pyrosoma only a single egg comes to maturity at one time. This egg is contained in a capsule formed of a structureless wall lined by a flattened epithelioid layer. From this capsule a duct passes to the atrial cavity, which, though called the oviduct, functions as an afferent duct for the spermatozoa.
The segmentation is meroblastic, and the germinal disc adjoins the opening of the oviduct. The segmentation is very similar to that which occurs in Teleostei, and at its close the germinal disc has the form of a cap of cells, without a trace of stratification or of a segmentation cavity, resting upon the surface of the yolk, which forms the main mass of the ovum.
After segmentation the blastoderm, as we may call the layer of cells derived from the germinal disc, rapidly spreads over the surface of the yolk, and becomes divided into two layers, the epiblast and the hypoblast. At the same time it exhibits a distinction into a central clearer and a peripheral more opaque region. At one end of the blastoderm, which for convenience sake may be spoken of as the posterior end, a disc of epiblast appears, which is the first rudiment of the nervous system, and on each side of the middle of the blastoderm there arises an epiblastic involution. The epiblastic involutions give rise to the atrial cavity.
These involutions rapidly grow in length, and soon form longish tubes, opening at the surface by pores situated not far from the posterior end of the blastoderm.
The blastoderm at this stage, as seen on the surface of the yolk, is shewn in fig. 12 A. It is somewhat broader than long. The nervous system is shewn at n, and at points to an atrial tube. A transverse section, through about the middle of this blastoderm, is represented in fig. 12 B. The epiblast is seen above. On each side is the section of an atrial tube (at). Below is the hypoblast which is separated from the yolk especially in the middle line; at each side it is beginning to grow in below, on the surface of the yolk. The space below the hypoblast is the alimentary cavity, the ventral wall of which is formed by the cells growing in at the sides. Between the epiblast and hypoblast are placed scattered mesoblast cells, the origin of which has not been clearly made out.
[FIG. 12.
A. SURFACE VIEW OF THE OVUM OF PYROSOMA NOT FAR ADVANCED IN DEVELOPMENT. The embryonic structures are developed from a disc-like blastoderm. B. TRANSVERSE SECTION THROUGH THE MIDDLE PART OF THE SAME BLASTODERM.
at. atrial cavity; hy. hypoblast; n. nervous disc in the region of the future Cyathozooid.]
In a later stage the openings of the two atrial tubes gradually travel backwards, and at the same time approximate, till finally they meet and coalesce at the posterior end of the blastoderm behind the nervous disc (fig. 13, cl). The tubes themselves at the same time become slightly constricted not far from their hinder extremities, and so divided into a posterior region nearly coterminous with the nervous system (fig. 13), and an anterior region. These two regions have very different histories in the subsequent development.
The nervous disc has during these changes become marked by a median furrow (fig. 13, ng), which is soon converted into a canal by the same process as in the simple Ascidians. The closure of the groove commences posteriorly and travels forwards. These processes are clearly of the same nature as those which take place in Chordata generally in the formation of the central nervous system.
In the region of the germinal disc which contains the anterior part of the atrial tubes, the alimentary cavity becomes, by the growth of the layer of cells described in the last stage, a complete canal, on the outer wall of which the endostyle is formed as a median fold. The whole anterior part of the blastoderm becomes at the same time gradually constricted off from the yolk.
[FIG. 13. BLASTODERM OF PYROSOMA SHORTLY BEFORE ITS DIVISION INTO CYATHOZOOID AND ASCIDIOZOOIDS. (After Kowalevsky.)
cl. cloacal (atrial) opening; en. endostyle; at. atrial cavity; ng. nervous groove.
The heart and pericardial cavity are seen to the left.]
The fate of the anterior and posterior parts of the blastoderm is very different. The anterior part becomes segmented into four zooids or individuals, called by Huxley Ascidiozooids, which give rise to a fresh colony of Pyrosoma. The posterior part forms a rudimentary zooid, called by Huxley Cyathozooid, which eventually atrophies. These five zooids are formed by a process of embryonic fission. This fission commences by the appearance of four transverse constrictions in the anterior part of the blastoderm; by which the whole blastoderm becomes imperfectly divided into five regions, fig. 14 A.
The hindermost constriction (uppermost in my figure) lies just in front of the pericardial cavity; and separates the Cyathozooid from the four ascidiozooids. The three other constrictions mark off the four Ascidiozooids. The Cyathozooid remains for its whole length attached to the blastoderm, which has now nearly enveloped the yolk. It contains the whole of the nervous system (ng), which is covered behind by the opening of the atrial tubes (cl). The alimentary tract in the Cyathozooid forms a tube with very delicate walls. The pericardial cavity is completely contained within the Cyathozooid, and the heart itself (ht) has become formed by an involution of the walls of the cavity.
The Ascidiozooids are now completely separated from the yolk. They have individually the same structure as the undivided rudiment from which they originated; so that the organs they possess are simply two atrial tubes, an alimentary tract with an endostyle, and undifferentiated mesoblast cells.
In the following stages the Ascidiozooids grow with great rapidity. They soon cease to lie in a straight line, and eventually form a ring round the Cyathozooid and attached yolk sack.
While these changes are being accomplished in the external form of the colony, both the Cyathozooids and the Ascidiozooids progress considerably in development. In the Cyathozooid the atrial spaces gradually atrophy, with the exception of the external opening, which becomes larger and more conspicuous. The heart at the same time comes into full activity and drives the blood through the whole colony. The yolk becomes more and more enveloped by the Cyathozooid, and is rapidly absorbed; while the nutriment derived from it is transported to the Ascidiozooids by means of the vascular connection. The nervous system retains its previous condition; and round the Cyathozooid is formed the test into which cells migrate, and arrange themselves in very conspicuous hexagonal areas. The delicate alimentary tract of the Cyathozooid is still continuous with that of the first Ascidiozooid. After the Cyathozooid has reached the development just described it commences to atrophy.
[FIG. 14. TWO STAGES IN THE DEVELOPMENT OF PYROSOMA IN WHICH THE CYATHOZOOID AND FOUR ASCIDIOZOOIDS ARE ALREADY DISTINCTLY FORMED. (After Kowalevsky.)
cy. cyathozooid; as. ascidiozooid; ng. nervous groove; ht. heart of cyathozooid; cl. cloacal opening.]
The changes in the Ascidiozooids are even more considerable than those in the Cyathozooid. A nervous system appears as a fresh formation close to the end of each Ascidiozooid turned towards the Cyathozooid. It forms a tube of which the open front end eventually develops into the ciliated pit of the mouth, and the remainder into the actual nervous ganglion. Between the nervous system and the endostyle an involution appears, which gives rise to the mouth. On each side of the primitive alimentary cavity of each Ascidiozooid branchial slits make their appearance, leading into the atrial tubes; so that the primitive alimentary tract becomes converted into the branchial sacks of the Ascidiozooids. The remainder of the alimentary tract of each zooid is formed as a bud from the hind end of the branchial sack in the usual way. The alimentary tracts of the four Ascidiozooids are at first in free communication by tubes opening from the hinder extremity of one zooid into the dorsal side of the branchial sack of the next zooid. At the hinder end of each Ascidiozooid is developed a mass of fatty cells known as the elæoblast, which probably represents a rudiment of the larval tail of simple Ascidians. (Cf. pp. 30-32.)
The further changes consist in the gradual atrophy of the Cyathozooid, which becomes more and more enclosed within the four Ascidiozooids. These latter become completely enveloped in a common test, and form a ring round the remains of the yolk and of the Cyathozooid, the heart of which continues however to beat vigorously. The cloacal opening of the Cyathozooid persists through all these changes, and, after the Cyathozooid itself has become completely enveloped in the Ascidiozooids and finally absorbed, deepens to form the common cloacal cavity of the Pyrosoma colony.
The main parts of the Ascidiozooids were already formed during the last stage. The zooids long remain connected together, and united by a vascular tube with the Cyathozooid, and these connections are not severed till the latter completely atrophies. Finally, after the absorption of the Cyathozooid, the Ascidiozooids form a rudimentary colony of four individuals enveloped in a common test. The two atrial tubes of each zooid remain separate in front but unite posteriorly. An anus is formed leading from the rectum into the common posterior part of the atrial cavity; and an opening is established between the posterior end of the atrial cavity of each Ascidiozooid and the common axial cloacal cavity of the whole colony. The atrial cavities in Pyrosoma are clearly lined by epiblast, just as in simple Ascidians.
When the young colony is ready to become free, it escapes from the atrial cavity of the parent, and increases in size by budding.
Doliolidæ. The sexually developed embryos of Doliolum have been observed by Krohn (No. 23), Gegenbaur (No. 10), and Keferstein and Ehlers (No. 17); but the details of the development have been very imperfectly investigated.
The youngest embryo observed was enveloped in a large oval transparent covering, the exact nature of which is not clear. It is perhaps a larval rudiment of the test which would seem to be absent in the adult. Within this covering is the larva, the main organs of which are already developed; and which primarily differs from the adult in the possession of a larval tail similar to that of simple Ascidians.
In the body both oral and atrial openings are present, the latter on the dorsal surface; and the alimentary tract is fully established. The endostyle is already formed on the ventral wall of the branchial sack, but the branchial slits are not present. Nine muscular rings are already visible. The tail, though not so developed as in the simple Ascidians, contains an axial notochord of the usual structure, and lateral muscles. It is inserted on the ventral side, and by its slow movements the larva progresses.
In succeeding stages the tail gradually atrophies, and the gill slits, four in number, develop; at the same time a process or stolon, destined to give rise by budding to a second non-sexual generation, makes its appearance on the dorsal side in the seventh intermuscular space. This stolon is comparable with that which appears in the embryo of Salpa. When the tail completely atrophies the larva leaves its transparent covering, and becomes an asexual Doliolum with a dorsal stolon.
Salpidæ. As is well known the chains of Salpa alone are sexual, and from each individual of the chain only a single embryo is produced. The ovum from which this embryo takes its origin is visible long before the separate Salps of the chain have become completely developed. It is enveloped in a capsule continuous with a duct, which opens into the atrial cavity, and is usually spoken of as the oviduct. The capsule with the ovum is enveloped in a maternal blood sinus. Embryonic development commences after the chain has become broken up, and the spermatozoa derived from another individual would seem to be introduced to the ovum through the oviduct.
At the commencement of embryonic development the oviduct and ovicapsule undergo peculiar changes; and in part at least give rise to a structure subservient to the nutrition of the embryo, known as the placenta. These changes commence with the shortening of the oviduct, and the disappearance of a distinction between oviduct and ovicapsule. The cells lining the innermost end of the capsule, i.e. that at the side of the ovum turned away from the atrial cavity, become at the same time very columnar. The part of the oviduct between the ovum and the atrial cavity dilates into a sack, communicating on the one hand with the atrial cavity, and on the other by a very narrow opening with the chamber in which the egg is contained. This sack next becomes a prominence in the atrial cavity, and eventually constitutes a brood-pouch. The prominence it forms is covered by the lining of the atrial cavity, immediately within which is the true wall of the sack. The external opening of the sack becomes gradually narrowed, and finally disappears. In the meantime the chamber in which the embryo is at first placed acquires a larger and larger opening into the sack; till finally the two chambers unite, and a single brood-pouch containing the embryo is thus produced. The inner wall of the chamber is formed by the columnar cells already spoken of. They form the rudiment of the placenta. The double wall of the outer part of the brood-pouch becomes stretched by the growth of the embryo; the inner of its two layers then atrophies. The outer layer subsequently gives way, and becomes rolled back so as to lie at the inner end of the embryo, leaving the latter projecting freely into the atrial cavity.
While these changes are taking place the placenta becomes fully developed. The first rudiment of it consists, according to Salensky, of the thickened cells of the ovicapsule only, though this view is dissented from by Brooks, Todaro, etc. Its cells soon divide to form a largish mass, which becomes attached to a part of the epiblast of the embryo.
On the formation of the body cavity of the embryo a central axial portion of the placenta becomes separated from a peripheral layer; and a channel is left between them which leads from a maternal blood sinus into the embryonic body cavity. The peripheral layer of the placenta is formed of cells continuous with the epiblast of the embryo; while the axial portion is constituted of a disc of cells adjoining the embryo, with a column of fibres attached to the maternal side. The fibres of this column are believed by Salensky to be products of the original rudiment of the placenta. The placenta now assumes a more spherical form, and its cavity becomes shut off from the embryonic body cavity. The fibrous column breaks up into a number of strands perforating the lumen of the organ, and the cells of the wall become stalked bodies projecting into the lumen.
When the larva is nearly ready to become free the placenta atrophies.
The placenta functions in the nutrition of the embryo in the following way. It projects from its first formation into a maternal blood sinus, and, on the appearance of a cavity in it continuous with the body cavity of the embryo, the blood of the mother fully intermingles with that of the embryo. At a later period the communication with the body cavity of the embryo is shut off, but the cavity of the placenta is supplied with a continuous stream of maternal blood, which is only separated from the foetal blood by a thin partition.
It is now necessary to turn to the embryonic development about which it is unfortunately not as yet possible to give a completely satisfactory account. The statements of the different investigators contradict each other on most fundamental points. I have followed in the main Salensky (No. 34), but have also called attention to some points where his observations diverge most from those of other writers, or where they seem unsatisfactory.
The development commences at about the period when the brood-pouch is becoming formed; and the ovum passes entirely into the brood-pouch before the segmentation is completed. The segmentation is regular, and the existence of a segmentation cavity is denied by Salensky, though affirmed by Kowalevsky and Todaro[11].
[11] From Todaro's latest paper (No. 39) it would seem the segmentation cavity has very peculiar relations.
At a certain stage in the segmentation the cells of the ovum become divided into two layers, an epiblast investing the whole of the ovum with the exception of a small area adjoining the placenta, where the inner layer or hypoblast, which forms the main mass of the ovum, projects at the surface. The epiblast soon covers the whole of the hypoblast, so that there would seem (according to Salensky's observations) to be a kind of epibolic invagination: a conclusion supported by Todaro's figures.
At a later stage, on one side of the free apex of the embryo, a mesoblastic layer makes its appearance between the epiblast and hypoblast. This layer is derived by Salensky, as it appears to me on insufficient grounds, from the epiblast. Nearly at the same time there arises not far from the same point of the embryo, but on the opposite side, a solid thickening of epiblast which forms the rudiment of the nervous system. The nervous system is placed close to the front end of the body; and nearly at the opposite pole, and therefore at the hind end, there appears immediately below the epiblast a mass of cells forming a provisional organ known as the elæoblast. Todaro regards this organ as mesoblastic in origin, and Salensky as hypoblastic. The organ is situated in the position which would be occupied by the larval tail were it developed. It may probably be regarded (Salensky) as a disappearing rudiment of the tail, and be compared in this respect with the more or less similar mass of cells described by Kupffer in Molgula, and with the elæoblast in Pyrosoma.
After the differentiation of these organs a cavity makes its appearance between the epiblast and hypoblast, which is regarded by Salensky as the body cavity. It appears to be equivalent to the segmentation cavity of Todaro. According to Todaro's statements, it is replaced by a second cavity, which appears between the splanchnic and somatic layers of mesoblast, and constitutes the true body cavity. The embryo now begins to elongate, and at the same time a cavity makes its appearance in the centre of the hypoblast cells. This cavity is the rudiment of the branchial and alimentary cavities: on its dorsal wall is a median projection, the rudiment of the so-called gill of Salpa.
At two points this cavity comes into close contact with the external skin. At one of these, situated immediately ventral to the nervous system, the mouth becomes formed at a later period. At the other, placed on the dorsal surface between the nervous system and the elæoblast, is formed the cloacal aperture.
By the stage under consideration the more important systems of organs are established, and the remaining embryonic history may be very briefly narrated.
The embryo at this stage is no longer covered by the walls of the brood-pouch but projects freely into the atrial cavity, and is only attached to its parent by means of the placenta. The epiblast cells soon give rise to a deposit which forms the mantle. The deposit appears however to be formed not only on the outer side of the epiblast but also on the inner side; so that the epiblast becomes cemented to the subjacent parts, branchial sack, etc., by an intercellular layer, which would seem to fill up the primitive body cavity with the exception of the vascular channels (Salensky).
The nervous system, after its separation from the epiblast, acquires a central cavity, and subsequently becomes divided into three lobes, each with an internal protuberance. At its anterior extremity it opens into the branchial sack; and from this part is developed the ciliated pit of the adult. The nervous ganglion at a later period becomes solid, and a median eye is subsequently formed as an outgrowth from it.
According to Todaro there are further formed two small auditory (? olfactory) sacks on the ventral surface of the brain, each of them placed in communication with the branchial cavity by a narrow canal.
The mesoblast gives rise to the muscles of the branchial sack, to the heart, and to the pericardium. The two latter are situated on the ventral side of the posterior extremity of the branchial cavity.
Branchial sack and alimentary tract. The first development of the enteric cavity has already been described. The true alimentary tract is formed as a bud from the hinder end of the primitive cavity. The remainder of the primitive cavity gives rise to the branchial sack. The so-called gill has at first the form of a lamella attached dorsally to the walls of the branchial sack; but its attachment becomes severed except at the two ends, and it then forms a band stretching obliquely across the branchial cavity, which subsequently becomes hollow and filled with blood corpuscles. The whole structure is probably homologous with the peculiar fold, usually prolonged into numerous processes, which normally projects from the dorsal wall of the Ascidian branchial sack.
On the completion of the gill the branchial sack becomes divided into a region dorsal to the gill, and a region ventral to it. Into the former the single atrial invagination opens. No gill slits are formed comparable with those in simple Ascidians, and the only representative of these structures is the simple communication which becomes established between the dorsal division of the branchial sack and the atrial opening. The whole branchial sack of Salpa, including both the dorsal and ventral divisions, corresponds with the branchial sack of simple Ascidians. On its ventral side the endostyle is formed in the normal way. The mouth arises at the point already indicated near the front end of the nervous system[12].
[12] Brooks takes a very different view of the nature of the parts in Salpa. He says, No. 7, p. 322, "The atrium of Salpa, when first observed, was composed of two broad lateral atria within the body cavity, one on each side of the branchial sack, and a very small mid-atrium.... The lateral atria do not however, as in most Tunicata, remain connected with the mid-atrium, and unite with the wall of the branchial sack to form the branchial slits, but soon become entirely separated, and the two walls of each unite so as to form a broad sheet of tissue, which soon splits up to form the muscular bands of the branchial sack." Again, p. 324, "During the changes which have been described as taking place in the lateral atria, the mid-atrium has increased in size.... The branchial and atrial tunics now unite upon each side, so that the sinus is converted into a tube which communicates, at its posterior end, with the heart and perivisceral sinus, and at the anterior end with the neural sinus. This tube is the gill.... The centres of the two regions upon the sides of the gill, where these two tissues have become united, are now absorbed, so that a single long and narrow branchial slit is produced on each side of the gill. The branchial cavity is thus thrown into communication with the atrium, and the upper surface of the latter now unites with the outer tunic, and the external atrial opening is formed by absorption."
The above description would imply that the atrial cavity is a space lined by mesoblast, a view which would upset the whole morphology of the Ascidians. Salensky's account, which implies only an immense reduction in the size of the atrial cavity as compared with other types, appears to me far more probable. The lateral atria of Brooks appear to be simply parts of the body cavity, and have certainly no connection with the lateral atria of simple Ascidians or Pyrosoma.
The observations of Todaro upon Salpa (No. 38) are very remarkable, and illustrated by beautifully engraved plates. His interpretations do not however appear quite satisfactory. The following is a brief statement of some of his results.
During segmentation there arises a layer of small superficial cells (epiblast) and a central layer of larger cells, which becomes separated from the former by a segmentation cavity, except at the pole adjoining the free end of the brood-pouch. At this point the epiblast cells become invaginated into the central cells and form the alimentary tract, while the primitive central cells remain as the mesoblast. A fold arises from the epiblast which Todaro compares to the vertebrate amnion, but the origin of it is unfortunately not satisfactorily described. The folds of the amnion project towards the placenta, and enclose a cavity which, as the folds never completely meet, is permanently open to the maternal blood sinus. This cavity corresponds with the cavity of the true amnion of higher Vertebrates. It forms the cavity of the placenta already described. Between the two folds of the amnion is a cavity corresponding with the vertebrate false amnion. A structure regarded by Todaro as the notochord is formed on the neck, connecting the involution of the alimentary tract with the exterior. It has only a very transitory existence.
In the later stages the segmentation cavity disappears and a true body cavity is formed by a split in the mesoblast.
Todaro's interpretations, and in part his descriptions also, both with reference to the notochord and amnion, appear to me quite inadmissible. About some other parts of his descriptions it is not possible to form a satisfactory judgment. He has recently published a short paper on this subject (No. 39) preliminary to a larger memoir, which is very difficult to understand in the absence of plates. He finds however in the placenta various parts which he regards as homologous with the decidua vera and reflexa of Mammalia.
Development of the chain of sexual Salps. My description of the embryonic development of Salpa would not be complete without some reference to the development of the stolon of the Solitary generation of Salps by the segmentation of which a chain of sexual Salps originates.
The asexual Salp, the embryonic development of which has just been described, may be compared to the Cyathozooid of Pyrosoma, from which it mainly differs in being fully developed. While still in an embryonic condition it gives rise to a process or stolon, which becomes divided into a number of zooids by transverse constrictions, in the same manner that part of the germ of the ovum of Pyrosoma is divided by transverse constrictions into four Ascidiozooids.
The stolon arises as a projection on the right side of the body of the embryo close to the heart. It is formed (Salensky, No. 35) of an outgrowth of the body wall, into which there grow the following structures:
(1) A central hollow process from the end of the respiratory sack. (2) A right and left lateral prolongation of the pericardial cavity. (3) A solid process of cells on the ventral side derived from the same mass of the cells as the elæoblast. (4) A ventral and a dorsal blood sinus.
Besides these parts there appears on the dorsal side a hollow tube, the origin of which is unknown, which gives rise to the nervous system.
The hollow process of the respiratory sack is purely provisional, and disappears without giving rise to any permanent structure. The right and left prolongations of the pericardial cavity become solid and eventually give origin to the mesoblast. The ventral process of cells is the most important structure in the stolon in that it gives rise both to the alimentary and respiratory sacks, and to the generative organs of the sexual Salps. The stolon containing the organs just enumerated becomes divided by transverse constrictions into a number of rings. These rings do not long remain complete, but become interrupted dorsally and ventrally. The imperfect rings so formed soon overlap, and each of them eventually gives rise to a sexual Salp. Although the stolon arises while the asexual Salp is still in an embryonic condition, it does not become fully developed till long after the asexual Salp has attained maturity.
Appendicularia. Our only knowledge of the development of Appendicularia is derived from Fol's memoir on the group (No. 8). He simply states that it develops, as far as he was able to follow, like other Ascidians; and that the extremely minute size of the egg prevented him from pursuing the subject. He also states that the pair of pores leading from the branchial cavity to the exterior is developed from epiblastic involutions meeting outgrowths of the wall of the branchial sack.
Metagenesis.
One of the most remarkable phenomena in connection with the life history of many Ascidians is the occurrence of an alternation of sexual and gemmiparous generations. This alternation appears to have originated from a complication of the process of reproduction by budding, which is so common in this group. The mode in which this very probably took place will be best understood by tracing a series of transitional cases between simple budding and complete alternations of generations.
In the simpler cases, which occur in some Composita Sedentaria, the process of budding commences with an outgrowth of the body wall into the common test, containing a prolongation of part of the alimentary tract[13].
[13] It is not within the scope of this work to enter into details with reference to the process of budding. The reader is referred on this head more especially to the papers of Huxley (No. 16) and Kowalevsky (No. 22) on Pyrosoma, of Salensky (No. 35) on Salpa, and Kowalevsky (No. 21) on Ascidians generally. It is a question of very great interest how budding first arose, and then became so prevalent in these degenerate types of Chordata. It is possible to suppose that budding may have commenced by the division of embryos at an early stage of development, and have gradually been carried onwards by the help of natural selection till late in life. There is perhaps little in the form of budding of the Ascidians to support this view--the early budding of Didemnum as described by Gegenbaur being the strongest evidence for it--but it fits in very well with the division of the embryo in Lumbricus trapezoides described by Kleinenberg, and with the not unfrequent occurrence of double monsters in Vertebrata which may be regarded as a phenomenon of a similar nature (Rauber). The embryonic budding of Pyrosoma, which might perhaps be viewed as supporting the hypothesis, appears to me not really in favour of it; since the Cyathozooid of Pyrosoma is without doubt an extremely modified form of zooid, which has obviously been specially developed in connection with the peculiar reproduction of the Pyrosomidæ.
Between the epiblastic and hypoblastic layers of the bud so formed, a mesoblastic and sometimes a generative outgrowth of the parent also appears.
The systems of organs of the bud are developed from the corresponding layers to those in the embryo[14]. The bud eventually becomes detached, and in its turn gives rise to fresh buds. Both the bud and its parent reproduce sexually as well as by budding: the new colonies being derived from sexually produced embryos.
[14] The atrial spaces form somewhat doubtful exceptions to the rule.
The next stage of complication is that found in Botryllus (Krohn, Nos. 25 and 26). The larva produced sexually gives rise to a bud from the right side of the body close to the heart. On the bud becoming detached the parent dies away without developing sexual organs. The bud of the second generation gives rise to two buds, a right one and a left one, and like the larva dies without reaching sexual maturity. The buds of the third generation each produce two buds and then suffer the same fate as their parent.
The buds of the third generation arrange themselves with their cloacal extremities in contact, and in the fourth generation a common cloaca is formed, and so a true radial system of zooids is established; the zooids of which are not however sexual.
The buds of the fourth generation in their turn produce two or three buds and then die away.
Fresh systems become formed by a continuation of the process of budding, but the zooids of the secondary systems so formed are sexual. The ova come to maturity before the spermatozoa, so that cross fertilization takes place.
In Botryllus we have clearly a rudimentary form of alternations of generations, in that the sexually produced larva is asexual, and, after a series of asexual generations, produced gemmiparously, there appear sexual generations, which however continue to reproduce themselves by budding.
The type of alternations of generations observable in Botryllus becomes, as pointed out by Huxley, still more marked in Pyrosoma.
The true product of the ovum is here (vide p. 25) a rudimentary individual called by Huxley the Cyathozooid. This gives rise, while still an embryo, by a process equivalent to budding to four fully developed zooids (Ascidiozooids) similar to the parent form, and itself dies away. The four Ascidiozooids form a fresh colony, and reproduce (1) sexually, whereby fresh colonies are formed, and (2) by ordinary budding, whereby the size of the colony is increased. All the individuals of the colony are sexual.
The alternation of generations in Pyrosoma widely differs from that in Botryllus in the fact of the Cyathozooid differing so markedly in its anatomical characters from the ordinary zooids.
In Salpa the process is slightly different[15]. The sexual forms are now incapable of budding, and, although at first a series of sexual individuals are united together in the form of a chain, so as to form a colony like Pyrosoma or Botryllus, yet they are so loosely connected that they separate in the adult state. As in Botryllus, the ova are ripe before the spermatozoa. Each sexual individual gives rise to a single offspring, which, while still in the embryonic condition, buds out a 'stolon' from its right ventral side. This stolon is divided into a series of lateral buds after the solitary asexual Salp has begun to lead an independent existence. The solitary asexual Salp clearly corresponds with the Cyathozooid of Pyrosoma, though it has not, like the Cyathozooid, undergone a retrogressive metamorphosis.
[15] Vide p. 33.
By far the most complicated form of alternation of generations known amongst the Ascidians is that in Doliolum. The discovery of this metamorphosis was made by Gegenbaur (No. 10). The sexual form of Doliolum is somewhat cask-shaped, with ring-like muscular bands, and the oral and atrial apertures placed at opposite ends of the cask. The number of gill slits varies according to the species. The ovum gives rise, as already described, to a tailed embryo which subsequently develops into a cask-shaped asexual form. On attaining its full size it loses its branchial sack and alimentary tract. While still in the embryonic condition, a stolon grows out from its dorsal side in the seventh intermuscular space. The stolon, like that in Salpa, contains a prolongation of the branchial sack[16].
[16] I draw this conclusion from Gegenbaur's fig. (No. 10), Pl. XVI., fig. 15. The body (x) in the figure appears to me without doubt the rudiment of the stolon, and not, as believed by Gegenbaur, the larval tail.
On this stolon there develop two entirely different types of buds, (1) lateral buds, (2) dorsal median buds.
The lateral buds are developed in regular order on the two sides of the stolon, and the most advanced buds are those furthest removed from the base. They give rise to forms with a very different organization to that of the parent. They are compared by Gegenbaur to a spoon, the bowl of which is formed by the branchial sack, and the handle by the stalk attaching the bud to the stolon. The oral opening into the branchial sack is directed upwards: an atrial opening is remarkably enough not present. The branchial sack is perforated by numerous openings. It leads into an alimentary tract which opens directly to the exterior by an anus opposite the mouth.
The stalks attaching the more mature buds to the stolon are provided with ventrally directed scales, which completely hide the stolon in a view from the ventral surface.
These buds have, even after their detachment, no trace of generative organs, and shew no signs of reproducing themselves by budding. Their eventual fate is unknown.
The median dorsal buds have no such regular arrangement as the lateral buds, but arise in irregular bunches, those furthest removed from the base of the stolon being however the oldest. These buds are almost exactly similar to the original sexual form; they do not acquire sexual organs, but are provided with a stolon attached on the ventral side, in the sixth intermuscular space.
This stolon is simply the stalk by which each median bud was primitively attached to the stolon of the first asexual form.
From the stolon of the median buds of the second generation buds are developed which grow into the sexual forms.
The generations of Doliolum may be tabulated in the following way.
Sexual generation, | 1st asexual form with dorsal stolon, _________________|_____________________ | | spoon-like forms developed as 2nd asexual forms developed as lateral buds (eventual history median buds with ventral stolon, unknown). | sexual generation.
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(9) Ganin. "Neue Thatsachen a. d. Entwicklungsgeschichte d. Ascidien." Zeit. f. wiss. Zool., Vol. XX. 1870.
(10) C. Gegenbaur. "Ueber den Entwicklungscyclus von Doliolum nebst Bemerkungen über die Larven dieser Thiere." Zeit. f. wiss. Zool., Bd. VII. 1856.
(11) A. Giard. "Etudes critiques des travaux d'embryogénie relatifs à la parenté des Vertebrés et des Tuniciers." Archiv Zool. expériment., Vol. I. 1872.
(12) A. Giard. "Recherches sur les Synascidies." Archiv Zool. expér., Vol. I. 1872.
(13) O. Hertwig. "Untersuchungen üb. d. Bau u. d. Entwicklung des Cellulose-Mantels d. Tunicaten." Jenaische Zeitschrift, Bd. VII. 1873.
(14) Th. H. Huxley. "Remarks upon Appendicularia and Doliolum." Phil. Trans., 1851.
(15) Th. H. Huxley. "Observations on the anatomy and physiology of Salpa and Pyrosoma." Phil. Trans., 1851.
(16) Th. H. Huxley. "Anatomy and development of Pyrosoma." Linnean Trans., 1860, Vol. XXIII.
(17) Keferstein u. Ehlers. Zoologische Beiträge, 1861. Doliolum.
(18) A. Kowalevsky. "Entwicklungsgeschichte d. einfachen Ascidien." Mém. Acad. Pétersbourg, VII. série, T. X. 1866.
(19) A. Kowalevsky. "Beitrag z. Entwick. d. Tunicaten." Nachrichten d. königl. Gesell. zu Göttingen. 1868.
(20) A. Kowalevsky. "Weitere Studien üb. d. Entwicklung d. einfachen Ascidien." Archiv f. mikr. Anat., Vol. VII. 1871.
(21) A. Kowalevsky. "Ueber Knospung d. Ascidien." Archiv f. mikr. Anat., Vol. X. 1874.
(22) A. Kowalevsky. "Ueber die Entwicklungsgeschichte d. Pyrosoma." Archiv f. mikr. Anat., Vol. XI. 1875.
(23) A. Krohn. "Ueber die Gattung Doliolum u. ihre Arten." Archiv f. Naturgeschichte, Bd. XVIII. 1852.
(24) A. Krohn. "Ueber die Entwicklung d. Ascidien." Müller's Archiv, 1852.
(25) A. Krohn. "Ueber die Fortpflanzungsverhältnisse d. Botrylliden." Archiv f. Naturgeschichte, Vol. XXXV. 1869.
(26) A. Krohn. "Ueber die früheste Bildung d. Botryllenstöcke." Archiv f. Naturgeschichte, Vol. XXXV. 1869.
(27) C. Kupffer. "Die Stammverwandschaft zwischen Ascidien u. Wirbelthieren." Archiv f. mikr. Anat., Vol. VI. 1870.
(28) C. Kupffer. "Zur Entwicklung d. einfachen Ascidien." Archiv f. mikr. Anat., Vol. VIII. 1872.
(29) H. Lacaze Duthiers. "Recherches sur l'organisation et l'Embryogénie des Ascidies (Molgula tubulosa)." Comptes rendus, May 30, 1870, p. 1154.
(30) H. Lacaze Duthiers. "Les Ascidies simples des Côtes de France" (Development of Molgula). Archiv Zool. expér., Vol. III. 1874.
(31) R. Leuckart. "Salpa u. Verwandte." Zoologische Untersuchungen, Heft II.
(32) E. Metschnikoff. "Observations sur le développement de quelques animaux (Botryllus and Simple Ascidians)." Bull. d. l'Acad. Pétersbourg, Vol. XIII. 1869.
(33) H. Milne-Edwards. "Observations s. l. Ascidies composées des côtes de la Manche." Mémoires d. l'Institut, T. XVIII. 1842.
(34) W. Salensky. "Ueber d. embryonale Entwicklungsgeschichte der Salpen." Zeit. f. wiss. Zool., B. XXVII. 1877.
(35) W. Salensky. "Ueber die Knospung d. Salpen." Morphol. Jahrbuch, Bd. III. 1877.
(36) W. Salensky. "Ueber die Entwicklung d. Hoden u. über den Generationswechsel d. Salpen." Zeit. f. wiss. Zool., Bd. XXX. Suppl. 1878.
(37) C. Semper. "Ueber die Entstehung d. geschichteten Cellulose-Epidermis d. Ascidien." Arbeit. a. d. zool.-zoot. Instit. Würzburg, Vol. II. 1875.
(38) Fr. Todaro. Sopra lo sviluppo e l'anatomia delle Salpe. Roma, 1875.
(39) Fr. Todaro. "Sui primi fenomeni dello sviluppo delle Salpe." Reale Accademia dei Lincei, Vol. IV. 1880.
III. ELASMOBRANCHII
The impregnation of the ovum is effected in the oviduct. In most forms the whole of the subsequent development, till the time when the embryo is capable of leading a free existence, takes place in the uterus; but in other cases the egg becomes enveloped, during its passage down the oviduct, first in a layer of fluid albumen, and finally in a dense horny layer, which usually takes the form of a quadrilateral capsule with characters varying according to the species. After the formation of this capsule the egg is laid, and the whole of the development, with the exception of the very first stages, takes place externally.
In many of the viviparous forms (Mustelus, Galeus, Carcharias, Sphyrna) the egg is enclosed, during the early stages of development at any rate, in a very delicate shell homologous with that of the oviparous forms; there is usually also a scanty albuminous layer. Both of these are stated by Gerbe (No. 42) to be absent in Squalus spinax.
The following are examples of viviparous genera: Hexanchus, Notidanus, Acanthias, Scymnus, Galeus, Squalus, Mustelus, Carcharias, Sphyrna, Squatina, Torpedo; and the following of oviparous genera: Scyllium, Pristiurus, Cestracion, Raja[17].
[17] For further details, vide Müller (No. 48).
The ovum at the time of impregnation has the form of a large spherical mass, similar to the yolk of a bird's egg, but without a vitelline membrane[18]. The greater part of it is formed of peculiar oval spherules of food-yolk, held together by a protoplasmic network. The protoplasm is especially concentrated in a small lens-shaped area, known as the germinal disc, which is not separated by a sharp line from the remainder of the ovum. Yolk spherules are present in this disc as elsewhere, but are much smaller and of a different character. The segmentation has the normal meroblastic character (fig. 15) and is confined to the germinal disc. Before it commences the germinal disc exhibits amoeboid movements. During the segmentation nuclei make their appearance spontaneously (?) in the yolk adjoining the germinal disc (fig. 15, nx´), and around them portions of the yolk with its protoplasmic network become segmented off. Cells are thus formed which are added to those resulting from the segmentation proper. Even after the segmentation numerous nuclei are present in the granular matter below the blastoderm (fig. 16 A, n´); and around these cells are being continually formed, which enter the blastoderm, and are more especially destined to give rise to the hypoblast. The special destination of many of these cells is spoken of in detail below.
[18] Vide Vol. II., p. 62.
[FIG. 15. SECTION THROUGH GERMINAL DISC OF A PRISTIURUS EMBRYO DURING THE SEGMENTATION.
n. nucleus; nx. nucleus modified prior to division; nx´. modified nucleus in the yolk; f. furrow appearing in the yolk adjacent to the germinal disc.]
At the close of segmentation the blastoderm forms a somewhat lens-shaped disc, thicker at one end than at the other; the thicker end being the embryonic end. It is divided into two strata--an upper one, the epiblast--formed of a single row of columnar cells; and a lower one, the primitive hypoblast, consisting of the remaining cells of the blastoderm, and forming a mass several strata deep. These cells will be spoken of as the lower layer cells, to distinguish them from the true hypoblast which is one of their products.
[FIG. 16. TWO LONGITUDINAL SECTIONS OF THE BLASTODERM OF A PRISTIURUS EMBRYO DURING STAGES PRIOR TO THE FORMATION OF THE MEDULLARY GROOVE.
ep. epiblast; ll. lower layer cells or primitive hypoblast; m. mesoblast; hy. hypoblast; sc. segmentation cavity; es. embryo swelling; n´. nuclei of yolk; er. embryonic rim. c. lower layer cells at the non-embryonic end of the blastoderm.]
A cavity very soon appears in the lower layer cells, near the non-embryonic end of the blastoderm, but the cells afterwards disappear from the floor of this cavity, which then lies between the yolk and the lower layer cells (fig. 16 A, sc). This cavity is the segmentation cavity equivalent to that present in Amphioxus, Amphibia, etc. The chief peculiarity about it is the relatively late period at which it makes its appearance, and the fact that its roof is formed both by the epiblast and by the lower layer cells. Owing to the large size of the segmentation cavity the blastoderm forms a thin layer above the cavity and a thickened ridge round its edge.
[FIG. 17. LONGITUDINAL SECTION THROUGH THE BLASTODERM OF A PRISTIURUS EMBRYO OF THE SAME AGE AS FIG. 28 B.
ep. epiblast; er. embryonic rim; m. mesoblast; al. mesenteron.]
The epiblast in the next stage is inflected for a small arc at the embryonic end of the blastoderm, where it becomes continuous with the lower layer cells; at the same time some of the lower layer cells of the embryonic end of the blastoderm assume a columnar form, and constitute the true hypoblast. The portion of the blastoderm, where epiblast and hypoblast are continuous, forms a projecting structure which will be called the embryonic rim (fig. 16 B, er).
This rim is a very important structure, since it represents the dorsal portion of the lip of the blastopore of Amphioxus. The space between it and the yolk represents the commencing mesenteron, of which the hypoblast on the under side of the lip is the dorsal wall. The ventral wall of the mesenteron is at first formed solely of yolk held together by a protoplasmic network with numerous nuclei. The cavity under the lip becomes rapidly larger (fig. 17, al), owing to the continuous conversion of lower layer cells into columnar hypoblast along an axial line passing from the middle of the embryonic rim towards the centre of the blastoderm. The continuous differentiation of the hypoblast towards the centre of the blastoderm corresponds with the invagination in Amphioxus. During the formation of the embryonic rim the blastoderm grows considerably larger, but, with the exception of the formation of the embryonic rim, retains its primitive constitution.
The segmentation cavity undergoes however important changes. There is formed below it a floor of lower layer cells, derived partly from an ingrowth from the two sides, but mainly from the formation of cells around the nuclei of the yolk (fig. 16). Shortly after the floor of cells has appeared, the whole segmentation cavity becomes obliterated (fig. 17).
The disappearance of the segmentation cavity corresponds in point of time with the formation of the hypoblast by the pseudo-invagination above described; and is probably due to this pseudo-invagination, in the same way that the disappearance of the segmentation cavity in Amphioxus is due to the true invagination of the hypoblast.
When the embryonic rim first appears there are no external indications of the embryo as distinguished from the blastoderm, but when it has attained to some importance the position of the embryo becomes marked out by the appearance of a shield-like area extending inwards from the edge of the embryonic rim, and formed of two folds with a groove between them (fig. 28 B, mg), which is deepest at the edge of the blastoderm, and shallows out as it extends inwards. This groove is the medullary groove; and its termination at the edge of the blastoderm is placed at the hind end of the embryo.
At about the time of its appearance the mesoblast becomes first definitely established.
[FIG. 18. TWO TRANSVERSE SECTIONS OF AN EMBRYO OF THE SAME AGE AS FIG. 17.
A. Anterior section. B. Posterior section.
mg. medullary groove; ep. epiblast; hy. hypoblast; n.al. cells formed round the nuclei of the yolk which have entered the hypoblast; m. mesoblast.
The sections shew the origin of the mesoblast.]
At the edge of the embryonic rim the epiblast and lower layer cells are continuous. Immediately underneath the medullary groove, as is best seen in transverse section (fig. 18), the whole of the lower layer cells become converted into hypoblast, and along this line the columnar hypoblast is in contact with the epiblast above. At the sides however this is not the case; but at the junction of the epiblast and lower layer cells the latter remain undifferentiated. A short way from the edge the lower layer cells become divided into two distinct layers, a lower one continuous with the hypoblast in the middle line, and an upper one between this and the epiblast (fig. 18 B). The upper layer is the commencement of the mesoblast (m). The mesoblast thus arises as two independent lateral plates, one on each side of the medullary groove, which are continuous behind with the undifferentiated lower layer cells at the edge of the embryonic rim. The mesoblast plates are at first very short, and do not extend to the front end of the embryo. They soon however grow forwards as two lateral ridges, attached to the hypoblast, one on each side of the medullary groove (fig. 18 A, m). These ridges become separate from the hypoblast, and form two plates, thinner in front than behind; but still continuous at the edge of the blastoderm with the undifferentiated cells of the lip of the blastopore, and laterally with the lower layer cells of the non-embryonic part of the blastoderm. It results from the above mode of development of the mesoblast, that it may be described as arising in the form of a pair of solid outgrowths of the wall of the alimentary tract; which differ from the mesoblastic outgrowths of the wall of the archenteron in Amphioxus in not containing a prolongation of the alimentary cavity.
[FIG. 19. DIAGRAMMATIC LONGITUDINAL SECTIONS OF AN ELASMOBRANCH EMBRYO.
Epiblast without shading. Mesoblast black with clear outlines to the cells. Lower layer cells and hypoblast with simple shading.
ep. epiblast; m. mesoblast; al. alimentary cavity; sg. segmentation cavity; nc. neural canal; ch. notochord; x. point where epiblast and hypoblast become continuous at the posterior end of the embryo; n. nuclei of yolk.
A. Section of young blastoderm, with segmentation cavity enclosed in the lower layer cells.
B. Older blastoderm with embryo in which hypoblast and mesoblast are distinctly formed, and in which the alimentary slit has appeared. The segmentation cavity is still represented as being present, though by this stage it has in reality disappeared.
C. Older blastoderm with embryo in which the neural canal has become formed, and is continuous posteriorly with the alimentary canal. The notochord, though shaded like mesoblast, belongs properly to the hypoblast.]
A general idea of the structure of the blastoderm at this stage may be gathered from the diagram representing a longitudinal section through the embryo (fig. 19 B). In this figure the epiblast is represented in white and is seen to be continuous at the lip of the blastopore (x) with the shaded hypoblast. Between the epiblast and hypoblast is seen one of the lateral plates of mesoblast, represented by black cells with clear outlines. The non-embryonic lower layer cells of the blastoderm are represented in the same manner as the mesoblast of the body. The alimentary cavity is shewn at al, and below it is seen the yolk with nuclei (n). The segmentation cavity is represented as still persisting, though by this stage it would have disappeared.
[FIG. 20. THREE SECTIONS THROUGH A PRISTIURUS EMBRYO SOMEWHAT YOUNGER THAN FIG. 28 C.
A. Section through the cephalic plate. B. Section through the posterior part of the cephalic plate. C. Section through the trunk.
ch. notochord; mg. medullary groove; al. alimentary tract; lp. lateral plate of mesoblast; pp. body cavity.]
As to the growth of the blastoderm it may be noted that it has greatly extended itself over the yolk. Its edge in the meantime forms a marked ridge, which is due not so much to a thickening as to an arching of the epiblast. This ridge is continuous with the embryonic rim, which gradually concentrates itself into two prominences, one on each side of the tail of the embryo, mainly formed of masses of undifferentiated lower layer cells. These prominences will be called the caudal swellings.
By this stage the three layers of the body, the epiblast, mesoblast, and hypoblast, have become definitely established. The further history of these layers may now be briefly traced.
Epiblast. While the greater part of the epiblast becomes converted into the external epidermis, from which involutions give rise to the olfactory and auditory pits, the lens of the eye, the mouth cavity, and anus, the part of it lining the medullary groove becomes converted into the central nervous system and optic cup. The medullary groove is at first continued to the front end of the medullary plate; but the anterior part of this plate soon enlarges, and the whole plate assumes a spatula form (fig. 28 C, h, and fig. 20 A and B). The enlarged part becomes converted into the brain, and may be called the cephalic plate.
The posterior part of the canal deepens much more rapidly than the rest (fig. 20 C), and the medullary folds unite dorsally and convert the posterior end of the medullary groove into a closed canal, while the groove is still widely open elsewhere. The medullary canal does not end blindly behind, but simply forms a tube not closed at either extremity. The importance of this fact will appear later.
Shortly after the medullary folds have met behind the whole canal becomes closed in. This occurs in the usual way by the junction and coalescence of the medullary folds. In the course of the closing of the medullary groove the edges of the cephalic plate, which have at first a ventral curvature, become bent up in the normal manner, and enclose the dilated cephalic portion of the medullary canal. The closing of the medullary canal takes place earlier in the head and neck than in the back.
An anterior pore at the front end of the canal, like that in Amphioxus and the Ascidians, is not found. The further differentiation of the central nervous system is described in a special chapter: it may however here be stated that the walls of the medullary canal give rise not only to the central nervous system but to the peripheral also.
Mesoblast. The mesoblast was left as two lateral plates continuous behind with the undifferentiated cells of the caudal swellings.
The cells composing them become arranged in two layers (fig. 20 C, lp), a splanchnic layer adjoining the hypoblast, and a somatic layer adjoining the epiblast. Between these two layers there is soon developed in the region of the head a well-marked cavity (fig. 20 A, pp) which is subsequently continued into the region of the trunk, and forms the primitive body cavity, equivalent to the cavity originating as an outgrowth of the archenteron in Amphioxus. The body cavities of the two sides are at first quite independent.
[FIG. 21. TRANSVERSE SECTION THROUGH THE TRUNK OF AN EMBRYO SLIGHTLY OLDER THAN FIG. 28 E.
nc. neural canal; pr. posterior root of spinal nerve; x. subnotochordal rod; ao. aorta; sc. somatic mesoblast; sp. splanchnic mesoblast; mp. muscle-plate; mp´. portion of muscle-plate converted into muscle; Vv. portion of the vertebral plate which will give rise to the vertebral bodies; al. alimentary tract.]
Coincidentally with the appearance of differentiation into somatic and splanchnic layers the mesoblast plates become in the region of the trunk partially split by a series of transverse lines of division into mesoblastic somites. Only the dorsal parts of the plates become split in this way, their ventral parts remaining quite intact. As a result of this each plate becomes divided into a dorsal portion adjoining the medullary canal, which is divided into somites, and may be called the vertebral plate, and a ventral portion not so divided, which may be called the lateral plate. These two parts are at this stage quite continuous with each other; and the body cavity originally extends uninterruptedly to the summit of the vertebral plates (fig. 21).
[FIG. 22. HORIZONTAL SECTION THROUGH THE TRUNK OF AN EMBRYO OF SCYLLIUM CONSIDERABLY YOUNGER THAN 28 F.
The section is taken at the level of the notochord, and shews the separation of the cells to form the vertebral bodies from the muscle-plates.
ch. notochord; ep. epiblast; Vr. rudiment of vertebral body; mp. muscle-plate; mp´. portion of muscle-plate already differentiated into longitudinal muscles.]
The next change results in the complete separation of the vertebral portion of the plate from the lateral portion; thereby the upper segmented part of the body cavity becomes isolated, and separated from the lower and unsegmented part. As a consequence of this change the vertebral plate comes to consist of a series of rectangular bodies, the mesoblastic somites, each composed of two layers, a somatic and a splanchnic, between which is the cavity originally continuous with the body cavity (fig. 23, mp). The splanchnic layer of the plates buds off cells to form the rudiments of the vertebral bodies which are at first segmented in the same planes as the mesoblastic somites (fig. 22, Vr). The plates themselves remain as the muscle-plates (mp), and give rise to the whole of the voluntary muscular system of the body. Between the vertebral and lateral plates there is left a connecting isthmus, with a narrow prolongation of the body cavity (fig. 23 B, st), which gives rise (as described in a special chapter) to the segmental tubes and to other parts of the excretory system.
In the meantime the lateral plates of the two sides unite ventrally throughout the intestinal and cardiac regions of the body, and the two primitively isolated cavities contained in them coalesce. In the tail however the plates do not unite ventrally till somewhat later, and their contained cavities remain distinct till eventually obliterated.
At first the pericardial cavity is quite continuous with the body cavity; but it eventually becomes separated from the body cavity by the attachment of the liver to the abdominal wall, and by a horizontal septum in which run the two ductus Cuvieri (fig. 23 A, sv). Two perforations in this septum (fig. 23 A) leave the cavities in permanent communication.
The parts derived from the two layers of the mesoblast (not including special organs or the vascular system) are as follows:--
From the somatic layer are formed
(1) A considerable part of the voluntary muscular system of the body. (2) The dermis. (3) A large part of the intermuscular connective tissue. (4) Part of the peritoneal epithelium.
From the splanchnic layer are formed
(1) A great part of the voluntary muscular system. (2) Part of the intermuscular connective tissue. (3) The axial skeleton and surrounding connective tissue. (4) The muscular and connective-tissue wall of the alimentary tract. (5) Part of the peritoneal epithelium.
[FIG. 23. SECTIONS THROUGH THE TRUNK OF A SCYLLIUM EMBRYO SLIGHTLY YOUNGER THAN 28 F.
Figure A shews the separation of the body cavity from the pericardial cavity by a horizontal septum in which runs the ductus Cuvieri; on the left side is seen the narrow passage which remains connecting the two cavities. Fig. B through a posterior part of the trunk shews the origin of the segmental tubes and of the primitive ova.
sp.c. spinal canal; W. white matter of spinal cord; pr. commissure connecting the posterior nerve-roots; ch. notochord; x. subnotochordal rod; ao. aorta; sv. sinus venosus; cav. cardinal vein; ht. heart; pp. body cavity; pc. pericardial cavity; oes. solid oesophagus; l. liver; mp. muscle-plate; mp´. inner layer of muscle-plate; Vr. rudiment of vertebral body; st. segmental tube; sd. segmental duct; sp.v. spiral valve; v. subintestinal vein.]
In the region of the head the mesoblast does not at first become divided into somites; but on the formation of the gill clefts a division takes place, which is apparently equivalent to the segmentation of the mesoblast in the trunk. This division causes the body cavity of the head to be divided up into a series of separate segments, one of which is shewn in fig. 24, pp. The walls of the segments eventually give rise to the main muscles of the branchial clefts, and probably also to the muscles of the mandibular arch, of the eye, and of other parts. The cephalic sections of the body cavity will be spoken of as head cavities.
[FIG. 24. HORIZONTAL SECTION THROUGH THE LAST VISCERAL ARCH BUT ONE OF AN EMBRYO OF PRISTIURUS.
ep. epiblast; vc. pouch of hypoblast which will form the walls of a visceral cleft; pp. segment of body-cavity in visceral arch; aa. aortic arch.]
In addition to the parts already mentioned the mesoblast gives rise to the whole of the vascular system, and to the generative system. The heart is formed from part of the splanchnic mesoblast, and the generative system from a portion of the mesoblast of the dorsal part of the body cavity.
The hypoblast. Very shortly after the formation of the mesoblastic plates as lateral differentiations of the lower layer cells, an axial differentiation of the hypoblast appears, which gives rise to the notochord very much in the same way as in Amphioxus.
At first the hypoblast along the axial line forms a single layer in contact with the epiblast. Along this line a rod-like thickening of the hypoblast very soon appears (fig. 25, B and C, Ch´) at the head end of the embryo, and gradually extends backwards. This is the rudiment of the notochord; it remains attached for some time to the hypoblast, and becomes separated from it first at the head end of the embryo (fig. 25 A, ch): the separation is then carried backwards.
A series of sections taken through an embryo shortly after the first differentiation of the notochord presents the following characters.
In the hindermost sections the hypoblast retains a perfectly normal structure and uniform thickness throughout. In the next few sections (fig. 25 C, Ch´) a slight thickening is to be observed in it, immediately below the medullary groove. The layer, which elsewhere is composed of a single row of cells, here becomes two cells deep, but no sign of a division into two layers is exhibited.
In the next few sections the thickening of the hypoblast becomes much more pronounced; we have, in fact, a ridge projecting from the hypoblast towards the epiblast (fig. 25 B, Ch´). This ridge is pressed firmly against the epiblast, and causes in it a slight indentation. The hypoblast in the region of the ridge is formed of two layers of cells, the ridge being entirely due to the uppermost of the two.
[FIG. 25. THREE SECTIONS OF A PRISTIURUS EMBRYO SLIGHTLY OLDER THAN FIG. 28 B.
The sections shew the development of the notochord.
Ch. notochord; Ch´. developing notochord; mg. medullary groove; lp. lateral plate of mesoblast; ep. epiblast; hy. hypoblast.]
In sections in front of this a cylindrical rod, which can at once be recognized as the notochord, and is continuous with the ridge just described, begins to be split off from the hypoblast (fig. 25 A, Ch). It is difficult to say at what point the separation of this rod from the hypoblast is completed, since all intermediate gradations between complete separation and complete attachment are to be seen.
Shortly after the separation takes place, a fairly thick bridge is found connecting the two lateral halves of the hypoblast, but this bridge is anteriorly excessively delicate and thin, and in some cases is barely visible except with high powers. In some sections I have observed possible indications of the process like that described by Calberla for Petronyzon, by which the lateral parts of the hypoblast grow in underneath the axial part, and so isolate it bodily as the notochord.
It is not absolutely clear whether the notochord is to be regarded as an axial differentiation of the hypoblast, or as an axial differentiation of the lower layer cells.
The facts of development both in Amphioxus and Elasmobranchii tend towards the former view; but the nearly simultaneous differentiation of the notochord and the mesoblastic plates lends some support to the supposition that the notochord may be merely a median plate of mesoblast developed slightly later than the two lateral plates.
The alimentary canal or mesenteron was left as a space between the hypoblast and the yolk, ending blindly in front, but opening behind by a widish aperture, the blastopore or anus of Rusconi (vide fig. 19 B).
[FIG. 26. SECTION THROUGH THE ANTERIOR PART OF A PRISTIURUS EMBRYO TO SHEW THE FORMATION OF THE ALIMENTARY TRACT.
Ch. notochord; hy. hypoblast; al. alimentary tract; na. cells passing in from the yolk to form the ventral wall of the alimentary tract.]
The conversion of this irregular cavity into a closed canal commences first of all at the anterior extremity. In this conversion two distinct processes are concerned. One of these is a process of folding off of the embryo from the blastoderm. The other is a simple growth of cells independent of any fold. To the first of these processes the depth and narrowness of the alimentary cavity is due; the second is concerned in forming its ventral wall. The process of the folding off of the embryo from the blastoderm resembles exactly the similar process in the embryo bird. The fold is a perfectly continuous one round the front end of the embryo, but may be conveniently spoken of as composed of a head-fold and two lateral folds.
Of far greater interest than the nature of these folds is the formation of the ventral wall of the alimentary canal. This originates in a growth of cells from the two sides to the middle line (fig. 26). The cells for it are not however mainly derived from pre-existing hypoblast cells, but are formed de novo around the nuclei of the yolk which have already been spoken of (fig. 26, na). The ventral wall of the mesenteron is in fact, to a large extent at any rate, formed as a differentiation of the primitive yolk floor.
[FIG. 27. LONGITUDINAL VERTICAL SECTION OF AN EMBRYO SLIGHTLY YOUNGER THAN THAT IN FIG. 26 D.
The section shews the communication which exists between the neural and alimentary canals.
nc. neural canal; al. alimentary tract; Ch. notochord; Ts. tail swelling.]
The folding off and closing of the alimentary canal in the anterior part of the body proceeds rapidly, and not only is a considerable tract of the alimentary canal formed, but a great part of the head is completely folded off from the yolk before the medullary groove is closed.
The posterior part of the alimentary canal retains for a longer time its primitive condition. Finally however it also becomes closed in, by the lips of the blastopore at the hind end of the embryo meeting and uniting. The peculiarity of the closing in of the posterior part of the alimentary canal consists in the fact that a similar continuity to that in Amphioxus obtains between the neural and alimentary canals. This is due to the medullary folds being continuous at the end of the tail with the lips of the blastopore, which close in the hind end of the alimentary canal; so that, when the medullary folds unite to form a canal, this canal becomes continuous with the alimentary canal, which is closed in at the same time. In other words, the medullary folds assist in enveloping the blastopore which does not therefore become absolutely closed, but opens into the floor of the neural canal. It will afterwards be shewn that it is only the posterior part of the blastopore that becomes closed during the above process, and that the anterior and ventral part long remains open. The general arrangement of the parts, at the time when the hind end of the mesenteron is first closed, is shewn in fig. 27. The same points may be seen in the diagrammatic longitudinal section fig. 19 C.
The middle portion of the alimentary tract is the last to be closed in since it remains till late in embryonic life as the umbilical or vitelline canal, connecting the yolk-sack with the alimentary cavity. The umbilical canal falls into the alimentary tract immediately behind the entrance of the hepatic duct.
[FIG. 27*. TRANSVERSE SECTION THROUGH THE TAIL REGION OF A PRISTIURUS EMBRYO OF THE SAME AGE AS FIG. 28 E.
df. dorsal fin; sp.c. spinal cord; pp. body cavity; sp. splanchnic layer of mesoblast; so. somatic layer of mesoblast; mp. commencing differentiation of muscles; ch. notochord; x. subnotochordal rod arising as an outgrowth of the dorsal wall of the alimentary tract; al. alimentary tract.]
At a fairly early stage of development a rod is constricted off from the dorsal wall of the alimentary canal (figs. 27* and 23 x), which is known as the subnotochordal rod. It is placed immediately below the notochord, and disappears during embryonic life.
General features of the Elasmobranch embryo at successive stages.
Shortly after the three germinal layers become definitely established, the rudiment of the embryo, as visible from the surface, consists of an oblong plate, which extends inwards from the periphery of the blastoderm, and is bounded on its inner side by a head-fold and two lateral folds (fig. 28 B). This plate is the medullary plate; along its axial line is a shallow groove--the medullary groove (mg). The rudiment of the embryo rapidly increases in length, and takes a spatula-like form (fig. 28 C). The front part of it, turned away from the edge of the blastoderm, soon becomes dilated into a broad plate,--the cephalic plate (h)--while the tail end at the edge of the blastoderm is also enlarged, being formed of a pair of swellings--the tail swellings (ts)--derived from the lateral parts of the original embryonic rim. By this stage a certain number of mesoblastic somites have become formed but are not shewn in my figure. They are the foremost somites of the trunk, and those behind them continue to be added, like the segments in Chætopods, between the last formed somite and the end of the body. The increase in length of the body mainly takes place by growth in the region between the last mesoblastic somite and the end of the tail. The anterior part of the body is now completely folded off from the blastoderm, and the medullary groove of the earlier stage has become converted into a closed canal.
By the next stage (fig. 28 D) the embryo has become so much folded off from the yolk both in front and behind that the separate parts of it begin to be easily recognizable.
The embryo is attached to the yolk by a distinct stalk or cord, which in the succeeding stages gradually narrows and elongates, and is known as the umbilical cord (so. s.). The medullary canal has now become completely closed. The anterior region constitutes the brain; and in this part slight constrictions, not perceptible in views of the embryo as a transparent object, mark off three vesicles. These vesicles are known as the fore, mid, and hind brain. From the fore-brain there is an outgrowth on each side, the first rudiment of the optic vesicles (op). The tail swellings are still conspicuous.
[FIG. 28. VIEWS OF ELASMOBRANCH EMBRYOS. A-F. PRISTIURUS. G. and H. SCYLLIUM.
A. A blastoderm before the formation of the medullary plate. sc. segmentation cavity; es. embryonic swelling. B. A somewhat older blastoderm in which the medullary groove has been established. mg. medullary groove. C. An embryo from the dorsal surface, as an opaque object, after the medullary groove has become posteriorly converted into a tube. mg. medullary groove: the reference line points very nearly to the junction between the open medullary groove with the medullary tube; h. cephalic plate; ts. tail swelling. D. Side view of a somewhat older embryo as a transparent object. ch. notochord; op. optic vesicle; 1.v.c. 1st visceral cleft; al. alimentary tract; so.s. stalk connecting the yolk-sack with the embryo. E. Side view of an older embryo as a transparent object. mp. muscle-plates; au.v. auditory vesicle; vc. visceral cleft; ht. heart; m. mouth invagination; an. anal diverticulum; al.v. posterior vesicle of postanal gut. F. G. H. Older embryos as opaque objects.]
The tissues of the body have now become fairly transparent, and there may be seen at the sides of the body seventeen mesoblastic somites. The notochord, which was formed long before the stage represented in figure 28 D, is now also distinctly visible. It extends from almost the extreme posterior to the anterior end of the embryo, and lies between the ventral wall of the spinal canal and the dorsal wall of the intestine. Round its posterior end the neural and alimentary tracts become continuous with each other. Anteriorly the termination of the notochord cannot be seen, it can only be traced into a mass of mesoblast at the base of the brain, which there separates the epiblast from the hypoblast. The alimentary canal (al) is completely closed anteriorly and posteriorly, though still widely open to the yolk-sack in the middle part of its course. In the region of the head it exhibits on each side a slight bulging outwards, the rudiment of the first visceral cleft. This is represented in the figure by two lines (1. v.c.).
The embryo represented in fig. 28 E is far larger than the one just described, but it has not been convenient to represent this increase of size in the figure. Accompanying this increase in size, the folding off from the yolk has considerably progressed, and the stalk which unites the embryo with the yolk is proportionately narrower and longer than before.
The brain is now very distinctly divided into the three lobes, the rudiments of which appeared during the last stage. From the foremost of these the optic vesicles now present themselves as well-marked lateral outgrowths, towards which there has appeared an involution from the external skin (op) to form the lens.
A fresh organ of sense, the auditory sack, now for the first time becomes visible as a shallow pit in the external skin on each side of the hind-brain (au.v). The epiblast which is involuted to form this pit becomes much thickened, and thereby the opacity, indicated in the figure, is produced.
The mesoblastic somites have greatly increased in number by the formation of fresh somites in the tail. Thirty-eight of them were present in the embryo figured. The mesoblast at the base of the brain is more bulky, and there is still a mass of unsegmented mesoblast which forms the tail swellings. The first rudiment of the heart (ht) becomes visible during this stage as a cavity between the mesoblast of the splanchnopleure and the hypoblast.
The fore and hind guts are now longer than they were. An invagination from the exterior to form the mouth has appeared (m) on the ventral side of the head close to the base of the thalamencephalon. The upper end of this eventually becomes constricted off as the pituitary body, and an indication of the future position of the anus is afforded by a slight diverticulum of the hind gut towards the exterior, some little distance from the posterior end of the embryo (an). The portion of the alimentary canal behind this point, though at this stage large, and even dilated into a vesicle at its posterior end (al.v), becomes eventually completely atrophied. It is known as the postanal gut. In the region of the throat the rudiment of a second visceral cleft has appeared behind the first; neither of them is as yet open to the exterior.
In a somewhat older embryo the first spontaneous movements take place, and consist in somewhat rapid excursions of the embryo from side to side, produced by a serpentine motion of the body.
[FIG. 28*. FOUR SECTIONS THROUGH THE POSTANAL PART OF THE TAIL OF AN EMBRYO OF THE SAME AGE AS FIG. 28 F.
A is the posterior section.
nc. neural canal; al. postanal gut; alv. caudal vesicle of postanal gut; x. subnotochord rod; mp. muscle-plate; ch. notochord; cl.al. cloaca; ao. aorta; v.cau. caudal vein.]
A ventral flexure of the præoral part of the head, known as the cranial flexure, which commenced in earlier stages (fig. 28 D and E), has now become very evident, and the mid-brain[19] begins to project in the same manner as in the embryo fowl on the third day, and will soon form the anterior termination of the long axis of the embryo. The fore-brain has increased in size and distinctness, and the anterior part of it may now be looked on as the unpaired rudiment of the cerebral hemispheres.
[19] The part of the brain which I have here called mid-brain, and which unquestionably corresponds to the part called mid-brain in the embryos of higher vertebrates, becomes in the adult what Miklucho-Maclay and Gegenbaur called the vesicle of the third ventricle or thalamencephalon.
Further changes have taken place in the organs of sense, especially in the eye, in which the involution for the lens has made considerable progress. The number of the muscle-plates has again increased, but there is still a region of unsegmented mesoblast in the tail. The thickened portions of mesoblast, which caused the tail swellings, are still to be seen, and would seem to act as the reserve from which is drawn the matter for the rapid growth of the tail, which occurs soon after this. The mass of the mesoblast at the base of the brain has again increased. No fresh features of interest are to be seen in the notochord. The heart is very much more conspicuous than before, and its commencing flexure is very apparent. It now beats actively. The postanal gut is much longer than during the last stage; and the point where the anus will appear is very easily detected by a bulging out of the gut towards the external skin. The alimentary vesicle at the end of the postanal gut, first observable during the last stage, is now a more conspicuous organ. There are three visceral clefts, none of which are as yet open to the exterior.
Figure 28 F represents a considerably older embryo viewed as an opaque object, and fig. 29 A is a view of the head as a transparent object. The stalk connecting it with the yolk is now, comparatively speaking, quite narrow, and is of sufficient length to permit the embryo to execute considerable movements.
The tail has grown immensely, but is still dilated terminally. The terminal dilatation is mainly due to the alimentary vesicle (fig. 28* alv), but the postanal section of the alimentary tract in front of this is now a solid cord of cells. Both the alimentary vesicle and this cord very soon disappear. Their relations are shewn in section in fig. 28*.
The two pairs of limbs have appeared as differentiations of a continuous but not very conspicuous epiblastic thickening, which is probably the rudiment of a lateral fin. The anterior pair is situated just at the front end of the umbilical stalk; and the posterior pair, which is the later developed and less conspicuous of the two, is situated some little distance behind the stalk.
[FIG. 29. VIEWS OF THE HEAD OF ELASMOBRANCH EMBRYOS AT TWO STAGES AS TRANSPARENT OBJECTS.
A. Pristiurus embryo of the same stage as fig. 28 F. B. Somewhat older Scyllium embryo.
III. third nerve; V. fifth nerve; VII. seventh nerve; au.n. auditory nerve; gl. glossopharyngeal nerve; Vg. vagus nerve; fb. fore-brain; pn. pineal gland; mb. mid-brain; hb. hind-brain; iv.v. fourth ventricle; cb. cerebellum; ol. olfactory pit; op. eye; au.V. auditory vesicle; m. mesoblast at base of brain; ch. notochord; ht. heart; Vc. visceral clefts; eg. external gills; pp. sections of body cavity in the head.]
The cranial flexure has greatly increased, and the angle between the long axis of the front part of the head and of the body is less than a right angle. The conspicuous mid-brain (29 A, mb) forms the anterior termination of the long axis of the body. The thin roof of the fourth ventricle (hb) may be noticed in the figure behind the mid-brain. The auditory sack (au.V) is nearly closed, and its opening is not shewn in the figure. In the eye (op) the lens is completely formed. The olfactory pit (ol) is seen a little in front of the eye.
Owing to the opacity of the embryo, the muscle-plates are only indistinctly indicated in fig. 28 F, and no other features of the mesoblast are to be seen.
The mouth is now a deep pit, the hind borders of which are almost completely formed by a thickening in front of the first branchial or visceral cleft, which may be called the first branchial arch or mandibular arch.
Four branchial clefts are now visible, all of which are open to the exterior, but in the embryo, viewed as a transparent object, two more, not open to the exterior, are visible behind the last of these.
Between each of these and behind the last one there is a thickening of the mesoblast which gives rise to a branchial arch. The arch between the first and second cleft is known as the hyoid arch.
Fig. 29 B is a representation of the head of a slightly older embryo in which papillæ may be seen in the front wall of the second, third, and fourth branchial clefts; these papillæ are the commencements of filiform processes which grow out from the gill-clefts and form external gills. The peculiar ventral curvature of the anterior end of the notochord (ch) both in this and in the preceding figure deserves notice.
A peculiar feature in the anatomy makes its appearance at this period, viz. the replacement of the original hollow oesophagus by a solid cord of cells (fig. 23 A, oes) in which a lumen does not reappear till very much later. I have found that in some Teleostei (the Salmon) long after they are hatched a similar solidity in the oesophagus is present. It appears not impossible that this feature in the oesophagus may be connected with the fact that in the ancestors of the present types the oesophagus was perforated by gill slits; and that in the process of embryonic abbreviation the stage with the perforated oesophagus became replaced by a stage with a cord of indifferent cells (the oesophagus being in the embryo quite functionless) out of which the non-perforated oesophagus was directly formed. In the higher types the process of development appears to have become quite direct.
By this stage all the parts of the embryo have become established, and in the succeeding stages the features characteristic of the genus and species are gradually acquired.
Two embryos of Scyllium are represented in fig. 28 G and H, the head and anterior part of the trunk being represented in fig. G, and the whole embryo at a much later stage in fig. H.
In both of these, and especially in the second, an apparent diminution of the cranial flexure is very marked. This diminution is due to the increase in the size of the cerebral hemispheres, which grow upwards and forwards, and press the original fore-brain against the mid-brain behind.
In fig. G the rudiments of the nasal sacks are clearly visible as small open pits.
The first cleft is no longer similar to the rest, but by the closure of the lower part has commenced to be metamorphosed into the spiracle.
Accompanying the change in position of the first cleft, the mandibular arch has begun to bend round so as to enclose the front as well as the sides of the mouth. By this change in the mandibular arch the mouth becomes narrowed in an antero-posterior direction.
In fig. H are seen the long filiform external gills which now project out from all the visceral clefts, including the spiracle. They are attached to the front wall of the spiracle, to both walls of the next four clefts, and to the front wall of the last cleft. They have very possibly become specially developed to facilitate respiration within the egg; and they disappear before the close of larval life.
When the young of Scyllium and other Sharks are hatched they have all the external characters of the adult. In Raja and Torpedo the early stages, up to the acquirement of a shark-like form, are similar to those in the Selachoidei, but during the later embryonic stages the body gradually flattens out, and assumes the adult form, which is thus clearly shewn to be a secondary acquirement.
An embryonic gill cleft behind the last present in the adult is found (Wyman, No. 54) in the embryo of Raja batis.
The unpaired fins are developed in Elasmobranchs as a fold of skin on the dorsal side, which is continued round the end of the tail along the ventral side to the anus. Local developments of this give rise to the dorsal and anal fins. The caudal fin is at first symmetrical, but a special lower lobe grows out and gives to it a heterocercal character.
Enclosure of the yolk-sack and its relation to the embryo.
The blastoderm at the stage represented in fig. 28 A and B forms a small and nearly circular patch on the surface of the yolk, composed of epiblast and lower layer cells. While the body of the embryo is gradually being moulded this patch grows till it envelopes the yolk; the growth is not uniform, but is less rapid in the immediate neighbourhood of the embryonic part of the blastoderm than elsewhere. As a consequence of this, that part of the edge, to which the embryo is attached, forms a bay in the otherwise regular outline of the edge of the blastoderm, and by the time that about two-thirds of the yolk is enclosed this bay is very conspicuous. It is shewn in fig. 30 A, where bl points to the blastoderm, and yk to the part of the yolk not yet covered by the blastoderm. The embryo at this time is only connected with the yolk-sack by a narrow umbilical cord; but, as shewn in the figure, is still attached to the edge of the blastoderm.
[FIG. 30. THREE VIEWS OF THE VITELLUS OF AN ELASMOBRANCH, SHEWING THE EMBRYO, THE BLASTODERM, AND THE VESSELS OF THE YOLK-SACK.
The shaded part (bl) is the blastoderm; the white part the uncovered yolk.
A. Young stage with the embryo still attached at the edge of the blastoderm. B. Older stage with the yolk not quite enclosed by the blastoderm. C. Stage after the complete enclosure of the yolk.
yk. yolk; bl. blastoderm; v. venous trunks of yolk-sack; a. arterial trunks of yolk-sack; y. point of closure of the yolk blastopore; x. portion of the blastoderm outside the arterial sinus terminalis.]
Shortly subsequent to this the bay in the blastoderm, at the head of which the embryo is attached, becomes obliterated by its two sides coming together and coalescing. The embryo then ceases to be attached at the edge of the blastoderm. But a linear streak formed by the coalesced edges of the blastoderm is left connecting the embryo with the edge of the blastoderm. This streak is probably analogous to (though not genetically related with) the primitive streak in the Amniota.
This stage is represented in fig. 30 B. In this figure there is only a small patch of yolk (yk) not yet enclosed, which is situated at some little distance behind the embryo. Throughout all this period the edge of the blastoderm has remained thickened: a feature which persists till the complete investment of the yolk, which takes place shortly after the stage last described. In this thickened edge a circular vein arises which brings back the blood from the yolk-sack to the embryo. The opening in the blastoderm, exposing the portion of the yolk not yet covered, may be conveniently called the yolk blastopore. It is interesting to notice that, owing to the large size of the yolk in Elasmobranchs, the posterior part of the primitive blastopore becomes encircled by the medullary folds and tail swellings, and is so closed long before the anterior and more ventral part, which is represented by the uncovered portion of the yolk. It is also worth remarking that, owing to the embryo becoming removed from the edge of the blastoderm, the final closure of the yolk blastopore takes place at some little distance from the embryo.
The blastoderm enclosing the yolk is formed of an external layer of epiblast, a layer of mesoblast below in which the blood-vessels are developed, and within this a layer of hypoblast, which is especially well marked and ciliated (Leydig, No. 46) in the umbilical stalk, where it lines the canal leading from the yolk-sack to the intestine. In the region of the yolk-sack proper the blastoderm is so thin that it is not easy to be quite sure that a layer of hypoblast is throughout distinct. Both the hypoblast and mesoblast of the yolk-sack are formed by a differentiation of the primitive lower layer cells.
Nutriment from the yolk-sack is brought to the embryo partly through the umbilical canal and so into the intestine, and partly by means of blood-vessels in the mesoblast of the sack. The blood-vessels arise before the blastoderm has completely covered the yolk.
Fig. 30 A represents the earliest stage of the circulation of the yolk-sack. At this stage there is visible a single arterial trunk (a) passing forwards from the embryo and dividing into two branches. No venous trunk could be detected with the simple microscope, but probably venous channels were present in the thickened edge of the blastoderm.
In fig. 30 B the circulation is greatly advanced. The blastoderm has now nearly completely enveloped the yolk, and there remains only a small circular space (yk) not enclosed by it. The arterial trunk is present as before, and divides in front of the embryo into two branches which turn backwards and form a nearly complete ring round the embryo. In general appearance this ring resembles the sinus terminalis of the area vasculosa of the Bird, but in reality bears quite a different relation to the circulation. It gives off branches on its inner side only.
A venous system of returning vessels is now fully developed, and its relations are very remarkable. There is a main venous ring in the thickened edge of the blastoderm, which is connected with the embryo by a single stem running along the seam where the edges of the blastoderm have coalesced. Since the venous trunks are only developed behind the embryo, it is only the posterior part of the arterial ring that gives off branches.
The succeeding stage (fig. 30 C) is also one of considerable interest. The arterial ring has greatly extended, and now embraces nearly half the yolk, and sends off trunks on its inner side along its whole circumference. More important changes have taken place in the venous system. The blastoderm has now completely enveloped the yolk, and the venous ring is therefore reduced to a point. The small veins which originally started from it may be observed diverging in a brush-like fashion from the termination of the unpaired trunk, which originally connected the venous ring with the heart.
At a still later stage the arterial ring embraces the whole yolk, and, as a result of this, vanishes in its turn, as did the venous ring before it. There is then present a single arterial and a single venous trunk. The arterial trunk is a branch of the dorsal aorta, and the venous trunk originally falls into the heart together with the subintestinal or splanchnic vein. On the formation of the liver the proximal end of the subintestinal vein becomes the portal vein, and it is joined just as it enters the liver by the venous trunk from the yolk-sack. The venous trunk leaves the body on the right side, and the arterial on the left.
The yolk-sack persists during the whole of embryonic life, and in the majority of Elasmobranch embryos there arises within the body walls an outgrowth from the umbilical canal into which a large amount of the yolk passes. This outgrowth forms an internal yolk-sack. In Mustelus vulgaris the internal yolk-sack is very small, and in Mustelus lævis it is absent. The latter species, which is one of those in which development takes place within the uterus, presents a remarkable peculiarity in that the vascular surface of the yolk-sack becomes raised into a number of folds, which fit into corresponding depressions in the vascular walls of the uterus. The yolk-sack becomes in this way firmly attached to the walls of the uterus, and the two together constitute a kind of placenta. A similar placenta is found in Carcharias.
After the embryo is hatched or born, as the case may be, the yolk-sack becomes rapidly absorbed.
BIBLIOGRAPHY.
(40) F. M. Balfour. "A preliminary account of the development of the Elasmobranch Fishes." Quart. J. of Micr. Science, Vol. XIV. 1876.
(41) F. M. Balfour. "A Monograph on the development of Elasmobranch Fishes." London, 1878. Reprinted from the Journal of Anat. and Physiol. for 1876, 1877, and 1878.
(42) Z. Gerbe. "Recherches sur la segmentation de la cicatrule et la formation des produits adventifs de l'oeuf des Plagiostomes et particulièrement des Raies." Vide also Journal de l'Anatomie et de la Physiologie, 1872.
(43) W. His. "Ueb. d. Bildung v. Haifischenembryonen." Zeit. für Anat. u. Entwick., Vol. II. 1877.
(44) A. Kowalevsky. "Development of Acanthias vulgaris and Mustelus lævis." (Russian.) Transactions of the Kiew Society of Naturalists, Vol. I. 1870.
(45) R. Leuckart. "Ueber die allmählige Bildung d. Körpergestalt bei d. Rochen." Zeit. f. wiss. Zool., Bd. II., p. 258.
(46) Fr. Leydig. Rochen u. Haie. Leipzig, 1852.
(47) A. W. Malm. "Bidrag till kännedom om utvecklingen af Rajæ." Kongl. vetenskaps akademiens förhandlingar. Stockholm, 1876.
(48) Joh. Müller. Glatter Haie des Aristoteles und über die Verschiedenheiten unter den Haifischen und Rochen in der Entwicklung des Eies. Berlin, 1840.
(49) S. L. Schenk. "Die Eier von Raja quadrimaculata innerhalb der Eileiter." Sitz. der k. Akad. Wien, Vol. LXXIII. 1873.
(50) Alex. Schultz. "Zur Entwicklungsgeschichte des Selachiereies." Archiv für micro. Anat., Vol. XI. 1875.
(51) Alex. Schultz. "Beitrag zur Entwicklungsgeschichte d. Knorpelfische." Archiv für micro. Anat., Vol. XIII. 1877.
(52) C. Semper. "Die Stammesverwandschaft d. Wirbelthiere u. Wirbellosen." Arbeit. a. d. zool.-zoot. Instit. Würzburg, Vol. II. 1875.
(53) C. Semper. "Das Urogenitalsystem d. Plagiostomen, etc." Arbeit. a. d. zool.-zoot. Instit. Würzburg, Vol. II. 1875.
(54) Wyman. "Observations on the Development of Raja batis." Memoirs of the American Academy of Arts and Sciences, Vol. IX. 1864.
IV. TELEOSTEI
The majority of the Teleostei deposit their eggs before impregnation, but some forms are viviparous, e.g. Blennius viviparus. Not a few carry their eggs about; but this operation is with a few exceptions performed by the male. In Syngnathus the eggs are carried in a brood-pouch of the male situated behind the anus. Amongst the Siluroids the male sometimes carries the eggs in the throat above the gill clefts. Ostegeniosus militaris, Arius falcarius, and Arius fissus have this peculiar habit.
The ovum when laid is usually invested in the zona radiata only, though a vitelline membrane is sometimes present in addition, e.g. in the Herring. It is in most cases formed of a central yolk mass, which may either be composed of a single large vitelline sphere, or of distinct yolk spherules. The yolk mass is usually invested by a granular protoplasmic layer, which is especially thickened at one pole to form the germinal disc.
In the Herring's ovum the germinal disc is formed, as in many Crustacea, at impregnation; the protoplasm which was previously diffused through the egg becoming aggregated at the germinal pole and round the periphery.
Impregnation is external, and on its occurrence a contraction of the vitellus takes place, so that a space is formed between the vitellus and the zona radiata, which becomes filled with fluid.
The peculiarities in the development of the Teleostean ovum can best be understood by regarding it as an Elasmobranch ovum very much reduced in size. It seems in fact very probable that the Teleostei are in reality derived from a type of Fish with a much larger ovum. The occurrence of a meroblastic segmentation, in spite of the ovum being usually smaller than that of Amphibia and Acipenser, etc., in which the segmentation is complete, as well as the solid origin of many of the organs, receives its most plausible explanation on this hypothesis.
The proportion of the germinal disc to the whole ovum varies considerably. In very small eggs, such as those of the Herring, the disc may form as much as a fifth of the whole.
The segmentation, which is preceded by active movements of the germinal disc, is meroblastic. There is nothing very special to note with reference to its general features, but while in large ova like those of the Salmon the first furrows only penetrate for a certain depth through the germinal disc, in small ova like those of the Herring they extend through the whole thickness of the disc. During the segmentation a great increase in the bulk of the blastoderm takes place.
In hardened specimens a small cavity amongst the segmentation spheres may be present at any early stage; but it is probably an artificial product, and in any case has nothing to do with the true segmentation cavity, which does not appear till near the close of segmentation. The peripheral layer of granular matter, continuous with the germinal disc, does not undergo division, but it becomes during the segmentation specially thickened and then spreads itself under the edge of the blastoderm; and, while remaining thicker in this region, gradually grows inwards so as to form a continuous sub-blastodermic layer. In this layer nuclei appear, which are equivalent to those in the Elasmobranch ovum. A considerable number of these nuclei often become visible simultaneously (van Beneden, No. 60) and they are usually believed to arise spontaneously, though this is still doubtful[20]. Around these nuclei portions of protoplasm are segmented off, and cells are thus formed, which enter the blastoderm, and have nearly the same destination as the homologous cells of the Elasmobranch ovum.
[20] Vide Vol. II. p. 108.
During the later stages of segmentation one end of the blastoderm becomes thickened and forms the embryonic swelling; and a cavity appears between the blastoderm and the yolk which is excentrically situated near the non-embryonic part of the blastoderm. This cavity is the true segmentation cavity. Both the cavity and the embryonic swelling are seen in section in fig. 31 A and B.
In Leuciscus rutilus Bambeke describes a cavity as appearing in the middle of the blastoderm during the later stages of segmentation. From his figures it might be supposed that this cavity was equivalent to the segmentation cavity of Elasmobranchs in its earliest condition, but Bambeke states that it disappears and that it has no connection with the true segmentation cavity. Bambeke and other investigators have failed to recognize the homology of the segmentation cavity in Teleostei with that in Elasmobranchii, Amphibia, etc.
With the appearance of the segmentation cavity the portion of the blastoderm which forms its roof becomes thinned out, so that the whole blastoderm consists of (1) a thickened edge especially prominent at one point where it forms the embryonic swelling, and (2) a thinner central portion. The changes which now take place result in the differentiation of the embryonic layers, and in the rapid extension of the blastoderm round the yolk, accompanied by a diminution in its thickness.
[FIG. 31. LONGITUDINAL SECTIONS THROUGH THE BLASTODERM OF THE TROUT AT AN EARLY STAGE OF DEVELOPMENT.
A. at the close of the segmentation; B. after the differentiation of the germinal layers.
ep´. epidermic layer of the epiblast; sc. segmentation cavity.]
The first differentiation of the layers consists in a single row of cells on the surface of the blastoderm becoming distinctly marked off as a special layer (fig. 31 A); which however does not constitute the whole epiblast but only a small part of it, which will be spoken of as the epidermic layer. The complete differentiation of the epiblast is effected by the cells of the thickened edge of the blastoderm becoming divided into two strata (fig. 31 B). The upper stratum constitutes the epiblast. It is divided into two layers, viz., the external epidermic layer already mentioned, and an internal layer known as the nervous layer, formed of several rows of vertically arranged cells. According to the unanimous testimony of investigators the roof of the segmentation cavity is formed of epiblast cells only. The lower stratum in the thickened rim of the blastoderm is several rows of cells deep, and corresponds with the lower layer cells or primitive hypoblast in Elasmobranchii. It is continuous at the edge of the blastoderm with the nervous layer of the epiblast.
In smaller Teleostean eggs there is formed, before the blastoderm becomes differentiated into epiblast and lower layer cells, a complete stratum of cells around the nuclei in the granular layer underneath the blastoderm. This layer is the hypoblast; and in these forms the lower layer cells of the blastoderm are stated to become converted into mesoblast only. In the larger Teleostean eggs, such as those of the Salmonidæ, the hypoblast, as in Elasmobranchs, appears to be only partially formed from the nuclei of the granular layer. In these forms however, as in the smaller Teleostean ova and in Elasmobranchii, the cells derived from the granular stratum give rise to a more or less complete cellular floor for the segmentation cavity. The segmentation cavity thus becomes enclosed between an hypoblastic floor and an epiblastic roof several cells deep. It becomes obliterated shortly after the appearance of the medullary plate.
At about the time when the three layers become established the embryonic swelling takes a somewhat shield-like form (fig. 33 A). Posteriorly it terminates in a caudal prominence (ts) homologous with the pair of caudal swellings in Elasmobranchs. The homologue of the medullary groove very soon appears as a shallow groove along the axial line of the shield. After these changes there takes place in the embryonic layers a series of differentiations leading to the establishment of the definite organs. These changes are much more difficult to follow in the Teleostei than in the Elasmobranchii, owing partly to the similarity of the cells of the various layers, and partly to the primitive solidity of all the organs.
The first changes in the epiblast give rise to the central nervous system. The epiblast, consisting of the nervous and epidermic strata already indicated, becomes thickened along the axis of the embryo and forms a keel projecting towards the yolk below: so great is the size of this keel in the front part of the embryo that it influences the form of the whole body and causes the outline of the surface adjoining the yolk to form a strong ridge moulded on the keel of the epiblast (fig. 32 A and B). Along the dorsal line of the epiblast keel is placed the shallow medullary groove; and according to Calberla (No. 61) the keel is formed by the folding together of the two sides of the primitively uniform epiblastic layer. The keel becomes gradually constricted off from the external epiblast and then forms a solid cord below it. Subsequently there appears in this cord a median slit-like canal, which forms the permanent central canal of the cerebrospinal cord. The peculiarity in the formation of the central nervous system of Teleostei consists in the fact that it is not formed by the folding over of the sides of the medullary groove into a canal, but by the separation, below the medullary groove, of a solid cord of epiblast in which the central canal is subsequently formed. Various views have been put forward to explain the apparently startling difference between Teleostei, with which Lepidosteus and Petromyzon agree, and other vertebrate forms. The explanations of Götte and Calberla appear to me to contain between them the truth in this matter. The groove above in part represents the medullary groove; but the closure of the groove is represented by the folding together of the lateral parts of the epiblast plate to form the medullary keel.
According to Götte this is the whole explanation, but Calberla states for Syngnathus and Salmo that the epidermic layer of the epiblast is carried down into the keel as a double layer just as if it had been really folded in. This ingrowth of the epidermic layer is shewn in fig. 32 A where it is just commencing to pass into the keel; and at a later stage in fig. 32 B where the keel has reached its greatest depth.
Götte maintains that Calberla's statements are not to be trusted, and I have myself been unable to confirm them for Teleostei or Lepidosteus; but if they could be accepted the difference in the formation of the medullary canal in Teleostei and in other Vertebrata would become altogether unimportant and consist simply in the fact that the ordinary open medullary groove is in Teleostei obliterated in its inner part by the two sides of the groove coming together. Both layers of epiblast would thus have a share in the formation of the central nervous system; the epidermic layer giving rise to the lining epithelial cells of the central canal, and the nervous layer to the true nervous tissue.
The separation of the solid nervous system from the epiblast takes place relatively very late; and, before it has been completed, the first traces of the auditory pits, of the optic vesicles, and of the olfactory pits are visible. The auditory pit arises as a solid thickening of the nervous layer of the epiblast at its point of junction with the medullary keel; and the optic vesicles spring as solid outgrowths from part of the keel itself. The olfactory pits are barely indicated as thickenings of the nervous layer of the epiblast.
[FIG. 32. TWO TRANSVERSE SECTIONS OF SYNGNATHUS. (After Calberla.)
A. Younger stage before the definite establishment of the notochord. B. Older stage. The epidermic layer of the epiblast is represented in black.
ep. epidermic layer of epiblast; mc. neural cord; hy. hypoblast; me. mesoblast; ch. notochord.]
At this early stage all the organs of special sense are attached to a layer continuous with or forming part of the central nervous system; and this fact has led Götte (No. 63) to speak of a special-sense plate, belonging to the central nervous system and not to the skin, from which all the organs of special sense are developed; and to conclude that a serial homology exists between these organs in their development. A comparison between Teleostei and other forms shews that this view cannot be upheld; even in Teleostei the auditory and olfactory rudiments arise rather from the epiblast at the sides of the brain than from the brain itself, while the optic vesicles spring from the first directly from the medullary keel, and are therefore connected with the central nervous system rather than with the external epiblast. In a slightly later stage the different connections of the two sets of sense organs is conclusively shewn by the fact that, on the separation of the central nervous system from the epiblast, the optic vesicles remain attached to the former, while the auditory and olfactory vesicles are continuous with the latter.
After its separation from the central nervous system the remainder of the epiblast gives rise to the skin, etc., and most probably the epidermic stratum develops into the outer layer of the epidermis and the nervous stratum into the mucous layer. The parts of the organs of special sense, which arise from the epiblast, are developed from the nervous layer. In the Trout (Oellacher, No. 72) both layers are continued over the yolk-sack; but in Clupeus and Gasterosteus only the epidermic has this extension. According to Götte the distinction between the two layers becomes lost in the later embryonic stages.
Although it is thoroughly established that the mesoblast originates from the lower of the two layers of the thickened embryonic rim, it is nevertheless not quite certain whether it is a continuous layer between the epiblast and hypoblast, or whether it forms two lateral masses as in Elasmobranchs. The majority of observers take the former view, while Calberla is inclined to adopt the latter. In the median line of the embryo underneath the medullary groove there are undoubtedly from the first certain cells which eventually give rise to the notochord; and it is these cells the nature of which is in doubt. They are certainly at first very indistinctly separated from the mesoblast on the two sides, and Calberla also finds that there is no sharp line separating them from the secondary hypoblast (fig. 32 A). Whatever may be the origin of the notochord the mesoblast very soon forms two lateral plates, one on each side of the body, and between them is placed the notochord (fig. 32 B). The general fate of the two mesoblast plates is the same as in Elasmobranchs. They are at first quite solid and exhibit relatively late a division into splanchnic and somatic layers, between which is placed the primitive body cavity. The dorsal part of the plates becomes transversely segmented in the region of the trunk; and thus gives rise to the mesoblastic somites, from which the muscle plates and the perichordal parts of the vertebral column are developed. The ventral or outer part remains unsegmented. The cavity of the ventral section becomes the permanent body cavity. It is continued forward into the head (Oellacher), and part of it becomes separated off from the remainder as the pericardial cavity.
The hypoblast forms a continuous layer below the mesoblast, and, in harmony with the generally confined character of the development of the organs in Teleostei, there is no space left between it and the yolk to represent the primitive alimentary cavity. The details of the formation of the true alimentary tube have not been made out; it is not however formed by a folding in of the lateral parts of the hypoblast, but arises as a solid or nearly solid cord in the axial line, between the notochord and the yolk, in which a lumen is gradually established.
In the just hatched larva of an undetermined freshwater fish with a very small yolk-sack I found that the yolk extended along the ventral side of the embryo from almost the mouth to the end of the gut. The gut had, except in the hinder part, the form of a solid cord resting in a concavity of the yolk. In the hinder part of the gut a lumen was present, and below this part the amount of yolk was small and the yolk nuclei numerous. Near the limit of its posterior extension the yolk broke up into a mass of cells, and the gut ended behind by falling into this mass. These incomplete observations appear to shew that the solid gut owes its origin in a large measure to nuclei derived from the yolk.
When the yolk has become completely enveloped a postanal section of gut undoubtedly becomes formed; and although, owing to the solid condition of the central nervous system, a communication between the neural and alimentary canals cannot at first take place, yet the terminal vesicle of the postanal gut of Elasmobranchii is represented by a large vesicle, originally discovered by Kupffer (No. 68), which can easily be seen in the embryos of most Teleostei, but the relations of which have not been satisfactorily worked out (vide fig. 34, hyv). As the tail end of the embryo becomes separated off from the yolk the postanal vesicle atrophies.
General development of the Embryo. Attention has already been called to the fact that the embryo first appears as a thickening of the edge of the blastoderm which soon assumes a somewhat shield-like form (fig. 33 A). The hinder end of the embryo, which is placed at the edge of the blastoderm, is somewhat prominent, and forms the caudal swelling (ts). The axis of the embryo is marked by a shallow groove.
[FIG. 33. THREE STAGES IN THE DEVELOPMENT OF THE SALMON. (After His.)
ts. tail swelling; au.v. auditory vesicle; oc. optic vesicle; ce. cerebral rudiment; m.b. mid-brain; cb. cerebellum; md. medulla oblongata; m.so. mesoblastic somite.]
The body now rapidly elongates, and at the same time becomes considerably narrower, while the groove along the axis becomes shallower and disappears. The anterior, and at first proportionately a very large part, soon becomes distinguished as the cephalic region (fig. 33 B). The medullary cord in this region becomes very early divided into three indistinctly separated lobes, representing the fore, the mid, and the hind brains: of these the anterior is the smallest. With it are connected the optic vesicles (oc)--solid at first--which are pushed back into the region of the mid-brain.
The trunk grows in the usual way by the addition of fresh somites behind.
After the yolk has become completely enveloped by the blastoderm the tail becomes folded off, and the same process takes place at the front end of the embryo. The free tail end of the embryo continues to grow, remaining however closely applied to the yolk-sack, round which it curls itself to an extent varying with the species (vide fig. 34).
The general growth of the embryo during the later stages presents a few special features of interest. The head is remarkable for the small apparent amount of the cranial flexure. This is probably due to the late development of the cerebral hemispheres. The flexure of the floor of the brain is however quite as considerable in the Teleostei as in other types. The gill clefts develop from before backwards. The first cleft is the hyomandibular, and behind this there are the hyobranchial and four branchial clefts. Simultaneously with the clefts there are developed the branchial arches. The postoral arches formed are the mandibular, hyoid and five branchial arches. In the case of the Salmon all of these appear before hatching.
[FIG. 34. VIEW OF AN ADVANCED EMBRYO OF A HERRING IN THE EGG. (After Kupffer.)
oc. eye; ht. heart; hyv. postanal vesicle; ch. notochord.]
The first cleft closes up very early (about the time of hatching in the Salmon); and about the same time there springs a membranous fold from the hyoid arch, which gradually grows backwards over the arches following, and gives rise to the operculum. There appear in the Salmon shortly before hatching double rows of papillæ on the four anterior arches behind the hyoid. They are the rudiments of the branchiæ. They reach a considerable length before they are covered in by the opercular membrane. In Cobitis (Götte, No. 64) they appear in young larvæ as filiform processes equivalent to the external gills of Elasmobranchs. The extremities of these processes atrophy; while the basal portions became the permanent gill lamellæ. The general relation of the clefts, after the closure of the hyomandibular, is shewn in fig. 35.
The air-bladder is formed as a dorsal outgrowth of the alimentary tract very slightly in front of the liver. It grows in between the two limbs of the mesentery, in which it extends itself backwards. It appears in the Salmon, Carp, and other types to originate rather on the right side of the median dorsal line, but whether this fact has any special significance is rather doubtful. In the Salmon and Trout it is formed considerably later than the liver, but the two are stated by Von Baer to arise in the Carp nearly at the same time. The absence of a pneumatic duct in the Physoclisti is due to a post-larval atrophy. The region of the stomach is reduced almost to nothing in the larva.
The oesophagus becomes solid, like that of Elasmobranchs, and remains so for a considerable period after hatching.
The liver, in the earliest stage in which I have met with it in the Trout (27 days after impregnation), is a solid ventral diverticulum of the intestine, which in the region of the liver is itself without a lumen.
[FIG. 35. DIAGRAMMATIC VIEW OF THE HEAD OF AN EMBRYO TELEOSTEAN, WITH THE PRIMITIVE VASCULAR TRUNKS. (From Gegenbaur.)
a. auricle; v. ventricle; abr. branchial artery; c´. carotid; ad. aorta; s. branchial clefts; sv. sinus venosus; dc. ductus Cuvieri; n. nasal pit.]
The excretory system commences with the formation of a segmental duct, formed by a constriction of the parietal wall of the peritoneal cavity. The anterior end remains open to the body cavity, and forms a pronephros (head kidney). On the inner side of and opposite this opening a glomerulus is developed, and the part of the body cavity containing both the glomerulus and the opening of the pronephros becomes shut off from the remainder of the body cavity, and forms a completely closed Malpighian capsule.
The mesonephros (Wolffian body) is late in developing.
The unpaired fins arise as simple folds of the skin along the dorsal and ventral edges, continuous with each other round the end of the tail. The ventral fold ends anteriorly at the anus.
The dorsal and anal fins are developed from this fold by local hypertrophy. The caudal fin[21], however, undergoes a more complicated metamorphosis. It is at first symmetrical or nearly so on the dorsal and ventral sides of the hinder end of the notochord. This symmetry is not long retained, but very soon the ventral part of the fin with its fin rays becomes much more developed than the dorsal part, and at the same time the posterior part of the notochord bends up towards the dorsal side.
[21] In addition to the paper by Alex. Agassiz (No. 55) vide papers by Huxley, Kölliker, Vogt, etc.
In some few cases, e.g. Gadus, Salmo, owing to the simultaneous appearance of a number of fin rays on the dorsal and ventral side of the notochord the external symmetry of the tail is not interfered with in the above processes. In most instances this is far from being the case.
[FIG. 36. THREE STAGES IN THE DEVELOPMENT OF THE TAIL OF THE FLOUNDER (PLEURONECTES). (After Agassiz.)
A. Stage in which the permanent caudal fin has commenced to be visible as an enlargement of the ventral side of the embryonic caudal fin. B. Ganoid-like stage in which there is a true external heterocercal tail. C. Stage in which the embryonic caudal fin has almost completely atrophied.
c. embryonic caudal fin; f. permanent caudal fin; n. notochord; u. urostyle.]
In the Flounder, which may serve as a type, the primitive symmetry is very soon destroyed by the appearance of fin rays on the ventral side. The region where they are present soon forms a lobe; and an externally heterocercal tail is produced (fig. 36 A). The ventral lobe with its rays continues to grow more prominent and causes the tail fin to become bilobed (fig. 36 B); there being a dorsal embryonic lobe without fin rays (c), which contains the notochord, and a ventral lobe with fin rays, which will form the permanent caudal fin. In this condition the tail fin resembles the usual Elasmobranch form or still more that of some Ganoids, e.g. the Sturgeon. The ventral lobe continues to develop; and soon projects beyond the dorsal, which gradually atrophies together with the notochord contained in it, and finally disappears, leaving hardly a trace on the dorsal side of the tail (fig. 36 C, c). In the meantime the fin rays of the ventral lobe gradually become parallel to the axis of the body; and this lobe, together with a few accessory dorsal and ventral fin rays supported by neural and hæmal processes, forms the permanent tail fin, which though internally unsymmetrical, assumes an externally symmetrical form. The upturned end of the notochord which was originally continued into the primitive dorsal lobe becomes ensheathed in a bone without a division into separate vertebræ. This bone forms the urostyle (u). The hæmal processes belonging to it are represented by two cartilaginous masses, which subsequently ossify, forming the hypural bones, and supporting the primary fin rays of the tail (fig. 36 C). The ultimate changes of the notochord and urostyle vary very considerably in the different types of Teleostei. Teleostei may fairly be described as passing through an Elasmobranch stage or a stage like that of most pre-jurassic Ganoids or the Sturgeon as far as concerns their caudal fin.
The anterior paired fins arise before the posterior; and there do not appear to be any such indications as in Elasmobranchii of the paired fins arising as parts of a continuous lateral fin.
Most osseous fishes pass through more or less considerable post-embryonic changes, the most remarkable of which are those undergone by the Pleuronectidæ[22]. These fishes, which in the adult state have the eyes unsymmetrically placed on one side of the head, leave the egg like normal Teleostei. In the majority of cases as they become older the eye on the side, which in the adult is without an eye, travels a little forward and then gradually rotates over the dorsal side of the head, till finally it comes to lie on the same side as the other eye. During this process the rotating eye always remains at the surface and continues functional; and on the two eyes coming to the same side of the head the side of the body without an organ of vision loses its pigment cells, and becomes colourless.
[22] Vide Agassiz (No. 56) and Steenstrup, Malm.
The dorsal fin, after the rotation of the eye, grows forward beyond the level of the eyes. In the genus Plagusia (Steenstrup, Agassiz, No. 56) the dorsal fin grows forward before the rotation of the eye (the right eye in this form), and causes some modifications in the process. The eye in travelling round gradually sinks into the tissues of the head, at the base of the fin above the frontal bone; and in this process the original large opening of the orbit becomes much reduced. Soon a fresh opening on the opposite and left side of the dorsal fin is formed; so that the orbit has two external openings, one on the left and one on the right side. The original one on the right soon atrophies, and the eye passes through the tissues at the base of the dorsal fin completely to the left side.
The rotating eye may be either the right or the left according to the species.
The most remarkable feature in which the young of a large number of Teleostei differ from the adults is the possession of provisional spines, very often formed as osseous spinous projections the spaces between which become filled up in the adult. These processes are probably, as suggested by Günther, secondary developments acquired, like the Zooea spines of larval Crustaceans, for purposes of defence.
The yolk-sack varies greatly in size in the different types of Teleostei.
According as it is enclosed within the body-wall, or forms a distinct ventral appendage, it is spoken of by Von Baer as an internal or external yolk-sack. By Von Baer the yolk-sack is stated to remain in communication with the intestine immediately behind the liver, while Lereboullet states that there is a vitelline pedicle opening between the stomach and the liver which persists till the absorption of the yolk-sack. My own observations do not fully confirm either of these statements for the Salmon and Trout. So far as I have been able to make out, all communication between the yolk-sack and the alimentary tract is completely obliterated very early. In the Trout the communication between the two is shut off before hatching, and in the just-hatched Salmon I can find no trace of any vitelline pedicle. The absorption of the yolk would seem therefore to be effected entirely by blood-vessels.
The yolk-sack persists long after hatching, and is gradually absorbed. There is during the stages either just before hatching or shortly subsequent to hatching (Cyprinus) a rich vascular development in the mesoblast of the yolk-sack. The blood is at first contained in lacunar spaces, but subsequently it becomes confined to definite channels. As to its exact relations to the vascular system of the embryo more observations seem to be required.
The following account is given by Rathke (No. 72*) and Lereboullet (No. 71). At first a subintestinal vein (vide chapter on Circulation) falls into the lacunæ of the yolk-sack, and the blood from these is brought back direct to the heart. At a later period, when the liver is developed, the subintestinal vessel breaks up into capillaries in the liver, thence passes into the yolk-sack, and from this to the heart. An artery arising from the aorta penetrates the liver, and there breaks up into capillaries continuous with those of the yolk-sack. This vessel is perhaps the equivalent of the artery which supplies the yolk-sack in Elasmobranchii, but it seems possible that there is some error in the above description.
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