The Works of Francis Balfour 2-12
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Foster M. and Sedgwick A. The Works of Francis Balfour Vol. II. A Treatise on Comparative Embryology 1. (1885) MacMillan and Co., London.
- The Ovum and Spermatozoon | The Maturation and Impregnation of the Ovum | The Segmentation of the Ovum | Dicyemae and Orthonectidae Dicyema | Porifera | Coelenterata | Platyhelminthes | Rotifera | Mollusca | Polyzoa | Brachiopoda | Chilopoda | Discophora | Gephyrea | Chaetognatha | Nemathelminthes | Tracheata | Crustacea | Pcecilopoda | Echinodermata | Enteropneusta | Bibliography
The Works of Francis Balfour Foster M. and Sedgwick A. The Works of Francis Balfour Vol. I. Separate Memoirs (1885) MacMillan and Co., London.
Foster M. and Sedgwick A. The Works of Francis Balfour Vol. II. A Treatise on Comparative Embryology 1. (1885) MacMillan and Co., London.
Foster M. and Sedgwick A. The Works of Francis Balfour Vol. III. A Treatise on Comparative Embryology 2 (1885) MacMillan and Co., London.
Foster M. and Sedgwick A. The Works of Francis Balfour Vol. IV. Plates (1885) MacMillan and Co., London.
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Vol II. A Treatise on Comparative Embryology (1885)
Chapter XII. Chaetopoda
Formation of the Germinal Layers.
MOST Chaetopoda deposit their eggs before development. The Oligochaeta lay them in peculiar cocoons or sacks formed by a secretion of the integument. Some marine Polychaeta carry them about during their development. Autolytus cornutus has a special sack on the ventral surface in which they are hatched. In Spirorbis Pagenstecheri they develop inside the opercular tentacle, and in Spirorbis spirillum inside the tube of the parent.
A few forms (e.g. Eunice sanguinea, Syllis vivipara, Nereis diversicolor) are viviparous.
Perhaps the most primitive type of Chaetopod development so far observed is that of Serpula (Stossich, No. 357) 2 . There is a regular segmentation resulting in the formation of a blastosphere with a central segmentation cavity. An invagination of the normal type now ensues. The blastopore soon narrows to become the permanent anus, while the invaginated hypoblast forms a small prominence with an imperfectly developed lumen, which does not nearly fill up the segmentation cavity (fig. 139 A). The embryo, which has in the meantime become completely
1 The following classification of the Chaetopoda is adopted in the present section.
I. Achseta (Polygordius).
ii. Polychseta. j Errantia ill. Oligochgeta.
2 The observations of Stossich are not thoroughly satisfactory.
320 FORMATION OF THE LAYERS.
covered with cilia, now assumes more or less the form of a cone, at the apex of which is the anus, while the base forms the rudiment of a large prae-oral lobe. The alimentary sack grows forwards and then bends upon itself nearly at right angles, and meets a stomodaeal invagination from the ventral side some way from the front end of the body.
The alimentary canal soon differentiates itself into three regions (i) oesophagus, (2) stomach, and (3) intestine. With
FlG. 139. TWO STAGES IN THE DEVELOPMENT OF SfiRPULA. (After StOSsich.)
m. mouth ; an. anus ; al. archenteron.
these changes the larva, which in the meantime becomes hatched, assumes the characters of a typical Annelid larva (fig. 139 B). In front is a large prae-oral lobe, at the sides of which the eyespots soon appear. The primitive segmentation cavity remains as a wide space between the curved alimentary tract and the body walls, and becomes traversed by muscular fibres passing between the two. The original chorion appears to serve as cuticle, and is perforated by the cilia.
The further changes in this larval form do not present features of general importance. A peculiar vesicle, which in anomalous cases is double, is formed near the anus. If it were shewn to occur widely amongst Chaetopoda, it might be perhaps regarded as homologous with the anal vesicles of the Gephyrea.
Serpula is one of the few Chaetopoda at present known in
which the segmentation is quite regular 1 . In other forms it is more or less unequal. The formation of the germinal layers has been far more fully studied in the Oligochaeta than in the Polychaeta, and though unfortunately the development is much abbreviated in the former group, they nevertheless have to serve as our type ; and unless the contrary is indicated the statements in the remainder of the section apply to the Oligochaeta. The segmentation is nearly regular in Lumbricus agricola (Kowalevsky) and results in the formation of a flattened blastosphere, one of the sides of which is hypoblastic and the other epiblastic, the hypoblast cells being easily distinguished from the epiblast cells by their clearer aspect. An invagination takes place, in the course of which the hypoblast becomes enclosed by the epiblast, and a somewhat cylindrical two-layered gastrula is formed. The opening of this gastrula at first extends over the whole of what becomes the ventral surface of the future worm, but gradually narrows to a small pore the permanent mouth near the front end. The central cavity of the gastrula is lined by hypoblast cells, but the oral opening, which leads by a narrow passage into the gastric cavity, is lined by epiblast cells.
The segmentation of Lumbricus trapezoides (Kleinenberg, No. 341), and of Criodrilus (Hatschek, No. 339), is more unequal and more irregular than that of Lumbricus agricola, and there is an invagination which is intermediate between the embolic and epibolic types.
The segmentation of Lumbricus trapezoides is especially remarkable. It is strangely irregular and at one period the segmentation cavity communicates by a pore with the exterior. Before the completion of the gastrula stage the ovum becomes partially divided into two halves, each of which gives rise to a complete embryo. The two embryos are at first united by an epiblast cord which connects their necks (fig. 141 A), but this cord is very early ruptured, and the two embryos then become quite independent. Some of the peculiarities of the segmentation may no doubt be explained by this remarkable embryonic fission.
The gastrula opening in both Lumbricus trapezoides and Criodrilus is placed on the ventral surface, and eventually narrows to form the mouth or possibly (Criodrilus) closes at the position of the mouth. In Lumbricus trapezoides the oral opening is at first lined by hypoblast, and in Criodrilus is bounded anteriorly by three large peculiar epiblast cells, which are
1 According to Willemoes-Suhm, Terebellides stroemii is also characterised by a regular segmentation,
3, II, 21
322 FORMATION OF THE LAYERS.
believed by Hatschek to assist in absorbing the albuminous fluid in which the eggs are suspended. These large cells are eventually covered by the normal epiblast cells and subsequently disappear. In both these types the hypoblast cells undergo, during their invagination, peculiar changes connected with their nutritive function.
In Euaxes (Kowalevsky) the segmentation is far more unequal than in the other types ; a typical epibolic invagination takes place (fig. 140), and the blastopore closes completely along the ventral surface.
In all the oligochaetous types, with the exception of Euaxes, where the blastopore closes completely, the blastopore becomes, or coincides with the mouth. In Serpula it is stated (Stossich), as we have seen, to coincide with the anus : a statement which receives confirmation from the similar statements of Willemoes-Suhm (No. 358). It is necessary either to suppose ^
a mistake on the part of Stossirh or that we have in Chaeto- FlG - l *' TRANSV EKSE SECTION
S1Cn > 01 THROUGH THE OVUM OF EUAXES
pods a case like that of Gas- DURING AN EARLY STAGE OF DEVELOP, . 1-1 f. 1-1 MENT. (After Kowalevsky.)
teropods in which a slit-like ^ epiblast; ms. mesoblastic band; blastopore originally extending h- hypoblast. along the ventral surface may in some forms become reduced to a pore at the oral, or in other forms at the anal extremity.
So far only two germinal layers the epiblast and the hypoblast have been spoken of. Before the invagination of the hypoblast is completed the mesoblast makes its appearance in the form of two bands or streaks, extending longitudinally for the whole length of the embryo. These are usually spoken of as germinal streaks, but to avoid the ambiguity of this term they will be spoken of as mesoblastic bands.
Their origin and growth has been most fully studied by Kleinenberg (No. 341) in Lum. trapezoides. They commence in this species shortly before the gastrula stage as two large cells on the surface of the blastoderm, which may be called mesoblasts. These cells lie one on each side of the median line at the hind end of the embryo. They soon travel inwards and become covered by the epiblast (fig. 141 A, m'\ while on their inner and anterior side a row of small cells appears (ms).
These rows of cells form the commencement of the mesoblastic bands, and in the succeeding stages they extend one on each side of the body (fig. 141 B, ms) till they reach the sides of the mouth. Their forward growth takes place mainly at the expense of the superjacent epiblast cells, but the two mesoblasts
FIG. 141. THREE SECTIONS ILLUSTRATING THE DEVELOPMENT OF LUMBRICUS
TRAPEZOIDES. (After Kleinenberg.) ms. mesoblastic band ; m' . mesoblast ; al. archenteron ; pp. body cavity.
A. Horizontal and longitudinal section of an embryo which is dividing into two embryos at the gastrula stage. It shews the mesoblasts and the mesoblastic bands proceeding from them.
B. Transverse section shewing the two widely-separated mesoblastic bands.
C. Transverse section at a later stage shewing the mesoblastic bands which have approached the ventral line and developed a body cavity^/.
at their hinder extremities probably assist in their growth. Each mesoblastic band is at first composed of only a single row of cells, but soon becomes thicker, first of all in front, and becomes composed of two, three or more rows of cells abreast. From the above it is clear that the mesoblastic bands have, in L. trapezoides at any rate, in a large measure an epiblastic origin.
At first the two bands end in front at the sides of the mouth, but subsequently their front ends grow dorsalwards at the
324 FORMATION OF THE LAYERS.
expense of the adjoining epiblast cells, and meet above the mouth, forming in this way a mesoblastic dorsal commissure.
The mesoblastic bands soon travel from the lateral position, which they at first occupy, towards the ventral surface. They do not however meet ventrally for some time, but form two bands, one on each side of the median ventral line (fig. 141 C).
The usual accounts of the origin and growth of the bands differ somewhat from the above. By Kowalevsky (No. 342) and Hatschek (No. 339) they are believed to increase in Lumbricus rubellus and Criodrilus entirely at the expense of the mesoblasts. Kowalevsky moreover holds that in L. rubellus the original mesoblasts spring from the hypoblast. In some forms, e.g. Lumbricus agricola, the mesoblasts are not present.
In Euaxes the origin of the mesoblast bands is somewhat interesting as illustrating the relation of the Chaetopod mesoblastic bands to the mesoblast of other forms. To render intelligible the origin of the mesoblast in this form, it is necessary to say a few words about the segmentation.
By a somewhat abnormal process of segmentation the ovum divides into four spheres, of which one is larger than the others, and occupies a position corresponding with the future hind end of the embryo. The three smaller spheres give rise on their dorsal side by a kind of budding to small cells, which become the epiblast ; and the epiblast is also partly formed from the hinder large cell in that this cell produces by budding a small cell, which again divides into two. The anterior of the two cells so formed divides still further and becomes incorporated in the epiblast ; the posterior only divides into two which form the two mesoblasts. The remainder of the mesoblast is formed by further division of the three smaller of the primitive large spheres, and at first forms a continuous layer between the dorsal cap of epiblast and the four largest cells which, after giving rise to the epiblast and mesoblast, constitute the hypoblast. As the epiblast spreads over the hypoblast the mesoblastic sheet gives way in the middle, and the mesoblast remains as a ridge of cells at the edge of the epiblastic cup. It forms in fact a thickening of the lips of the blastopore. Behind the thickening is completed by the two mesoblasts. The appearance of the mesoblast in section is shewn in fig. 140. As the epiblast accompanied by the mesoblast grows round the hypoblast, the blastopore assumes an oval form, and the mesoblast appears as two bands forming the sides of the oval. The epiblast travels over the hypoblast more rapidly than the mesoblast, so that when the blastopore becomes closed ventrally the mesoblastic bands are still some little way apart on the ventral side.
In Euaxes the mesoblast originates in a manner which is very similar to that in some of the Gasteropoda, e.g. Nassa, vide p. 234, and Vermes, e.g. Bonellia, etc. As mentioned in the chapter on the
Mollusca the origin of the mesoblast in Planorbis, p. 227, is very similar to that in Lumbricus.
Hatschek has shewn that in Polygordius the mesoblast arises in fundamentally the same way as in the Oligochaeta.
Besides the mesoblast which arises from the mesoblastic bands, there is evidence of the existence of further mesoblast in the larvae of many Polychaeta in the form of muscular fibres which traverse the space between the body wall and the wall of the enteric cavity prior to the formation of the permanent body cavity. These fibres have already been described in the embryo of Serpula, and are probably represented by stellate cells in the cephalic region (pras-oral lobe) of the Oligochaeta. These cells are probably of the same nature as the amoeboid cells in the larvae of Echinodermata, some Mollusca and other types.
The Larval form.
True larval forms are not found in the Oligochaeta where the development is abbreviated. They occur however in the majority of the marine Polychseta.
They present a great variety of characters with variously arranged ciliated bands. Most of these forms can be more or less satisfactorily derived from a larval form, like that of Serpula (fig. 139 B) or Polygordius (fig. 142); and the constant recurrence of this form amongst the Chsetopoda, combined with the fact that it presents many points of resemblance to the larval forms of many Rotifers, Molluscs, and Gephyreans, seems to point to its being a primitive ancestral form for all these groups.
The important characters of this larval form are (i) the division of the body into a large prae-oral lobe and a relatively small post-oral region containing the greater part of the alimentary tract ; (2) the presence of a curved alimentary canal divided into stomodaeum (oesophagus), stomach and intestine, and opening by a ventrally placed mouth, and an anus near the hind end of the body. To these may be added the frequent presence of (i) a ganglion at the apex of the prae-oral lobe, (2) a large cavity between the wall of the gut and the skin, which is the remnant of the segmentation cavity, and is usually traversed by muscular strands, of which one connecting the apex of the prae-oral lobe and the stomach or oesophagus is very commonly present (fig. 142).
The arrangement of the ciliated bands presents great varia
THE LARVAL FORM.
tions, though in some instances it is constant through large groups. In Chaetopods there is a widely distributed prae-oral ciliated band, which is similarly placed to the ring constantly found in the larvae of Molluscs, Rotifers, etc. In many of these forms the band is practically double, the opening of the mouth being placed between its two component rings (vide fig. 142). The best introduction to the study of the Chaetopod larval forms will be the history of the changes of a typical larval form in becoming converted into the adult.
For this purpose no better form can be selected than the interesting larva of Polygordius (vide Agassiz, No. 332, Schneider, No. 352, and Hatschek, No. 339), which was first discovered by Lovdn, and believed by him to be the larva of an ordinary Chaetopod. Its true nature was determined by Schneider.
At a very young stage the larva has the form (fig. 142) of a flattened sphere, with a small conical knob at the posterior extremity.
At the equator are situated two parallel ciliated bands 1 , between which lies the ventrally placed mouth (ni). The more conspicuous ciliated band is formed of a double row of cilia, and is situated in front of the mouth. The thinner ciliated band behind the mouth appears to be absent in the American species.
The mouth leads into an oesophagus, and this into a globular stomach (<?/), which is continuous with a rectum terminating by an anus (an) placed at the hind end of the posterior conical knob. The whole alimentary tract is ciliated. In the American form of larva there is a ring of cilia round the anus, which is developed at a somewhat later stage in the form observed by Hatschek.
The position of the ciliated bands and the alimentary tract enables us to divide the embryo into three regions : a prae-oral region bounded by the anterior ciliated band, a gastric region in which the embryonic stomach is situated, and an abdominal region formed of the posterior conical
FlG. 142. POLYGORDIUS
LARVA. (After Hatschek.)
m. mouth; sg. supra-cesophageal ganglion ; nph. nephridion ; me.p. mesoblastic band ; an. anus ; ol. stomach.
FIG. 143. POLYGORDIUS LARVA . ( From Alex . Agassiz.)
1 These two rings are at first (Hatschek) not quite closed dorsally, calling to mind the early condition of the Echinoderm larva with a prae-oral and post-oral ciliated
FlG. 144. POLYGORDIUS LARVA. (From Alex. Agassiz.)
portion, which by its subsequent elongation gives rise to the whole segmented portion of the future Polygordius.
At the front end of the prae-oral lobe is situated the early formed supracesophageal ganglion (sg) (first noticed by Agassiz) in connection with which is a pair of eyes, and a ramified system of nerves. The ganglion is marked externally by a crown of cilia.
The larval epidermis bears a delicate cuticula, and is separated by a considerable interval from the walls of the alimentary tract. The space between the two represents a provisional body cavity, which is eventually replaced by the permanent body cavity formed between the two layers of the mesoblast. It is doubtful when the replacement takes place in the head. It probably does so very early. The mesoblast is present in the usual form of two bands (me.p] (germinal streaks), which are anteriorly continued into two muscular bands which pass through the embryonic body cavity to the front end of the prae-oral lobe. Another pair of contractile bands passes from the same region of the prse-oral lobe to the oesophagus.
There is no trace of the ventral nerve cord. The most remarkable organ of the larva is a paired excretory organ (npti) discovered by Hatschek. This is a ciliated canal with at first one and subsequently several funnel-shaped openings into the body cavity in front and an external opening behind. It is situated immediately anterior to the lateral band of mesoblast, and is parallel with, and dorsal to, the contractile band which passes off from this. It occupies therefore a position in front of the segmented region of the adult Polygordius.
The changes by which this peculiar larval form reaches the adult condition will be easily gathered from an inspection of figs. 143 148. They consist essentially in the elongation of what has been termed the abdominal region of the body, and the appearance of a segmentation in the mesoblast ; the segments being formed from before backwards, and each fresh segment being interpolated between the anus-bearing end of the body and the last segment.
As the hind portion of the body becomes elongated the stomach extends into it, and gives rise to the mesenteron of the adult (figs. 143, 144, and 145). For a long time the anterior spherical dilated portion of the larva remains very large, consisting of a prae-oral lobe and a post-oral section. The two together may be regarded as constituting the head.
At a comparatively late stage a pair of tentacles arises from the front
FIG. 145. POLYGORDIUS LARVA. (From Alex. Agassiz.)
THE LARVAL FORM.
end of the prae-oral lobe (fig. 146), and finally the head becomes relatively reduced as compared with the body, and gives rise to the simple head of
FIG. 146. POLYGORDIUS LARVA. (From Alex. Agassiz.)
the fully formed worm (fig. 148). The two ciliated bands disappear, the posterior vanishing first. The ciliated band at the hind end of the body also atrophies ; and just in front of it the ring of wart-like prominences used by the adult to attach itself becomes developed.
At the sides of the head there is formed a pair of ciliated pits, also found by Hatschek in the embryo of Criodrilus, and characteristic of many Chaetopod larvae, but persistent in the adult Polygordius, Saccocirrus, Polyophthalmus, etc. They are perhaps the same structures as the ciliated pits in Nemertines.
During the external changes above described, by which the adult form of Polygordius is reached, a series of internal changes also takes place which are for the most part the same as in other Chaetopoda ; and do not require a detailed description. The nervous 1 and muscular systems have precisely the normal development. The division of the mesoblast into somites is not externally indicated. The organs most worthy of notice are the excretory organs.
FIG. 147. POLYGORDIUS LARVA. (From Alex. Agassiz.)
The essential points in the above development of Polygordius are (i) the gradual elongation and corresponding segmentation of the post-cephalic part of the body ; and (2) the relative reduction in size of the prae-oral lobe and its conversion together with the oral region into the head ; (3) the atrophy of the ciliated bands. The conversion of the larva into the adult takes place in fact by the intercalation of a segmented region
1 The structure of the ventral cord in the adult requires further elucidation.
between a large mouth-bearing portion of the primitive body and a small anus-bearing portion 1 .
The general mode of development of Chsetopod larvae is similar to the above except in details, which are however no doubt often of great importance. The history of the larvae may
FIG. 148. POLYGORDIUS LARVA. (From Alex. Agassiz.)
be conveniently treated under three heads, (i) The form of the primitive unsegmented larva; (2) the arrangement of the cilia on the unsegmented larva, and on the larva at later stages ; (3) the character of the metamorphosis and the development of the permanent external organs.
A larva similar to the Polygordius larva with a greatly developed prae-oral lobe is widely distributed amongst the Annelids.
An almost identical form is that of Nepthys scolopendroides (Claparede and Metschnikoff, No. 336) ; that of Phyllodoce (fig. 149) is also very similar, and that of Saccocirrus (Metsch. and Clap. No. 336, PL XIII. fig. i), a very primitive form most nearly related to Polygordius, clearly belongs to the same type. Many other larval forms, such as that of Spio fuliginosus (Metsch. and Clap. No. 336), Terebella, Nerine, etc., also closely approach this form.
FIG. 149. LARVA OF PHYLLODOCE. (From Alex. Agassiz.)
Other really similar forms at first sight appear very different, but this is mainly owing to the fact that their prae-oral lobe never attains a considerable development. Its smallness, though obviously of no deep morphological significance, at once produces a very different appearance in a larva.
1 For Semper's view as to the intercalation of segments in the cephalic region, vide note on p. 333.
THE LARVAL FORM.
A good example of a larval form with a small prae-oral lobe is afforded by Capitella, which is figured by Clap, and Metsch. (No. 336, PI. xvn. fig. 2). The imperfect development of the prae-oral lobe is also generally characteristic of the Oligochasta. The persistence of a relatively large pras-oral lobe for so long a time as in Polygordius is very unusual.
The arrangement of the cilia in Chaetopod larvae has been employed as a means of classifying them. Although a classification so framed has no morphological value, yet the terms themselves which have been invented are convenient. The terms most usually employed are Atrochae, Monotrochae, Telotrochae, Polytrochae, Mesotrochae. The polytrochae may again be subdivided into Polytrochae proper, Nototrochae, Gasterotrochae, and Amphitrochae.
The atrochae contain forms (fig. 139) in which the larva is at first coated by an uniform covering of cilia, which, though it may subsequently disappear from certain areas, does not break up into a series of definite bands.
The monotrochae or cephalotrochae are larvae in which only a single prae-oral ring is developed (fig. 150 B).
In the telotrochae there is present a prae-oral and a postoral, i.e. peri-anal ring (fig. 150 A) ; the latter sometimes having the form of a peri-anal patch.
The polytrochae are segmented larvae with perfect or imperfect rings of cilia on the segments of the body usually one ring to each segment between the two characteristic
FIG. 150. Two CH>ETOPOD LARVAE.
o. mouth ; i. intestine ; a. anus ; v. pne-oral ciliated band ; w. peri-anal ciliated band.
telotrochal rings. When these
rings are complete the larvae
are polytrochae proper, when they are only half rings they are
either nototrochae or gasterotrochae. Sometimes there are both
dorsal and ventral half rings which do not however correspond,
such forms constitute the amphitrochae.
In the mesotrochae one or two rings are present in the middle of the body, and the characteristic telotrochal rings are absent.
Larvae do not necessarily continue to belong to the same group at all ages. A larva may commence as a monotrochal form and then become telotrochal and from this pass into a polytrochal condition, etc.
The atrochal forms are to be regarded as larvae which never pass beyond the primitive stage of uniform ciliation, which in other instances may precede that of definite rings. They usually lose their cilia early, as in the cases of Serpula and other larvae described below.
The atrochal larvae are not common. The following history of an Eunicidan larva (probably Lumbriconereis) from Claparede and Metschnikoff (No. 336) will illustrate their general history.
In the earliest stage noticed the larva has a spherical form, the prae-oral lobe not being very well marked. In the interior is a globular digestive tract. The cilia form a broad central band leaving free a narrow space at the apex of the prae-oral lobe, and also a circumanal space. At the apex of the pras-oral lobe is placed a bunch of long cilia, and a patch of cilia also marks out the anal area.
As the larva grows older it becomes elongated, and the anterior bunch of cilia is absorbed. The alimentary canal divides itself into pharynx and intestine. The former opens (?) by the mouth in the middle of the central band of cilia, the latter in the anal patch. The setae indicating the segmentation are formed successively in the posterior ring-like area free from cilia. The cilia disappear after the formation of two segments.
In Lumbricus, the embryo of which ought perhaps to be grouped with the atrochae, the cilia (Kleinenberg) cover a ventral tract of epiblast between the two mesoblastic cords, and are continued anteriorly to form a circle round the mouth.
The monotrochal larvae are provided only with the important prae-oral ciliated ring before mentioned. In the majority of cases they are transitional forms destined very shortly to become telotrochal, and in such instances they usually have a more or less spherical body which is nearly divided into two equal halves by a ciliated ring. In some few instances, such as Polynoe, Dasychone, etc., the monotrochal characters are not lost till the larval cilia are exuviated.
The telotrochal forms (of which examples are shewn in figs. 144, 150, etc.) may (i) start as monotrochal; or (2) from the first have a telotrochal character ; or (3) be derived from atrochal forms. The last mode of origin probably represents the ancestral one.
332 LARVAL FORMS.
Their mode of development is well illustrated by the case of Terebella nebulosa (vide Milne-Edwards, No. 347). The embryo is at first a nearly spherical ciliated mass. One end slightly elongates and becomes free from cilia, and, acquiring dorsally two eye-spots, constitutes a prse-oral lobe. The elongation continues at the opposite end, and near this is formed a narrow area free from cilia. The larva now has the same characters as the atrochal Eunicidan larva described above. It consists of a non-ciliated prae-oral lobe, followed by a wide ciliated band, behind which is a ring-like area free from cilia ; and behind this again a peri-anal patch of cilia. The ring-like area free from cilia is, as in the Eunicidan larva, the region which becomes segmented. It soon becomes longer, and is then divided into two segments ; a third and fourth etc. non-ciliated segment becomes successively interposed immediately in front of the peri-anal patch ; and, after a certain number of segments have become formed, there appear on some of the hinder of them short tubercles, provided with single setae (the notopodia), which are formed from before backwards, like the segments.
The mouth, anus, and intestine become in the meantime clearly visible. The mouth is on the posterior side of the ciliated band, and the anus in the centre of the peri-anal patch.
The ciliated band in front now becomes contracted and provided with long cilia. It passes below completely in front of the mouth, and constitutes, in fact, a well-marked pras-oral ring, while the cilia behind constitute an equally marked peri-anal ring. The larva has in fact now acquired all the characters of a true telotrochal form.
Only a comparatively small number of Chsetopod larvae remain permanently telotrochal. Of these Terebella nebulosa, already cited (though not Terebella conchilega), is one ; Polygordius, Saccocirrus and Capitella are other examples of the same, though in the latter form the whole ventral surface becomes ciliated.
The majority of the originally telotrochal forms become polytrochal.
In most cases the ciliated rings or half rings of the polytrochal forms are placed at equal distances, one for each segment. They are especially prominent in surface-swimming larvae, and are in rare cases preserved in the adult. In some instances (e.g. Nerine and Spio) the ventral half rings, instead of being segmentally arranged, are somewhat irregularly distributed amongst the segments, so that there does not seem to be a necessary correspondence between the ciliated rings and the segments. This is further shewn by the fact that the ciliated rings are not precursors of the true segmentation, but are
developed after the establishment of the segments, and thus seem rather to be secondarily adapted to the segments than primarily indicative of them.
In most Polytrochae the rings are incomplete, so that they fall under the category of Nototrochae or Gasterotrochae.
The larva of Odontosyllis is an example of the former, and that of Magelona of the latter. The larvae of Nerine and Spio, already quoted as examples of an unsegmented arrangement of the ventral ciliated half rings, are both amphitrochal forms.
As an example of a polytrochal form with complete ciliated rings Ophryotrocha puerilis may be cited. This form, discovered by Claparede and Metschnikoff, develops a complete ciliated ring on each segment : and the prae-oral ring, though at first single, becomes at a later period divided into two. This form is further exceptional in that the ciliated rings are persistent in the adult.
The unimportance of the character of the rings in the polytrochal forms is shewn by such facts as the absence of these rings in Terebella nebulosa and the presence of dorsal half rings in Terebella conchilega.
The mesotrochal forms are the rarest of Chaetopod larvae, and would seem to be confined to the Chaetopteridae.
Their most striking character is the presence of one or two complete ciliated rings which girth the body between the mouth and anus. The whole body is further covered with short cilia. The anus has a distinct dorsal situation, while on its ventral side there projects backwards a peculiar papilla.
The total absence of the typical prae-oral and of the peri-anal bands separates the mesotrochal larvae very sharply from all the previous types.
A characteristic of many Chaetopod larvae is the presence of a bunch of cilia or a single flagellum at the apex of the prae-oral lobe. The presence of such a structure is characteristic of the larval forms of many other groups, Turbellarians, Nemertines, Molluscs, etc.
In the preceding section the mode of multiplication of the segments has already been sufficiently described 1 .
1 It has been insisted by Semper (No. 355) that certain of the anterior segments, belonging to what he regards as the head region in opposition to the trunk, become interpolated between the trunk and the head. The general evidence, founded on observations of budding, which he brings forward, cannot be discussed here. But the special instance which he cites (founded on Milne-Edwards's (No. 347) observations)
FIG. 151. LARVA OF PHYLLODOCE FROM THE
VENTRAL SIDE. (From
Apart from the formation of the segments the larval metamorphosis consists in the atrophy of the provisional ciliated rings and other provisional organs, and in the acquirement of the organs of the adult.
The great variations in the nature of the Chaetopod appendages render it impossible to treat this part of the developmental history of the Chaetopoda in a systematic way.
The mode of development of the appendages is not constant, so that it is difficult to draw conclusions as to the primitive form from which the existing types of appendages are derived.
In a large number of cases the primitive rudiments of the feet exhibit no indication of a division into notopodium and neuropodium ; while in other instances (e.g. Terebella and Nerine, fig. 152) the notopodium is first developed, and subsequently the neuropodium quite independently.
In many cases the setae appear before there are any other visible rudiments of the feet (e.g. Lumbriconereis) ; while in other cases the reverse holds good. The gills arc usually the last parts to appear.
Not only does the mode of development of the feet differ greatly in different types, but also the period. The appearance of setae may afford the first external indication of segmentation, or the rudiments of the feet may not appear till a large number of segments are definitely established.
A very considerable number of Chaetopod larvae are provided with very long provisional setae (figs. 152 and 153). These setae
of the interpolation of the head segments, bearing the gills, in Terebella appears to me quite unjustified from Milne-Edwards's own statements ; and is clearly shewn to be unfounded by the careful observations of Claparede on Ter. conchilega, where the segments in question are demonstrated to be present from the first.
FIG. 152. LARVA OF NERINE,
WITH PROVISIONAL SET>E. (From
are usually placed at the sides of the anterior part of the body, immediately behind the head, and also sometimes on the posterior parts of the body. In some instances (e.g. fig. 153)
FIG. 153. EMRRYO CH^ETOPOU WITH PROVISIONAL SEIVE. (From Agassiz.)
they form the only appendages of the trunk. Alex. Agassiz .has pointed out that setae of this kind, though not found in existing Chaetopods, are characteristic of the fossil forms. Setae of this kind are found in chaetopod-like larvae of some Brachiopods (Argiope, fig. 136).
It is tempting to suppose that the long provisional bristles springing from the oral region are the setiform appendages handed down from the unsegmented ancestors of the existing Chaetopod forms. Claparede has divided Chaetopod larvae into two great groups of Metachaetae and Perennichaetae, according as they possess or are without provisional setae.
With reference to the head and its appendages it has already been stated that the head is primarily formed of the prae-oral lobe and of the peristomial region.
The embryological facts are opposed to the view that the prae-oral region either represents a segment or is composed of segments equivalent to those of the trunk. The embryonic peristomial region may, on the other hand, be regarded as in a certain sense the first segment. Its exact relations to the succeeding segments become frequently more or less modified in the adult. The prae-oral region is in most larvae bounded behind by the ciliated ring already described. On the dorsal part of the prae-oral lobe in front of this ring are placed the eyes, and from it there may spring a variable number of processes which form antennae or cephalic tentacles. The number and position of these latter are very variable. They appear as simple processes, sometimes arising in pairs, and at
336 LARVAL FORMS.
other times alternating on the two sides. There is frequently a median unpaired tentacle.
The development of the median tentacle in Terebella, where there is in the adult a great number of similar tentacles, is sufficiently remarkable to deserve special notice ; vide Milne-Edwards, Claparede, etc. It arises long before any of the other tentacles as a single anterior prolongation of the prae-oral lobe containing a parenchymatous cavity, which communicates freely with the general perivisceral cavity. It soon becomes partially constricted off at its base from the procephalic lobe, but continues to grow till it becomes fully half as long as the remainder of the body. A very characteristic figure of the larva at this stage is given by Claparede and Metschnikoff, PI. XVII., Fig. I E. It now strikingly resembles the larval proboscis of Balanoglossus, and it is not easy to avoid the conclusion that they are homologous structures.
Another peculiar cephalic structure which deserves notice is the gill apparatus of the Serpulidae.
In Dasychone (Sabella) the gill apparatus arises (Claparede and Metschnikoff, No. 336) as a pair of membranous wing-like organs on the dorsal side of the prae-oral lobe immediately in front of the ciliated ring. Each subsequently becomes divided into two rays, and new rays then begin to sprout on the ventral side of the two pairs already present. A cartilaginous axis soon becomes formed in these rays, and after this is formed fresh rays sprout irregularly from the cartilaginous skeleton.
In Spirorbis spirillum as observed by Alex. Agassiz, the right gill-tentacle (fig. 154, /) first appears, and then the left, and subsequently the odd opercular tentacle which covers the right original tentacle. FIG. 154. LARVA OF SPIROR The third and fourth tentacles are formed BIS. (From Alex. Agassiz.) successively on the two sides, and rapidly The first odd tentacle (t) is shewn
become branched in the succeeding stages. on J\?e ht , side Behind the prse-oral ciliated ring
With reference to the sense
organs it may be noted that the eyes, or at any rate the cephalic pigment spots, are generally more numerous in the embryo than in the adult, and that they are usually present in the larvae of the Sedentaria, though absent in the adults of these forms. The Sedentaria thus pass through a larval stage in which they resemble the Errantia.
Paired auditory vesicles of a provisional character have been found on the ventral side of the body, in the fourth segment
behind the mouth, in the larva of Terebella conchilega (Claparede).
Mitraria. A peculiar larval Ch?etopod form known as Mitraria, the metamorphosis of which was first worked out by Metschnikoff, deserves a special notice.
This form (fig. 155 A) in spite of its remarkable appearance can easily be reduced to the normal type of larva.
The mouth (m) and anus (an) (fig. 155 A) are closely approximated, and situated within a vestibule the edge of which is lined by a simple or lobed ciliated ring. The shape of the body is somewhat conical. The cavity of
FlG. 155. TWO STAGES IN THE DEVELOPMENT OF MlTRARIA.
m. mouth; an. anus; sg. supra-oesophageal ganglion; br. provisional bristles; pr.b. prse-oral ciliated band.
the vestibule forms the base of the cone, and at the apex is placed a ciliated patch (sg). A pair of lobes (br) bear provisional setae. The alimentary canal is formed of the three normal parts, oesophagus, stomach, and intestine.
To compare this larva with an ordinary Chsetopod larva one must suppose that the alimentary canal is abnormally bent, so that the post-oral ventral surface is reduced to the small space between the mouth and the anus. The ciliated band surrounding the vestibule is merely the usual prae-oral band, borne on the very much extended edge of the pras-oral lobe. The apex of the larva is the front end of the pras-oral lobe with the usual ciliated patch. The two lobes with provisional bristles are really dorsal and not posterior.
338 FORMATION OF ORGANS.
The correctness of the above interpretation is clearly shewn by the metamorphosis.
The first change consists in the pushing in of a fold of skin, between the mouth and anus, towards the intestine, which at the same time rapidly elongates, and forms the axis of a conical projection, which thereupon becomes segmented and is thereby shewn to be the rudiment of the trunk (fig. 155 B). On the elongation of the trunk in this way the prae-oral lobe and its ciliated ring assume an appearance not very dissimilar to the same structures in Polygordius. At the ciliated apex of the prae-oral lobe a paired thickening of epiblast gives rise to the supra-cesophageal ganglia (sg). In the further metamorphosis, the prae-oral lobe and its ciliated ring gradually become reduced, and finally atrophy in the normal way, while the trunk elongates and acquires setae. The dorsally situated processes with provisional setae last for some time, but finally disappear. The young worm then develops a tube and shews itself as a normal tubicolous Chaetopod.
Formation of Organs.
Except in the case of a few organs our knowledge of the formation of the organs in the Chaetopoda is derived from investigations on the Oligochaeta.
The embryo of the Oligochaeta. has a more or less spherical form, but it soon elongates, and becoming segmented acquires a distinct vermiform character. The ventral surface is however for a considerable time markedly convex as compared to the dorsal.
The ventrally placed mouth is surrounded by a well-marked lip, and in front of it is placed a small prae-oral lobe.
The epiblast. The epiblast cells at the commencement of the gastrula stage become much flattened, and on the completion of the invagination form an investment of flattened cells, only thickened in the neighbourhood of the mesoblastic bands (fig. 141 B and C). In the Polychaeta at any rate the statements of several investigators would seem to in dicate that the cuticle is derived from the FJG i 6 SFCTION chorion. It is difficult to accept this THROUGH THE HEAD OF A
conclusion, but it deserves further in VCStigation. Kleinenberg. )
Nervous system. The most im- '-& cephalic ganglion;
, .. cc. cephalic portion of the
portant organ derived from the epiblast body cavity ; x. cesophagus.
FIG. 157. SECTION THROUGH PART
OF THE VENTRAL WALL OF THE TRUNK OF AN EMBRYO OF LUMBRI
is the nervous system ; the origin of which from this layer was first established by Kowalevsky (No. 342).
It arises 1 (Kleinenberg, No. 341) from two at first quite distinct structures, viz. (i) the supra-cesophageal rudiment and (2) the rudiment of the ventral cord. The former of these takes its origin as an unpaired dorsal thickening of the epiblast at the front end of the head (fig. 1 56, e.g.], which sends two prolongations downwards and backwards to meet the ventral cord. The latter arises as two independent thickenings of the epiblast, one on each side of the ventral furrow (fig. 157, Vg]. These soon unite underneath the furrow, in the median line, and after being differentiated into segmentally arranged ganglionic and interganglionic regions become separated from the epiblast. Both the supra-cesophageal and ventral cord become surrounded by a us TRAPEZOIDES. (After Kleinen berg.)
layer of somatic mesoblast. The Mm longitudinal muscles . S0m so .
junction between the tWO parts of matic mesoblast ; sp. splanchnic me! i . ' i soblast; hy. hypoblast ; Vg. ventral
the central nervous System takes nerve cord ; w. ventral vessel.
place comparatively late.
The mesoblast. It is to Kowalevsky (No. 342) and Kleinenberg (No. 341) that we mainly owe our knowledge of the history of the mesoblast. The fundamental processes which take place are (i) the splitting of the mesoblast into splanchnic and somatic layers with the body cavity between them, (2) the transverse division of the mesoblast of the trunk into distinct somites.
The former process commences in the cephalic mesoblastic commissure, where it results in the formation of a pair of cavities each with a thin somatic and thick splanchnic layer (fig. 156, cc) ; and thence extends gradually backwards into the trunk (fig. 141 C, //). In the trunk however the division into somites precedes the horizontal splitting of the mesoblast. The former process commences when the mesoblastic bands form widish columns quite separate from each other. These columns become
1 For further details, vide general chapter on Nervous System.
340 FORMATION OF ORGANS.
broken up successively from before backwards into somewhat cubical bodies, in the centre of which a cavity soon appears. The cavity in each somite is obviously bounded by four walls, (i) an outer, the somatic, which is the thickest; (2) an inner, the splanchnic ; and (3, 4) an anterior and posterior. The adjoining anterior and posterior walls of successive somites unite together to form the transverse dissepiments of the adult, which subsequently become very thin and are perforated in numerous places, thus placing in communication the separate compartments of the body cavity. The somites, though at first confined to a small area on the ventral side, gradually extend so as to meet their fellows above and below and form complete rings (fig. 157) of which the splanchnic layer (sp) attaches itself to the enteric wall and the somatic (so) to the epiblast. In Polygordius and probably also Saccocirrus and other forms the cavities of the somites of the two sides do not coalesce ; and the walls which separate them constitute dorsal and ventral mesenteries. The two cavities in the cephalic commissure unite dorsally, but ventrally open into the first somite of the trunk.
The mesoblastic masses of the head are probably not to be regarded as forming a pair of somites equivalent to those in the trunk, but as forming the mesoblastic part of the pras-oral lobe, of which so much has been said in the preceding pages. Kleinenberg's observations are however of great importance as shewing that the cephalic cavities are simply an anterior part of the true body cavity.
The splanchnic layer of the head cavity gives rise to the musculature of the oesophagus.
The somatic layer of the trunk somites becomes converted into the musculature of the body wall and the external peritoneal layer of body cavity. The first part of the muscular system to be definitely formed is the ventral band of longitudinal muscles which arises on each side of the nervous system in contact with the epidermis (fig. 157, m). How the circular muscles become subsequently formed outside these muscles has not been made out.
The splanchnic layer of the trunk somites gives rise to the muscular and connective-tissue wall of the mcscntcron, and also to the walls of the vascular trunks. The ventral vessel is first formed (Kowalevsky) as a solid mass of cells which subsequently
becomes hollowed out. The dorsal vessel in Lumbricus and Criodrilus is stated by Kowalevsky and Vejdovsky to be formed by the coalescence of two lateral vessels ; a peculiarity which is probably to be explained by the late extension of the mesoblast into the dorsal region.
The layer from which the sacks for the setae and the segmental organs spring is still doubtful. The sacks for the setae are believed by Kowalevsky (No. 342) to be epiblastic invaginations, but are stated by Hatschek (No. 339) to be mesoblastic products. For the development of the segmental organs the reader is referred to the chapter on the excretory system.
In marine Polychaeta the generative organs are no doubt mesoblastic products, as they usually spring from the peritoneal epithelium, especially the parts of it covering the vascular trunks.
The Alimentary Canal, In Lumbricus the enteric cavity is formed during the gastrula stage. In Criodrilus the hypoblast has at first no lumen, but this becomes very soon established. In Euaxes on the other hand, where there is a true epibolic gastrula, the mesenteron is at first represented by a solid mass of yolk (i.e. hypoblastj cells. As the central amongst these become absorbed a cavity is formed. The protoplasm of the yolk cells which line this cavity unites into a continuous polynuclear layer containing at intervals masses of yolk. These masses become gradually absorbed, and the protoplasmic wall of the mesenteron then breaks up into a cylindrical glandular epithelium similar to that of the other types.
In Lumbricus and Criodrilus the blastopore remains as the mouth, but in Euaxes a new mouth or rather stomodaeum is formed by an epiblastic invagination between the front end of the two mesoblastic bands. This epiblastic invagination forms the permanent oesophagus; and in Lumbricus trapezoides and Criodrilus, where the oral opening is at first lined by hypoblast, the epiblast soon becomes inflected so as to line the cesophageal region. The splanchnic mesoblast of the cephalic region subsequently invests the oesophagus, and some of its cells penetrating between the adjoining epiblast cells give rise to a thick wall for this part of the alimentary tract ; the original epiblast cells being reduced to a thin membrane. This mesoblastic wall is sharply
342 ALTERNATIONS OF GENERATIONS.
separated from the muscular wall outside, which is also formed of splanchnic mesoblast.
The anus is a late formation.
Alternations of generations.
Amongst Chaetopoda a considerable number of forms exhibit the phenomenon of alternations of generations, which in the same general way as in the case of the Ccelenterata, is secondarily caused by budding or fission.
The process of fission essentially consists in the division of a parent form into two zooids by the formation of a zone of fission between two old rings, which becomes differentiated (i) into an anal zone in front which forms the anal region of the anterior zooid, and (2) into a cephalic zone behind which forms the head and some of the succeeding segments of the posterior zooid. The anal zone is capable, by growth and successive segmentation, of giving rise to an indefinite number of fresh segments.
In Protula Dysteri, as shewn by Huxley, there is a simple fission into two in the way described. Sexual reproduction does not take place at the same time as reproduction by fission, but both zooids produced are quite similar and multiply sexually.
In the freshwater forms Nais and Chaetogaster a more or less similar phenomenon takes place. By a continual process of growth in the anal zones, and the formation of fresh zones of fission whenever four or five segments are added in front of an anal zone, complicated chains of adhering zooids are produced, each with a small number of segments. As long as the process of fission continues sexual products are not developed, but eventually the chains break up, the individuals derived from them cease to go on budding, and, after developing a considerably greater number of segments than in the asexual state, reproduce themselves sexually. The forms developed from the ovum then repeat again the phenomenon of budding, etc., and so the cycle is continued 1 .
The phenomena so far can hardly be described as cases of
1 Reproduction by budding and formation of the sexual products to some extent overlap.
alternation of generations. The process is however in certain types further differentiated. In Syllis (Quatrefages) fission takes place, the parent form dividing into two, of which only the posterior after its detachment develops sexual organs. The anterior asexual zooid continues to produce fresh sexual zooids by fission. In Myrianida also, where a chain of zooids is formed, the sexual elements seem to be confined to the individuals produced by budding.
The cases of Syllis and Myrianida seem to be genuine examples of alternations of generations, but a still better instance is afforded by Autolytus (Krohn, No. 343, and Agassiz, No. 333).
In Autolytus cornutus the parent stock, produced directly from the egg, acquires about 40 45 segments, and then gives rise by fission, with the production of a zone of fission between about the I3th and I4th rings, to a fresh zooid behind. This after becoming fully developed into either a male or a female is detached from the parent stock, from which it very markedly differs. The males and females are moreover very different from each other. In the female zooid the eggs are carried into a kind of pouch where they undergo their development and give rise to asexual parent stocks. After the young are hatched the female dies. The asexual stock, after budding off one asexual zooid, elongates again and buds off a second zooid. It never develops generative organs.
The life history of some species of the genus Nereis presents certain very striking peculiarities which have not yet been completely elucidated.
As was first shewn by Malmgren asexual examples of various species of Nereis may acquire the characters of Heteronereis and become sexually mature.
The metamorphosis of Nereis Dumerilii has been investigated by Claparede, who has arrived at certain very remarkable conclusions. He finds that there are two distinct sexual generations of the Nereis form of this species, and two distinct sexual generations of the Heteronereis form.
One sexual Nereis, characterized by its small size, is dioecious, the other discovered by Metschnikoff is hermaphrodite.
Of the Heteronereis sexual forms, both are dioecious, one is small, and swims on the surface, the other is larger and lives at the bottom.
How these various generations are mutually related has not been made out ; but Claparede traced the passage of large asexual examples of the Nereis form into the large Heteronereis form.
(332) Alex. Agassiz. "On the young stages of a few Annelid.^." Annuls Lyceum Nat. Hist, of New York, Vol. vin. 1866.
(333) Alex. Agassiz. " On the embr}'ology of Autolytus cornutus and alternations of generations, etc." Boston Journal of Nat. History, Vol. VII. 1859 63.
(334) W. Busch. Beobachtnngcn ii. Anat. u. Entwick. einiger wirbel loser Seethiere, 1851.
(335) Ed. Claparede. Beobachlungen ii. Anat. it. Entwick. wirbelloser Thiere an d. Kiiste von Normandie. Leipzig, 1863.
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(344) R. Leuckart. " Ueb. d. Jugendzustande ein. Anneliden, etc." Archiv f. Naturgesch. 1855.
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