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.
Chapter 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.
Chapter 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.
Chapter 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.
Chapter 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.
Chapter 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].
Chapter 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].
Chapter 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].
Chapter VIII. Aves. Pp. [145]-201.
Segmentation and formation of the layers, pp. [145]-166. General history of of the germinal layers, pp. [166]-169. General development of the embryo, pp. [169]-180. Fœtal membranes, pp. [185]-199. Amnion, pp. [185]-191. Allantois, pp. [191]-193. Yolk-sack, pp. [193]-199.
Chapter 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.
Chapter 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 fœtal 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.
Chapter 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].
Chapter 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.
Chapter 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].
PART II. ORGANOGENY;
Introduction. Pp. [391], [392].
Chapter XIV. The Epidermis and its Derivatives. Pp. [393]-399.
Protective epidermic structures, pp. [393]-397. Dermal skeletal structures, p. [397]. Glands, pp. [397], [398].
Chapter 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.
Chapter XVI. Organs of Vision. Pp. [470]-511.
Cœlenterata, 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. Ammocœte 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].
Chapter 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 Cœlenterata, 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].
Chapter 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].
Chapter 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].
Chapter 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].
Chapter 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].
Chapter 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].
Chapter 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.
Chapter XXIV. Generative Organs and Genital Ducts. Pp. [741]-753.
Generative organs, pp. [741]-748. Porifera, p. [741]. Cœlenterata, 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.
Chapter 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.
CHAPTER 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.
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; soI, soII. 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.
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.
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].
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.
[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.
[2] The protovertebræ of most embryologists will be spoken of as mesoblastic somites.
[3] The details of this process are spoken of below.
[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.
CHAPTER II.
UROCHORDA[5].
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 fœtus, 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.
al. alimentary tract in anterior 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.
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].
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 œsophagus 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 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]).
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. œsophageal 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.
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 œsophagus, 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 œsophagus, 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 œsophagus, 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].
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.
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 œsophagus, 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.
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.
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.
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 fœtal 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].
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].
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].
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.
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.
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].
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 lateralbuds (eventual history unknown). | 2nd asexual forms developed as median buds with vental stolon, | |
| | | ||
| sexual generation. | ||
Bibliography.
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[5] The following classification of the Urochorda is adopted in the present chapter.
I. Caducichordata.
A. Simplicia
Solitaria ex. Ascidia.
Socialia ex. Clavellina.
B. Composita
Sedentaria ex. Botryllus.
Natantia ex. Pyrosoma.
C. Conserta
Salpidæ.
Doliolidæ.
II. Perennichordata.
Ex. Appendicularia.
[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.
[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.
[8] For a fuller account of the organs of sense vide the chapters on the eye and ear.
[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.
[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.
[11] From Todaro’s latest paper (No. [39]) it would seem the segmentation cavity has very peculiar relations.
[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.
[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.
[14] The atrial spaces form somewhat doubtful exceptions to the rule.