III. THE SEGMENTATION OF THE OVUM
The immediate result of the fusion of the male and female pronucleus is the segmentation or division of the ovum usually into two, four, eight, etc. successive parts. The segmentation may be dealt with from two points of view, viz. (1) the nature of the vital phenomena which take place in the ovum during its occurrence, which may be described as the internal phenomena of segmentation. (2) The external characters of the segmentation.
Internal Phenomena of Segmentation.
Numerous descriptions have been given during the last few years of the internal phenomena of segmentation. The most recent contribution on this head is that of Fol (No. 87). He appears to have been more successful than other observers in obtaining a complete history of the changes which take place, and it will therefore be convenient to take as type the ovum of Toxopneustes (Echinus) lividus, on which he made his most complete series of observations. The changes which take place may be divided into a series of stages. The ovum immediately after the fusion of the male and female pronucleus contains a central segmentation nucleus.
In the first stage a clear protoplasmic layer derived from the plasma of the cell is formed round the nucleus, from which there start outwards a number of radial striæ, which are rendered conspicuous by the radial arrangement of the yolk granules between them. The nucleus during this process remains perfectly passive.
In the second stage the nucleus becomes less distinct and somewhat elongated, and around it the protoplasmic layer of the earlier stage is arranged in the form of a disc-shaped ring, compared by Fol to Saturn's ring. The protoplasmic rays still take their origin from the perinuclear protoplasm. This stage has a considerable duration (20 minutes).
In the third stage the protoplasm around the nucleus becomes transported to the two nuclear poles, at each of which it forms a clear mass surrounded by a star-shaped figure formed by radial striæ. The nucleus is hardly visible in the fresh condition, but when brought into view by reagents is found to contain many highly refractive particles, and to be still enveloped in a membrane.
In the fourth stage the nucleus when treated by reagents has assumed the well-known spindle form. The striæ of which it is composed are continuous from one end of the spindle to the other and are thickened at the centre. The central thickenings constitute the so-called nuclear plate. The clear protoplasmic masses and stars are present as before at the apices of the nucleus, and the rays of the latter converge as if they would meet at the centre of the clear masses, but stop short at their periphery. There is no trace of a membrane round either the nuclear spindle or the clear masses; and in the centre of the latter is a collection of granules. The striæ of the polar stars are very fine but distinct.
Between the stage with a completely formed spindle and the previous one the intermediate steps have not been made out for Toxopneustes; but for Heteropods Fol has been able to demonstrate that the striæ of the spindle and their central thickenings are formed, as in the case of the spindle derived from the germinal vesicle, from the metamorphosis of the nuclear reticulum. They commence to be formed at the two poles, and are then (in Heteropods) in immediate contiguity with the striæ of the stars. The striæ gradually grow towards the centre of the nucleus and there meet.
In the fifth stage the central thickenings of the spindle separate into two sets, which travel symmetrically outwards towards the clear masses, growing in size during the process. They remain however united for a short time by delicate filaments--named by Fol connective filaments--which very soon disappear. The clear masses also increase in size. During this stage the protoplasm of the ovum exhibits active amoeboid movements preparatory to division.
In the sixth stage, which commences when the central thickenings of the spindle have reached the clear polar masses, the division of the ovum into two parts is effected by an equatorial constriction at right angles to the long axis of the nucleus. The inner vitelline membrane follows the furrow for a certain distance, but does not divide with the ovum. All connection between the two parts of the spindle becomes lost during this stage, and the thickenings of the fibres of the spindle give rise to a number of spherical vesicular bodies, which pass into the clear masses and become intermingled with the granules which are placed there. The radii of the stars now extend round the whole circumference of each of the clear masses.
In the seventh stage the two clear masses become elongated and travel towards the outer sides of their segments; while the radii connected with them become somewhat bent, as if a certain amount of traction had been exercised on them in the movement of the clear masses. Shortly afterwards the spherical vesicles, each of which appears like a small nucleus and contains a central nucleolus, begin to unite amongst themselves, and to coalesce with the neighbouring granules. Those in each segment finally unite to form a nucleus which absorbs the substance of the clear mass. The new nucleus is therefore partly derived from the division of the old one and partly from the plasma of the cell. The two segments formed by division are at first spherical, but soon become flattened against each other. In each subsequent division of these cells the whole of the above changes are repeated.
The phenomena which have just been described would appear to occur in the segmentation of ova with remarkable constancy and without any very considerable variations.
The division of the ovum constitutes a special case of cell division, and it is important to determine to what extent the phenomena of ordinary cell division are related to those which take place in the division of the ovum. Without attempting a full discussion of the subject I will confine myself to a few remarks suggested by the observations of Flemming, Peremeschko and Klein. The observations of these authors shew that in the course of the division of nuclei in the salamander, newt, etc. the nuclear reticulum undergoes a series of peculiar changes of form, and after the membrane of the nucleus has vanished divides into two masses. The masses form the basis for the new nuclei, and become reconverted into an ordinary nuclear reticulum after repeating, in the reverse order, the changes of form undergone by the reticulum previous to its division.
It is clear without further explanation that the conversion of the nuclear reticulum of the segmentation nucleus into the striæ of the spindle is a special case of the same phenomenon as that first described by Flemming in the salamander. There are however some considerable differences. In the first place the fibres in the salamander do not, according to Flemming, unite in the middle line, though they appear to do so in the newt. This clearly cannot be regarded as a fact of great importance; nor can the existence of the central thickenings of the striæ (nuclear plate), constant as it is for the division of the nucleus of the ovum, be considered as constituting a fundamental difference between the two cases. More important is the fact that the striæ in the case of the ovum do not appear, at any rate have not been shewn, to form themselves again into a nuclear network.
With reference to the last point it is however to be borne in mind (1) that the gradual travelling outwards of the two halves of the nuclear plate is up to a certain point a repetition, in the reverse order, of the mode of formation of the striæ of the spindle, since the striæ first appeared at the poles and gradually grew towards the middle of the spindle; (2) that there is still considerable doubt as to how the vesicular bodies formed out of the nuclear plate reconstitute themselves into a nucleus.
The layer of clear protoplasm around the nucleus during its division has its homologue in the case of the division of the nuclei of the salamander, and the rays starting from this are also found. Klein has suggested that the extra-nuclear rays of the stars around the poles of the nucleus are derived from a metamorphosis of the extra-nuclear reticulum, which he believes to be continuous with the intra-nuclear reticulum.
The delicate connective filaments usually visible between the two halves of the nuclear plate would seem from Strasburger's latest observations (No. 104) to be derived from the nuclear substance between the striæ of the spindle, and to become eventually reabsorbed into the newly-formed nuclei.
We are it appears to me still in complete ignorance as to the physical causes of segmentation. The view that the nucleus is a single centre of attraction, and that by its division the centre of attraction becomes double and thereby causes division, appears to be quite untenable. The description already given of the phenomena of segmentation is in itself sufficient to refute this view. Nor is it in the least proved by the fact (shewn by Hallez) that the plane of division of the cell always bears a definite relation to the direction of the axis of the nucleus.
The arguments by which Kleinenberg (93) attempted to demonstrate that cell division was a phenomenon caused by alterations in the molecular cohesion of the protoplasm of the ovum still in my opinion hold good, but recent discoveries as to the changes which take place in the nucleus during division probably indicate that the molecular changes which take place in the cohesion of the protoplasm are closely related to, and possibly caused by, those in the nucleus. These alterations of cohesion are produced by a series of molecular changes, the external indications of which are to be found in the visible alterations in the constitution of the body of the cell and of the nucleus prior to division.
BIBLIOGRAPHY.
In addition to the papers cited in the last Chapter, vide
(101) W. Flemming. "Beiträge z. Kenntniss d. Zelle u. ihrer Lebenserscheinungen." Archiv f. mikr. Anat., Vol. XVI., 1878.
(102) E. Klein. "Observations on the glandular epithelium and division of nuclei in the skin of the Newt." Quart. J. of Micr. Science, Vol. XIX., 1879.
(103) Peremeschko. "Ueber d. Theilung d. thierischen Zellen." Archiv f. mikr. Anat., Vol. XVI., 1878.
(104) E. Strasburger. "Ueber ein z. Demonstration geeignetes Zelltheilungs-Object." Sitz. d. Jenaischen Gesell. f. Med. u. Naturwiss., July 18, 1879.
External Features of Segmentation.
[FIG. 38. VARIOUS STAGES IN PROCESS OF SEGMENTATION. (After Gegenbaur.)]
In the simplest known type of segmentation the ovum first of all divides into two, then four, eight, sixteen, thirty-two, sixty-four, etc. cells (fig. 38). These cells so long as they are fairly large are usually known as segments or spheres. At the close of such a simple segmentation the ovum becomes converted into a sphere composed of segments of a uniform size. These segments usually form a wall (fig. 39, E), one row of cells thick, round a central cavity, which is known as the segmentation cavity or cavity of Von Baer. Such a sphere is known as a blastosphere. The central cavity usually appears very early in the segmentation, in many cases when only four segments are present (fig. 39, B).
[FIG. 39. THE SEGMENTATION OF AMPHIOXUX. (Copied from Kowalevsky.)
sg. segmentation cavity. A. Stage with two equal segments. 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.]
In other instances, which however are rarer than those in which a segmentation cavity is present, there is no trace of a central cavity, and the sphere at the close of segmentation is quite solid. In such instances the solid sphere is known as a morula. It is found in some Sponges, many Coelenterata, some Nemertines, etc., and in Mammals; in which group the segmentation is not however quite regular. All intermediate conditions between a large segmentation cavity, and a very minute central cavity which may be surrounded by more than a single row of cells have been described.
The segmentation cavity has occasionally, as in Sycandra, the Ctenophora and Amphioxus, the form of an axial perforation of the ovum open at both extremities.
When the process of regular segmentation is examined somewhat more in detail it is found to follow as a rule a rather definite rhythm. The ovum is first divided in a plane which may be called vertical, into two equal parts (fig. 39, A). This division is followed by a second, also in a vertical plane, but at right angles to the first plane, and by it each of the previous segments is halved (fig. 39, B.) In the third segmentation the plane of division is horizontal or equatorial and divides each of the four segments into two halves, making eight segments in all (fig. 39, C). In the fourth period the segmentation takes place in two vertical planes each at an angle of 45° with one of the previous vertical planes. All the segments are thus again divided into two equal parts. In the fifth period there are two equatorial planes one on each side of the original equatorial plane, and thirty-two spheres are present at the close of this period. Sixty-four segments are formed at the sixth period, but beyond the fourth and fifth periods the original regularity is not usually preserved.
In many instances the type of segmentation just described cannot be distinctly recognized. All that can be noticed is that at each fresh segmentation every segment becomes divided into two equal parts. It is not absolutely certain that there is not always some slight inequality in the segments formed, by which, what are known as the animal and vegetative poles of the ovum, can very early be distinguished. A regular segmentation is found in species in most groups of the animal kingdom. It is very common in Sponges and Coelenterates. Though less common so far as is known amongst the Vermes, it is yet found in many of the lower types, viz. Nematoidea, Gordiacea, Trematoda, Nemertea (apparently as a rule), Sagitta, Chætonotus, some Gephyrea (Phoronis); though not usual it occurs amongst Chætopoda, E.G. SERPULA. It is the usual type of segmentation amongst the Echinodermata. Amongst the Crustacea it appears (for the earlier phases of segmentation at any rate) not infrequently amongst the lower forms, and even occurs amongst the Amphipoda (Phronima). It is however very rare amongst the Tracheata, Podura affording the one example of it known to me. It is almost as rare amongst Mollusca as amongst the Tracheata, but occurs in Chiton and is nearly approached in some Nudibranchiata. In Vertebrata it is most nearly approached in Amphioxus[36].
[36] In the Rabbit and probably other Monodelphous Mammalia the segmentation is nearly though not quite regular.
Most of the eggs which have a perfectly regular segmentation are of a very insignificant size and rarely contain much food-yolk: in the vast majority of eggs there is present however a considerable bulk of food material usually in the form of highly refracting yolk-spherules. These yolk-spherules lie embedded in the protoplasm of the ovum, but are in most instances not distributed uniformly, being less closely packed and smaller at one pole of the ovum than elsewhere. Where the yolk-spherules are fewest the active protoplasm is necessarily most concentrated, and we can lay down as a general law[37] that the velocity of segmentation in any part of the ovum is roughly speaking proportional to the concentration of the protoplasm there; and that the size of the segments is inversely proportional to the concentration of the protoplasm. Thus the segments produced from that part of an egg where the yolk-spherules are most bulky, and where therefore the protoplasm is least concentrated, are larger than the remaining segments, and their formation proceeds more slowly.
[37] Vide F. M. Balfour, "Comparison of the early stages of development in Vertebrates." Quart. Jour. of Micr. Science, July, 1875.
Though where much food-yolk is present it is generally distributed unequally, yet there are many cases in which it is not possible to notice this very distinctly. In most of these cases the segmentation is all the same unequal, and it is probable that they form apparent rather than real exceptions to the law laid down above. Although before segmentation the protoplasm may be uniformly distributed, yet in many instances, e.g. Mollusca, Vermes, etc., during or at the commencement of segmentation the protoplasm becomes aggregated at one pole, and one of the segments formed consists of clear protoplasm, all the food-yolk being contained in the other and larger segment.
Unequal Segmentation. The type of segmentation I now proceed to describe has been called by Haeckel (No. 105) 'unequal segmentation', a term which may conveniently be adopted. I commence by describing it as it occurs in the well-known and typical instance of the Frog[38].
[38] Vide Remak, Entwicklung d. Wirbelthiere; and Götte, Entwicklung d. Unke.
The ripe ovum of the common Frog and of most other tailless Amphibians presents the following structure. One half appears black and the other white. The former I shall call the upper pole, the latter the lower. The ovum is composed of protoplasm containing in suspension numerous yolk-spherules. The largest of these are situated at the lower pole, the smaller ones at the upper pole, and the smallest of all in the peripheral layer of the upper pole, in which also pigment is scattered and causes the black colour visible from the surface.
[FIG. 40. SEGMENTATION OF COMMON FROG. RANA TEMPORARIA. (Copied from Ecker.)
The numbers above the figures refer to the number of segments at the stage figured.]
The first formed furrow is a vertical furrow. It commences in the upper half of the ovum, through which it extends rapidly, and then more slowly through the lower. As soon as the first furrow has extended through the egg, and the two halves have become separated from each other, a second vertical furrow appears at right angles to the first and behaves in the same way (fig. 40, 4).
The next furrow is equatorial or horizontal (fig. 40, 8). It does not arise at the true equator of the egg, but much nearer to its upper pole. It extends rapidly round the egg and divides each of the four previous segments into two parts, one larger and one smaller. Thus at the end of this stage there are present four small and four large segments. At the meeting point of these a small cavity appears, which is the segmentation cavity, already described for uniformly segmenting eggs. It increases in size in subsequent stages, its roof being formed of the smaller cells and its floor of the larger. The appearance of the equatorial furrow is followed by a period of repose, after which two rapidly succeeding vertical furrows are formed in the upper pole, dividing each of the four segments of which this is composed into two. After a short period these furrows extend to the lower pole, and when completed 16 segments are present--eight larger and eight smaller (fig. 40, 16). A pause now ensues, after which the eight upper segments become divided by an equatorial furrow, and somewhat later a similar furrow divides the eight lower segments. At the end of this stage there are therefore present 16 smaller and 16 larger segments (fig. 40, 32). After 64 segments have been formed by vertical furrows which arise symmetrically in the two poles (fig. 40, 64), two equatorial furrows appear in the upper pole before a fresh furrow arises in the lower; so that there are 128 segments in the upper half, and only 32 in the lower. The regularity is quite lost in subsequent stages, but the upper pole continues to undergo a more rapid segmentation than the lower. While the segments have been increasing in number the segmentation cavity has been rapidly growing in size; and at the close of segmentation the egg forms a sphere, containing an excentric cavity, and composed of two unequal parts (fig. 41). The upper part, which forms the roof of the segmentation cavity, is formed of smaller cells: the lower of larger yolk-containing cells.
[FIG. 41. SECTION THROUGH FROG'S OVUM AT THE CLOSE OF SEGMENTATION.
sg. segmentation cavity. ll. large yolk-containing cells. ep. small cells at formative pole (epiblast).]
The mode of segmentation of the Frog's ovum is typical for unequally segmenting ova, and it deserves to be noticed that as regards the first three or more furrows the segmentation occurs with the same rhythm in the unequally segmenting ova as in those which have an uniform segmentation. There appear two vertical furrows followed by an equatorial furrow. The general laws which were stated with reference to the velocity of segmentation and the size of the resulting segments are well exemplified in the case of the Frog's ovum.
The majority of the smaller segments in the segmented Frog's ovum are destined to form into the epiblast, and the larger segments become hypoblast and mesoblast.
With a few exceptions (the Rabbit, Lymnæus, etc.) the majority of the smaller segments always become epiblast and of the larger segments hypoblast.
The Frog's ovum serves as a good medium type for unequally segmenting ova. There are many cases however in which a regular segmentation is far more closely approached, and others in which it is less so.
One familiar instance in which a regular segmentation is nearly approached is afforded by the Rabbit's ovum, which has indeed usually been regarded as offering an example of a regular segmentation.
The ovum of the Rabbit[39] becomes first divided into two sub-equal spheres. The larger and more transparent of the two may, from its eventual fate, be called the epiblastic sphere, and the other the hypoblastic. The two spheres are divided into four, and then by an equatorial furrow into eight--four epiblastic and four hypoblastic. One of the latter assumes a central position. The four epiblastic spheres now divide before the four hypoblastic. There is thus introduced a stage with twelve spheres. It is followed by one with sixteen, and that by one with twenty-four. During the stages with sixteen spheres and onwards the epiblastic spheres gradually envelop the hypoblastic, which remain exposed on the surface at one point only. There is no segmentation cavity.
[39] Van Beneden, "Développement embryonnaire des Mammifères." Bull. de l'Acad. Belgique, 1874.
In Pedicellina, one of the entoproctous Polyzoa, there is a sub-regular segmentation, where however the two primary spheres can be distinguished much in the same way as in the case of the Rabbit.
A very characteristic type of unequal segmentation is that presented by the majority of Gasteropods and Pteropods and probably also of some Lamellibranchiata. It is also found in some Turbellarians, in Bonellia, some Annelids, etc. In many instances it offers a good example of the type where in the course of segmentation the protoplasm becomes aggregated at one pole of the ovum, or of its segments, to become separated off as a clear sphere.
The first four segments formed by two vertical furrows at right angles are equal, but from these there are budded off four smaller segments, which in subsequent stages divide rapidly, receiving however, a continual accession of segments budded off from the larger spheres. The four larger spheres remain conspicuous till near the close of the segmentation. The process of budding, by which the smaller spheres become separated from the larger, consists in a larger sphere throwing out a prominence, which then becomes constricted off from it.
In the extreme forms of this unequal segmentation we find at the end of the second cleavage two larger spheres filled with yolk material and two smaller clear spheres; and in the later stages, though the large spheres continue to bud off small spheres, only the two smaller ones undergo a regular segmentation, and eventually completely envelop the former. Such a case as this has been described in Aplysia by Lankester[40].
[40] Phil. Trans. 1875.
The types I have described serve to exemplify unequal segmentation. The Rabbit's ovum stands at one end of the series, that of Aplysia at the other; and the Frog's ovum between the two.
Great variations are presented by the ova with unequal segmentation as to the presence of a segmentation cavity. In some instances, e.g. the Frog, such a cavity is well developed. In other cases it is small, e.g. most Mollusca, while not unfrequently it is altogether absent.
Before leaving this important type of segmentation, it will be well to enter with slightly greater detail into some of the more typical as well as some of the special forms which it presents.
As an example of the typical Molluscan type the normal Heteropod segmentation, accurately described by Fol[41], may be selected.
[41] Fol, Archives de Zoologie Expérimentale, Vol. IV. 1875.
The ovum divides into two and then four equal segments in the usual vertical planes. Each segment has a protoplasmic and a vitelline pole. The protoplasmic pole is turned towards the polar bodies. In the third segmentation, which takes place along an equatorial plane, four small protoplasmic cells or segments are segmented or rather budded off from the four large segments, so that there are four small segments in one plane and four large below these. In the fourth segmentation the four large segments alone are active and give rise to four small and four large cells; so that there are formed in all eight small and four large cells. The four small cells of the third generation next divide, forming in all twelve small cells and four large. The small cells of the fourth generation then divide, and subsequently the four large cells give rise to four new small ones, so that there are twenty small cells and four large. The small cells form a cap embracing the upper pole of the large segments. It may be noted that from the third stage onwards the cells increase in arithmetical progression--a characteristic feature of the typical gasteropod segmentation.
In the later stages of segmentation the large cells cease to give rise to smaller ones in the same manner as before. One of them divides first into two unequal parts, of which the smaller becomes pushed in towards the centre of the egg. The larger cell then divides again into two, and the three cells so formed occupy the centre of a shallow depression. The remaining larger cells divide in the same way, and give rise to smaller cells which line a pit which becomes formed on one side of the ovum. The original smaller cells continue in the meantime to divide and so form a layer enclosing the larger, leaving exposed however the opening of the pit lined by the latest products of the larger cells.
The eggs of Anodon and Unio serve as excellent examples of the type in which the ovum has a uniform structure before the commencement of segmentation, but in which a separation into a protoplasmic and a nutritive portion becomes obvious during segmentation.
In Anodon[42] the egg is at first uniformly granular, but after impregnation it throws out on one side a protuberance nearly free from granules (fig. 42, 1)
[42] Flemming, "Entwick. der Najaden," Sitz. d. Akad. Wiss. Wien, Bd. 4, 1875.
[FIG. 42. SEGMENTATION OF ANODON PISCINALIS. (Copied from Flemming.) r. polar cells. v. vitelline sphere. 1. Commencing division into two segments; one mainly formed of protoplasm, the other of yolk. 2. Stage with four segments. 3. Formation of blastosphere, and segmentation cavity. 4. Definite segmentation of the yolk sphere.]
In the case of this clear protuberance and of the similar protuberances which follow it, the protoplasm is not at first quite free from food-yolk, but only becomes so on being separated from the yolk-containing part of the ovum. We must therefore suppose that the production of the clear segments is in part at least due to the yolk-spherules becoming used up to form protoplasm. Such a formation of protoplasm from yolk-spherules has been clearly shewn to occur in other types by Bobretzky and Fol.
The protuberance soon becomes separated off from the larger part of the egg as a small segment composed of clear protoplasm. From the larger segment filled with food-yolk, a second small clear segment is next budded off, and simultaneously (fig. 42, 2) the original small segment divides into two. Thus there are formed four segments, one large and three small; the large segment as before being filled with food-yolk. The continuation of a similar process of budding off and segmentation eventually results in the formation of a considerable number of small and of one large segment (fig. 42, 3). Between this large and the small segments is a segmentation cavity.
Eventually the large yolk segment, which has hitherto merely budded off a series of small segments free from yolk, itself divides into two similar parts. This process is then repeated (fig. 42, 4) and there is at last formed a number of yolk segments filled with yolk spheres, which occupy the place of the original large yolk segment. Between these yolk segments and the small segments is placed the segmentation cavity.
The segmentation of the ovum of Euaxes[43] resembles that of Unio in the budding off of clear segments from those filled with yolk, but presents many interesting individualities.
[43] Kowalevsky, Mem. Akad. Petersburg, Series VII, 1871.
A very peculiar modification of the ordinary Gasteropod segmentation is that described by Bobretzky for Nassa mutabilis[44].
[44] Archiv. f. mikr. Anat. Vol. XIII. 1877.
The ovum contains a large amount of food-yolk, and the protoplasm is aggregated at the formative pole, adjoining which are placed the polar bodies. An equatorial and a vertical furrow (fig. 43 A), the former near the upper pole, appear simultaneously, and divide the ovum into three segments, two small, each with a protoplasmic pole, and one large entirely formed of yolk material. One of the two small segments next completely fuses with the large segment (fig. 43 B), and after the fusion is complete, a triple segmentation of the large segment takes place as at the first division, and at the same time the single small segment divides into two. In this way four partially protoplasmic segments and one yolk segment are formed (fig. 43 C). One of the small segments again fuses with the large segment, so that the number of segments becomes again reduced to four, three small and one large. The protoplasmic ends of these segments are turned towards each other, and where they meet four very small cells become budded off, one from each segment (fig. 43 D). Four small cells are again budded off twice in succession, while the original small cells remain passive, so that there come to be twelve small and four large cells. In later stages the four first-formed small cells give rise to still smaller cells and then the next-formed do the same. The large cells continue also to give rise to small ones, and finally, by a continuous process of division, and fresh budding of small cells from large cells, a cap of small cells becomes formed covering the four large cells which have in the meantime pressed themselves together (fig. 43 E). A segmentation cavity of not inconsiderable dimensions becomes established between this cap of small cells and the large cells.
[FIG. 43. SEGMENTATION OF NASSA MUTABILIS (from Bobretzky). A. Upper half divided into two segments. B. One of these has fused with the large lower segment. C. Four small and one large segment, one of the former fusing with the large segment. D. Each of the four segments has given rise to a small segment. E. Small segments have increased to thirty-six.]
Many eggs, such as those of the Myriapods[45], present an irregular segmentation; but the segmentation is hardly unequal in the sense in which I have been using the term. Such cases should perhaps be placed in the first rather than in the present category.
[45] Metschnikoff, Zeitschrift f. wiss. Zoologie, 1874.
The type of unequal segmentation is on the whole the most widely distributed in the animal kingdom. There is hardly a group without examples of it.
It occurs in Porifera, Hydrozoa, Actinozoa and Ctenophora. Amongst the Ctenophora this segmentation is of the most typical kind. Four equal segments are first formed in the two first periods. In the third period a circumferential furrow separates four smaller from four larger segments.
This type is also widely distributed amongst the unsegmented (Gephyrea, Turbellaria), as well as the segmented Vermes, and is typical for the Rotifera. It appears to be very rare in Echinoderms (Echinaster Sarsii). It is not uncommon in early stages of the segmentation of the lower Crustacea.
For Mollusca (except Cephalopoda) it is typical. Amongst the Ascidia it occurs in several forms (Salpa, Molgula) and amongst the Craniata it is typical in the Cyclostomata, Amphibia, and some Ganoids, e.g. Accipenser.
Partial segmentation. The next type of segmentation we have to deal with has long been recognized as partial segmentation. It is a type in which only part of the ovum, called the germinal disc, undergoes segmentation, the remainder usually forming an appendage of the embryo known as the yolk-sack. Ova belonging to the two groups already dealt with are frequently classed together as holoblastic ova, in opposition to ova of the present group in which the segmentation is only partial, and which are therefore called meroblastic. For embryological purposes this is in many ways a very convenient classification, but ova belonging to the present group are in reality separated by no sharp line from those belonging to the group just described.
[FIG. 44. SURFACE VIEWS OF THE EARLY STAGES OF THE SEGMENTATION IN A FOWL'S EGG. (After Coste.)
a. edge of germinal disc. b. vertical furrow. c. small central segment. d. larger peripheral segment.]
The origin and nature of meroblastic ova will best be understood by taking an ovum with an unequal segmentation, such as that of the frog, and considering what would take place in accordance with the laws already laid down, supposing the amount of food-yolk at the vitelline pole to be enormously increased. What would happen may be conveniently illustrated by fig. 44, representing the segmentation of a fowl's egg. There would first obviously appear a vertical furrow at the formative or protoplasmic pole. (Fig. 44 A, b.) This would gradually advance round the ovum and commence to divide it into two halves. Before the furrow had however proceeded very far it would come to the vitelline part of the ovum; here, according to the law previously enunciated, it would travel very slowly, and if the amount of the food-yolk was practically infinite as compared with the protoplasm, it would absolutely cease to advance. A second vertical furrow would soon be formed, crossing the first at right angles, and like it not advancing beyond the edge of the germinal disc. (Fig. 44 B.)
The next furrow should be an equatorial one (as a matter of fact in the fowl's ovum an equatorial furrow is not formed till after two more vertical furrows have appeared). The equatorial furrow would however, in accordance with the analogy of the frog, not be formed at the equator, but very close to the formative pole. It would therefore separate off as a distinct segment (fig. 44 C, c), a small central, i.e. polar, portion of each of the imperfect segments formed by the previous vertical furrows. By a continuation of the process of segmentation, with the same alternation of vertical and equatorial furrows as in the frog, a cap or disc of small segments would obviously be formed at the protoplasmic pole of the ovum, outside which would be a number of deep radiating grooves (fig. 45), formed by the vertical furrows, the advance of which round the ovum has come to an end owing to the too great proportion of yolk spheres at the vitelline pole.
[FIG. 45. SURFACE VIEW OF THE GERMINAL DISC OF FOWL'S EGG DURING A LATE STAGE OF THE SEGMENTATION.
c. small central segmentation spheres; b. larger segments outside these; a. large, imperfectly circumscribed, marginal segments; e. margin of germinal disc.]
It is clear from the above that an immense accumulation of food-yolk at the vitelline pole necessarily causes a partial segmentation. It is equally clear that the part of meroblastic ova which does not undergo segmentation is not a new addition absent in other cases. It is on the contrary to be regarded merely as a part of the ovum in which the yolk-spherules have attained to a very great bulk as compared with the protoplasm; sometimes even to the complete exclusion of the protoplasm.
An ordinary meroblastic ovum consists then of a small disc at the formative pole, known as the germinal disc, composed mainly of protoplasm in which comparatively little food-yolk is present. This graduates into the remainder of the ovum, being separated from it by a more or less sharp line. This remainder of the ovum, which almost always forms the major part, usually consists of numerous yolk-spherules, embedded in a very scanty protoplasmic matrix.
In some cases, e.g. the eggs of Elasmobranchii[46], the protoplasm is present in the form of a delicate network; in other and perhaps the majority of cases, too little protoplasm is present to be detected, or the protoplasm may even be completely absent. In some Osseous Fishes, e.g. Lota, the yolk forms a homogeneous transparent albuminoid substance containing a large globule at the pole furthest removed from the germinal disc. In this case the germinal disc is sharply separated from the yolk. In other Osseous Fishes the separation between the two parts is not so sharp[47]. In these cases we find adjoining the germinal disc a finely granular material containing a large proportion of protoplasm; this graduates into a material with very little protoplasm and numerous yolk-spherules, which is in its turn continuous with an homogeneous albuminoid yolk substance. In Elasmobranchii we find that immediately beneath the germinal disc there is present a finely granular matter, rich in protoplasm, which is continuous with the normal yolk.
[46] Vide Schultze, Archiv. f. mikr. Anat. Vol. XI.; and F. M. Balfour, Monograph on the Development of Elasmobranch Fishes.
[47] Vide Klein, Quart. Journal of Micr. Science, April, 1876. Bambeke, Mem. Cour. Acad. Belgique, 1875. His, Zeit. für Anat. u. Entwicklung. Vol. I.
The Elasmobranch ovum may conveniently serve as type for the Vertebrata. The ovum is formed of a spherical vitellus without any investing membrane. The germinal disc is recognizable on this as a small yellow spot about 1-1/2 millimetres in diameter. In the germinal disc a furrow appears bisecting the disc, followed by a second furrow at right angles to the first. Thus after the formation of the second furrow the disc is divided into four equal areas. Fresh furrows continue to rise, and eventually a circular furrow, equivalent to the equatorial furrow of the frog's ovum, makes its appearance, and separates off a number of smaller central segments from peripheral larger segments. In the later stages the smaller segments at first divide more rapidly than the larger, but eventually the latter also divide rapidly, and the germinal disc becomes finally formed of a series of segments of a fairly uniform size. So much may be observed in surface views of the segmenting ovum, and it may be noted that there is not much difference to be observed between the segmentation of the germinal disc of the Fowl's ovum and that of the Elasmobranchii. Indeed the figure of the former (fig. 44) would serve fairly well for the latter. When however we examine the segmenting germinal discs by means of sections, there are some differences between the two types, and several interesting features which deserve to be noticed in the segmentation of the Elasmobranchii. In the first stages the furrows visible on the surface are merely furrows, which do not meet so as to isolate distinct segments; they merely, in fact, form a surface pattern. It is not till after the appearance of the equatorial furrow that the segments begin to be distinctly isolated. In the subsequent stages not only do the segments already existing in the germinal disc increase by division, but fresh segments are continually being formed from the adjacent yolk, and added to those already present in the germinal disc. (Fig. 46.) This fact is one out of many which prove that the germinal disc is merely part of the ovum characterized by the presence of more protoplasm than the remainder which forms the so-called food-yolk. During the latest stages of segmentation there appear in the yolk around the blastoderm a number of nuclei. (Fig. 46, nx´.) These are connected with a special protoplasmic network (already described) which penetrates through the yolk. Towards the end of segmentation, and during the early periods of development which succeed the segmentation, these nuclei become very numerous. (Fig. 47 A, n´.) Around many of them a protoplasmic investment is established, and cells are thus formed which eventually enter the blastoderm.
[FIG. 46. SECTION THROUGH GERMINAL DISC OF A PRISTIURUS EMBRYO DURING THE SEGMENTATION.
n. nucleus; nx. nucleus modified prior to division; nx´. modified nucleus of the yolk; f. furrow appearing in the yolk adjacent to the germinal disc.]
The result of segmentation is the formation of a lens-shaped mass of cells lying in a depression on the yolk. In this a cavity appears, the homologue of the segmentation cavity already spoken of. It lies at first in the midst of the cells of the blastoderm, but very soon its floor of cells vanishes, and it lies between the yolk and the blastoderm. (Fig. 47 A.) Its subsequent history is given in a future Chapter.
Segmentation proceeds in Osseous Fishes in nearly the same manner as in Elasmobranchii. In some cases the germinal disc is small as compared with the yolk, in other cases it is almost as large as the yolk. The only points which deserve special notice are the following: (1) Nuclei, precisely similar to those in the Elasmobranch yolk, appear in the protoplasmic matter around the germinal disc; (2) After the deposition of the ova there is present in some forms a network of protoplasm extending from the germinal disc through the yolk[48]. At impregnation this withdraws itself from the yolk. It is to be compared to the protoplasmic network of the Elasmobranch ovum.
[48] Vide Bambeke, loc. cit.
[FIG. 47. TWO LONGITUDINAL SECTIONS OF THE BLASTODERM OF A PRISTIURUS EMBRYO AT STAGES PRIOR TO THE FORMATION OF THE MEDULLARY GROOVE.
ep. epiblast; ll. lower layer cells; m. mesoblast; hy. hypoblast; sc. segmentation cavity; es. embryo swelling; n´. nuclei of yolk; er. embryonic rim.]
There are two types of meroblastic ova. In one of these (Aves, Elasmobranchii) the germinal disc is formed in the ovarian ovum. In the second type the germinal disc is formed after impregnation by a concentration of the protoplasm at one pole. This concentration is analogous to what has already been described for Anodon and other Molluscan ova (p. 100).
The ova of some Teleostei are intermediate between the two types.
The ovum of the wood-louse, Oniscus murarius[49], may be taken as an example of the second type of meroblastic ovum. In this egg development commences by the appearance of a small clear mass with numerous transparent vesicles. This mass is the protoplasm which has become separated from the yolk. It undergoes segmentation in a perfectly normal fashion. Examples of other cases of this kind have been described by Van Beneden and Bessels[50] in Anchorella, and in Hessia by Van Beneden[51]. It appears from their researches that the protoplasm collects itself together, first of all in the interior of the egg, and then travels to the surface. It arrives at the surface after having already divided into two or more segments, which then rapidly divide in the usual manner to form the blastoderm.
[49] Vide Bobretzky, Zeitschrift für wiss. Zoologie, Vol. XXIV., 1874.
[50] Loc. cit.
[51] Bulletins de l'Acad. Belgique, Tom. XXIX., 1870.
There are some grounds for thinking that the cases of partial segmentation in the Arthropoda are not really quite comparable with those in other groups, but more probably fall under the next type of segmentation to be described. The grounds for this view are mentioned in connection with the next type.
In most if not all meroblastic ova there appear during and after segmentation a number of nuclei in the yolk adjoining the blastoderm, around which cells become differentiated. (Figs. 46 and 47.) These cells join the part of the blastoderm formed by the normal segmentation of the germinal disc. Such nuclei are formed in all craniate meroblastic ova[52]. In Cephalopods they have been found by Lankester, and in Oniscus by Bobretzky. They have been by some authors supposed to originate from the nuclei of the blastoderm, and by others spontaneously in the yolk.
[52] Though less obvious in the ovum of the fowl than in that of some other types, they may nevertheless be demonstrated there without very much difficulty.
Some of the earliest observations on these nuclei were made by Lankester[53] in the Cephalopods. He found that they appeared first in a ring-like series round the edge of the blastoderm, and subsequently all over the yolk in a layer a little below the surface. He observed their development in the living ovum and found that they "commenced as minute points, gradually increasing in size like other free-formed nuclei." A cell area subsequently forms around them.
[53] Quart. Journ. of Micr. Science, Vol. XV. pp. 39, 40.
By E. van Beneden[54] they were observed in a Teleostean ovum to appear nearly simultaneously in considerable numbers in the granular matter beneath the blastoderm. Van Beneden concludes from the simultaneous appearance of these bodies that they develop autogenously. Kupffer at an earlier period arrived at a similar conclusion. My own observations on these nuclei in Elasmobranchii on the whole support the conclusions to be derived from Lankester's, Kupffer's and Van Beneden's observations. As mentioned above, the nuclei in Elasmobranchii do not appear simultaneously, but increase in number as development proceeds; and it is possible that Van Beneden may be mistaken on this point. No evidence came before me of derivation from pre-existing nuclei in the blastoderm. My observations prove however that the nuclei increase by division. This is shewn by the fact that I have found them with the spindle modification (fig. 46, nx´), and that in most cases they usually exhibit the form of a number of aggregated vesicles[55], which is a character of nuclei which have just undergone division. It should be mentioned however that I failed to find a spindle modification of the nuclei in the later stages. Against these observations must be set those of Bobretzky, according to which the nuclei in Oniscus are really the nuclei of cells which have migrated from the blastoderm. Bobretzky's observations do not however appear to be very conclusive.
[54] Quart. Journ. of Micr. Science, Vol. XVIII. p. 41.
[55] At the time when my observations on Elasmobranchii were carried out, this peculiar condition of the nucleus had not been elucidated.
It must be admitted that the general evidence at our command appears to indicate that the nuclei of the yolk in meroblastic ova originate spontaneously. There is however a difficulty in accepting this conclusion in the fact that all the other nuclei of the embryo are descendants of the first segmentation nucleus; and for this reason it still appears to me possible that the nuclei of the yolk will be found to originate from the continued division of one primitive nucleus, itself derived from the segmentation nucleus.
The existence of these nuclei in the yolk and the formation of a distinct cell body around them is a strong piece of evidence in favour of the view above maintained, (which is not universally accepted,) that the part of the ovum of meroblastic ova which does not segment is of the same nature as that which does segment, and differs only in being relatively deficient in active protoplasm.
The following forms have meroblastic ova of the first type: the Cephalopoda, Pyrosoma, Elasmobranchii, Teleostei, Reptilia, Aves, Ornithodelphia (?). The second type of meroblastic segmentation occurs in many Crustacea, (parasitic Copepoda, Isopoda Mysis, etc.). It is also stated to be found in Scorpio.
The ova of the majority of groups in the animal kingdom segment according to one of the types which have just been described. These types are not sharply separated, but form an unbroken series, commencing with the ovum which segments uniformly, and ending with the meroblastic ovum.
It is convenient to distinguish the ova which segment uniformly by some term; and I should propose for this the term alecithal[56], as implying that they are without food-yolk, or that what little food-yolk there is, is distributed uniformly.
[56] For this term as well as for the terms telolecithal and centrolecithal I am indebted to Mr Lankester.
The ova in which the yolk is especially concentrated at one pole I should propose to call telolecithal. They constitute together a group with an unequal or partial segmentation.
The telolecithal ova may be defined in the following way: ova in which the food-yolk is not distributed uniformly, but is concentrated at one pole of the ovum. When only a moderate quantity of food-yolk is present the pole at which it is concentrated merely segments more slowly than the opposite pole; but when food-yolk is present in very large quantity the part of the ovum in which it is located is incapable of segmentation, and forms a special appendage known as the yolk-sack.
There is a third group of ova including a series of types of segmentation nearly parallel to the telolecithal group. This group takes its start from the alecithal ovum as do the telolecithal ova, and equally with these includes a series of varieties of segmentation running parallel to the regular and unequal types of segmentation which directly result from the presence of a greater or smaller quantity of food-yolk. The food-yolk is however placed, not at one pole, but at the centre of the ovum. This group of ova I propose to name centrolecithal. It is especially characteristic of the Arthropoda, if not entirely confined to that group.
Centrolecithal ova. As might be anticipated on the analogy of the types of segmentation already described, the concentration of the food-yolk at the centre of the ovum does not always take place before segmentation, but is sometimes deferred till even the later stages of this process.
Examples of a regular segmentation in centrolecithal ova are afforded by Palæmon (Bobretzky) and Penæus (Hæckel). A type of unequal segmentation like that of the Frog occurs in Gammarus locusta (Beneden and Bessels), where however the formation of a central yolk mass does not appear to take place till rather late in the segmentation. More irregular examples of unequal segmentation are also afforded by other Crustaceans, e.g. various members of the genus Chondracanthus (Beneden and Bessels) and by Myriapods. In all these cases segmentation ends in the formation of a layer of cells enclosing a central mass of food-yolk.
[FIG. 48. SEGMENTATION OF A CRUSTACEAN OVUM (PENÆUS). (After Hæckel.)
The sections illustrate the type of segmentation in which the yolk is aggregated at the centre of the ovum.
yk. central yolk mass.
1 and 2. Surface view and section of the stage with four segments. In 2 it is seen that the furrows visible on the surface do not penetrate to the centre of the ovum.
3 and 4. Surface view and section of ovum near the end of segmentation. The central yolk mass is very clearly seen in 4.]
The peculiarity of the centrolecithal ova with regular or unequal segmentation is that (owing to the presence of the yolk in the interior) the furrows which appear on the surface are not continued to the centre of the egg. The spheres which are thus distinct on the surface are really united internally. Fig. 48, copied from Hæckel, shews this in a diagrammatic way.
Many ova, which in the later stages of segmentation exhibit the characteristics of true centrolecithal ova, in the early stages actually pass through nearly the same phases as holoblastic ova. Thus in Eupagurus prideauxii[57] (fig. 49), and probably in the majority of Decapods, the egg is divided successively into two, four and eight distinct segments, and it is not till after the fourth phase of the segmentation that the spheres fuse in the centre of the egg. Such ova belong to a type which is really intermediate between the ordinary type of segmentation and that with a central yolk mass. Eupagurus presents one striking peculiarity, viz. that the nucleus divides into two, four and eight nuclei, each surrounded by a delicate layer of protoplasm prolonged into a reticulum, before the ovum itself commences to become segmented. The ovum before segmentation is therefore in the condition of a syncytium.
[57] Mayer, Jenaische Zeitschrift, Vol. XI.
[FIG. 49. TRANSVERSE SECTION THROUGH FOUR STAGES IN THE SEGMENTATION OF EUPAGURUS PRIDEAUXII. (After P. Mayer.)]
The segmentation of Asellus aquaticus[58] is very similar to that of Eupagurus, etc. but the ovum at the very first divides into as many segments (viz. eight) as there are nuclei.
[58] Ed. van Beneden, Bull. d. l'Acad. roy. Belgique, 2me série, Tom. XXVIII. No. 7, 1869, p. 54.
In Gammarus locusta the resemblance to ordinary unequal segmentation is very striking, and it is not till a considerable number of segments have been formed that a central yolk mass appears.
In all the above types, as segmentation proceeds, the protoplasm becomes more and more concentrated at the surface, and finally a superficial layer of flat blastoderm cells is completely segmented off from the yolk below (fig. 49 D).
In cases like those of Penæus, Eupagurus, etc., the yolk in the interior is at first nearly homogeneous, but at a later period it generally becomes divided up partially or completely into a number of distinct spheres, which may have nuclei and therefore have the value of cells. In many cases nuclei have however not been demonstrated in these yolk spheres, though probably present; yet, till they have been demonstrated, some doubt must remain on the nature of these yolk spheres. It is probable that not all the nuclei which result from the division of the first segmentation nucleus become concerned in the formation of the superficial blastoderm, but that some remain in the interior of the ovum to become the nuclei of the yolk spheres.
[FIG. 50. SEGMENTATION AND FORMATION OF THE BLASTODERM IN CHELIFER. (After Metschnikoff.)
In A the ovum is divided into a number of separate segments. In B a number of small cells have appeared (bl) which form a blastoderm enveloping the large yolk spheres. In C the blastoderm has become divided into two layers.]
In Myriapods (Chilognatha) a peculiar form of segmentation has been observed by Metschnikoff[59]. The ovum commences by undergoing a perfectly normal, though rather irregular total segmentation. But after the process of division has reached a certain point, scattered masses of very small cells make their appearance on the surface of the large spheres. These small cells have probably arisen in a manner analogous to that which characterizes the formation of the superficial cells of the blastoderm in the types of centrolecithal ova already described. They rapidly increase in number and eventually form a continuous blastoderm; while the original large segments remain in the centre as the yolk mass. In the interesting Arachnid Chelifer segmentation takes place in nearly the same manner as in Myriapods (fig. 50).
[59] Zeitschrift für wiss. Zool., Vol. XXIV. 1874.
[FIG. 51. FOUR SUCCESSIVE STAGES IN THE SEGMENTATION OF THE EGG OF TETRANYCHUS TELARIUS. (After Claparède.)]
It is clear that it is not possible in centrolecithal ova to have any type of segmentation exactly comparable with that of meroblastic ova. There are however some types which fill the place of the meroblastic ova in the present group, in as much as they are characterised by the presence of a large bulk of food-yolk which either does not segment, or does not do so till a very late stage in the development. The essential character of this type of segmentation consists in the division of the germinal vesicle in the interior, or at the surface of the ovum into two, four, etc. nuclei (fig. 51). These nuclei are each of them surrounded by a specially concentrated layer of protoplasm (fig. 51) which is continuous with a general protoplasmic reticulum passing through the ovum [not shewn in fig. 51]. The yolk is contained in the meshes of this reticulum in the manner already described for other ova.
The ovum, like that of Eupagurus before segmentation, is now a syncytium. Eventually the nuclei, having increased by division and become very numerous, travel, unless previously situated there, to the surface of the ovum. They then either simultaneously or in succession become, together with protoplasm around them, segmented off from the yolk, and give rise to a peripheral blastoderm enclosing a central yolk mass. In the latter however many of the nuclei usually remain, and it also very often undergoes a secondary segmentation into a number of yolk spheres.
The eggs of Insects afford numerous examples of this mode of segmentation, of which the egg of Porthesia[60] may be taken as type. After impregnation it consists of a central mass of yolk which passes without a sharp line of demarcation into a peripheral layer of more transparent (protoplasmic) material. In the earliest stage observed by Bobretzky there were two bodies in the interior of the egg, each consisting of a nucleus enclosed in a thin protoplasmic layer with stellate prolongations. This stage corresponds with the division into two, but though the nucleus divides, the preponderating amount of yolk prevents the egg from segmenting at the same time. By a continuous division of the nuclei there becomes scattered through the interior of the ovum a series of bodies, each formed of nucleus and a thin layer of protoplasm with reticulate processes. After a certain stage some of these bodies pass to the surface, simultaneously (in Porthesia) or in some cases successively. At the surface the protoplasm round each nucleus contracts itself into a rounded cell body, distinctly cut off from the adjacent yolk.
[60] Bobretzky, Zeit. f. wiss. Zool., Bd. XXXI. 1878.
The cells so formed give rise to a superficial blastoderm of a single layer of cells. Many of the nucleated bodies remain in the yolk, and after a certain time, which varies in different forms, the yolk becomes segmented up into a number of rounded or polygonal bodies, in the interior of each of which one of the above nuclei with its protoplasm is present. This process, known as the secondary segmentation of the yolk, is really part of the true segmentation, and the bodies to which it gives rise are true cells.
Other examples of this type may be cited. In Aphis[61] Metschnikoff shewed that the first segmentation nucleus divides into two, each of which takes up a position in the clearer peripheral protoplasmic layer of the egg (fig. 52, 1 and 2). Following upon further division the nuclei enveloped in a continuous layer of protoplasm arrange themselves in a regular manner, and form a syncytium, which becomes segmented into definite cells (fig. 52, 3 and 4). The existence of a special clear superficial layer of protoplasm has been questioned by Brandt.
[61] Metschnikoff, "Embry. Stud. Insecten," Zeit. für wiss. Zool., Bd. XVI. 1866. My own observations on this form accord in the main with those of Metschnikoff.
[FIG. 52. SEGMENTATION OF APHIS ROSAE. (Copied from Metschnikoff.)
In all the stages there is seen to be a central yolk mass surrounded by a layer of protoplasm.
In this protoplasm two nuclei have appeared in 1, four nuclei in 2. In 3 the nuclei have arranged themselves regularly, and in 4 the protoplasm has become divided into a number of columnar cells corresponding to the nuclei.
w. pole of the blastoderm which has no share in forming the embryo.]
In Tetranychus telarius, one of the mites, Claparède found on the surface of the ovum a nucleus surrounded by granular protoplasm (fig. 51); which is no doubt the first segmentation nucleus. By a series of divisions, all on the surface, a layer of cells becomes formed round a central yolk mass. The result here is the same as in Insects, but the nucleus with its granular protoplasm is from the first superficial. In other cases, such as that of the common fly[62], a layer of protoplasm is stated to appear investing the yolk; and in this there arise simultaneously (?) a number of nuclei at regular intervals, around each of which the protoplasm separates itself to form a distinct cell. Closely allied is the type observed by Kowalevsky in Apis. Development here commences by the appearance of a number of protoplasmic prominences, each forming a cell provided with a nucleus, the nuclei having no doubt been formed by previous division in the interior of the ovum. They appear at the edge of the yolk, and are separated from one another by short intervals. Shortly after their appearance a second batch of similar bodies appears, filling up the interspaces between the first-formed prominences. In the fresh-water Gammarus fluviatilis the protoplasm is stated first of all to collect at the centre of the ovum, where no doubt the segmentation nucleus divides. Subsequently cells appear at numerous points on the surface, and by repeated division constitute an uniform blastoderm investing the central yolk mass. This mode of formation of the blastoderm is closely allied to that observed by Kowalevsky in Apis.
[62] Vide Weismann, Entwicklung d. Dipteren; and Auerbach, Organologische Studien.
Between ova with a segmentation like that of Insects, and those with a segmentation like that of Penæus, there is more than one intermediate form. The Eupagurus type, with the division of the first nucleus into eight nuclei before the division of the ovum, must be regarded in this light; but the most instructive example of such a transitional type of segmentation is that afforded by Spiders[63].
[63] Vide Ludwig, Zeit. f. wiss. Zool., 1876.
[FIG. 53. THREE STAGES IN THE SEGMENTATION OF PHILODROMUS LIMBATUS. (After Hub. Ludwig.)]
The first phenomenon which can be observed after impregnation is the conglomeration of the yolk spheres into cylindrical columns, which finally assume a radiating form diverging from the centre of the egg. In the centre of the radiate figure is a protoplasmic mass, probably containing a nucleus, which sends out protoplasmic filaments through the columns (fig. 53 A). After a certain period of repose the figure becomes divided into two rosette-like masses, which remain united for some time by a protoplasmic thread: this thread is finally ruptured (fig. 53 B). The whole egg does not in this process divide into two segments, but merely the radiate figure, which is enclosed in a finely granular material. The two rosettes next become simultaneously divided, giving rise to four rosettes (fig. 53 C): and the whole process is repeated with the same rhythm as in a regular segmentation till there are formed thirty-two rosettes in all (fig. 54 A). The rosettes by this time have become simple columns, which by mutual pressure arrange themselves radiately around the centre of the egg, which however they do not quite reach.
[FIG. 54. SURFACE VIEW AND OPTICAL SECTION OF A LATE STAGE IN THE SEGMENTATION OF PHILODROMUS LIMBATUS (Koch). (After Hub. Ludwig.)
bl. blastoderm; yk. yolk spheres.]
When only two rosettes are present the protoplasm with its nucleus occupies a central position in each rosette, but gradually, in the course of the subsequent subdivisions, it travels towards the periphery, and finally occupies, when the stage with thirty-two rosettes is reached, a peripheral position. The peripheral protoplasm next becomes separated off as a nucleated layer (fig. 54 B). It forms the proper blastoderm, and in it the nuclei rapidly multiply and finally around each an hexagonal or polygonal area of protoplasm is marked off; and a blastoderm, formed of a single layer of flattened cells, is thus constituted. The columns within the blastoderm now form (fig. 54 B) more or less distinct masses, which are stated by Ludwig to be without protoplasm.
From observations of my own I am inclined to differ from Ludwig as to the nature of the parts within the blastoderm. My observations have been made on Agelena labyrinthica and commence at the close of the segmentation. At this time I find a superficial layer of flattened cells, and within these a number of large polyhedral yolk cells. In many, and I believe all, of the yolk cells there is a nucleus surrounded by protoplasm. It is generally placed at one side and not in the centre of a yolk cell, and the nuclei are so often double that I have no doubt they are rapidly undergoing division. It appears to me probable that, at the time when the superficial layer of protoplasm is segmented off from the yolk below, the nuclei undergo division, and that a nucleus with surrounding protoplasm is left with each yolk column. For further details vide Chapter on Arachnida.
Although by the close of the segmentation the protoplasm has travelled to a superficial position, it may be noted that at first it forms a small mass in the centre of the egg, and only eventually assumes its peripheral situation. It is moreover clear that in the Spider's ovum there is, so to speak, an attempt at a complete segmentation, which however only results in an arrangement of the constituents of the ovum in masses round each nucleus, and not in a true division of the ovum into distinct segments.
It seems very probable that Ludwig's observations on the segmentation of Spiders only hold good for species with comparatively small ova.
In connection with the segmentation of the Insects' ovum and allied types it should be mentioned that Bobretzky, to whose observations we are largely indebted for our knowledge of this subject, holds somewhat different views from those adopted in the text. He regards the nuclei surrounded by protoplasm, which are produced by the division of the primitive segmentation nucleus, as so many distinct cells. These cells are supposed to move about freely in the yolk, which acts as a kind of intercellular medium. This view does not commend itself to me. It is opposed to my own observations on similar nuclei in the Spiders. It does not fit in with our knowledge of the nature of the ovum, and it cannot be reconciled with the segmentation of such types as Spiders or even Eupagurus, with which the segmentation in Insects is undoubtedly closely related.
The majority if not all the cases in which a central yolk mass is formed occur in the Arthropoda, in which group centrolecithal ova are undoubtedly in a majority. In Alcyonium palmatum the segmentation appears however to resemble that of many insects.
One or two peculiar varieties in the segmentation of ova of this type may be spoken of here. The first one I shall mention is detailed in the important paper of E. Van Beneden and Bessels which I have already so often had occasion to quote: it is characteristic of the eggs of most of the species of Chondracanthus, a genus of parasitic Crustaceans. The ovum divides in the usual way but somewhat irregularly into 2, 4, 8 segments which meet in a central yolk mass; but after the third division instead of each segment dividing into two equal parts it divides at once into four, and the division into four having started, reappears at every successive division. Thus the number of the segments at successive periods is 2, 4, 8, 32, 128, etc. In another peculiar case, an instance of which[64] is afforded by Asellus aquaticus, after each of the earlier segmentations all the segments fuse and become indistinguishable, but at the succeeding segmentation double the number of segments appears.
Although, as has been already stated, it does not seem possible to have a true meroblastic segmentation in centrolecithal ova, it does nevertheless appear probable that the apparent cases of a meroblastic segmentation in the Arthropoda are derivatives of this type of segmentation. The manner in which the one type might pass into the other may perhaps be explained by the segmentation in Asellus aquaticus[65]. In this ovum large segments are at first formed around a central yolk mass, in the peculiar manner mentioned in the previous paragraph, but at the close of the first period of segmentation minute cells, which eventually form a superficial blastoderm, are produced from the yolk cells. They do not however appear at once round the whole periphery of the egg, but at first only on the ventral surface and later on the dorsal surface. If the amount of food-yolk in the egg were to increase so as to render the formation of the yolk cells impossible, and at the same time the formation of the blastodermic cells were to take place at the commencement, instead of towards the close of the segmentation, a mass of protoplasm with a nucleus might first appear at the surface on the future ventral side of the egg, then divide in the usual way for meroblastic ova, and give rise to a layer of cells gradually extending round to the dorsal surface. A meroblastic segmentation might perhaps be even more easily derived from the type found in Insects. It is probable that the cases of Scorpio, Mysis, Oniscus, the parasitic Isopoda, and some parasitic Copepoda belong to this category; and it may be noticed that in these cases the blastopore would be situated on the dorsal and not on the ventral side of the ovum. The morphological importance of this latter fact will appear in the sequel.
[64] [65] Ed. van Beneden, Bull. Acad. Belgique, Vol. XXVIII. 1869.
The results arrived at in the present section may be shortly restated in the following way.
(1) A comparatively small number of ova contain very little or no food-yolk embedded in their protoplasm; and have what food-yolk may be present distributed uniformly. In such ova the segmentation is regular. They may be described as alecithal ova.
(2) The distribution of food-yolk in the protoplasm of the ovum exercises an important influence on the segmentation.
The rapidity with which any part of an ovum segments varies ceteris paribus with the relative amount of protoplasm it contains; and the size of the segments formed varies inversely to the relative amount of protoplasm. When the proportion of protoplasm in any part of an ovum becomes extremely small, segmentation does not occur in that part.
Ova with food-yolk may be divided into two great groups according to the eventual arrangement of the food-yolk in the protoplasm. In one of these, the food-yolk when present is concentrated at the vegetative pole of the ovum. In the other group it is concentrated at the centre of the ovum. Ova belonging to the former group are known as telolecithal ova, those to the latter as centrolecithal.
In each group more than one type may be distinguished. In the first group these types are (1) unequal segmentation, (2) partial segmentation. The features of these three types have been already so fully explained that I need not repeat them here.
In the second group there are three distinct types, (1) equal segmentation, (2) unequal segmentation. These two being externally similar to the similarly named types in the first group. (3) Superficial segmentation. This is unlike anything which is present in the first group, and is characterized by the appearance of a superficial layer of cells round a central yolk mass. These cells may either appear simultaneously or successively, and their nuclei are derived from the segmentation within the ovum of the first segmentation nucleus.
The types of ova in relation to the characters of the segmentation may be tabulated in the following way:
Segmentation. (1) alecithal } regular ova } (2) telolecithal } (a) unequal ova } (b) partial (3) centrolecithal } (a) regular (with segments united in ova } central yolk mass) } (b) unequal " " " " } (c) superficial.
Although the various types of segmentation which have been described present very different aspects, they must nevertheless be looked on as manifestations of the same inherited tendency to division, which differ only according to the conditions under which the tendency displays itself.
This tendency is probably to be regarded as the embryological repetition of that phase in the evolution of the Metazoa, which constituted the transition from the protozoon to the metazoon condition.
From the facts narrated in this chapter the reader will have gathered that similarity or dissimilarity of segmentation is no safe guide to affinities. In many cases, it is true, a special type of segmentation may characterize a whole group; but in other cases very closely allied animals present the greatest differences with respect to their segmentation; as for instance the different species of the genus Gammarus. The character of the segmentation has great influence on the early phenomena of development, though naturally none on the adult form.
EXTERNAL FEATURES OF SEGMENTATION.
(105) E. Haeckel. "Die Gastrula u. Eifurchung." Jenaische Zeitschrift, Vol. IX. 1877.
(106) Fr. Leydig. "Die Dotterfurchung nach ihrem Vorkommen in d. Thierwelt u. n. ihrer Bedeutung." Oken Isis. 1848.
Part I
SYSTEMATIC EMBRYOLOGY.
Introduction
In all the Metazoa the segmentation is followed by a series of changes which result in the grouping of the embryonic cells into definite layers, or membranes, known as the germinal layers. There are always two of these layers, known as the epiblast and hypoblast; and in the majority of instances a third layer, known as the mesoblast, becomes interposed between them. It is by the further differentiation of the germinal layers that the organs of the adult become built up. Owing to this it is usual, in the language of Embryology, to speak of the organs as derived from such or such a germinal layer.
At the close of the section of this work devoted to systematic embryology, there is a discussion of the difficult questions which arise as to the complete or partial homology of these layers throughout the Metazoa, and as to the meaning to be attached to the various processes by which they take their origin; but a few words as to the general fate of the layers, and the general nature of the processes by which they are formed, will not be out of place here.
Of the three layers the epiblast and hypoblast are to be regarded as the primary. The epiblast is essentially the primitive integument, and constitutes the protective and sensory layer. It gives rise to the skin, cuticle, nervous system, and organs of special sense. The hypoblast is essentially the digestive and secretory layer, and gives rise to the epithelium lining the alimentary tract and the glands connected with it.
The mesoblast is only found in a fully developed condition in the forms more highly organized than the Coelenterata. It gives origin to the general connective tissue, internal skeleton, the muscular system, the lining of the body cavity, the vascular, and excretory systems. It probably in the first instance originated from differentiations of the two primary layers, and in all groups with a well-developed body cavity it is divided into two strata. One of them forms part of the body wall and is known as the somatic mesoblast, the other forms part of the wall of the viscera and is known as the splanchnic mesoblast.
A very large number not to say the majority of organs are derived from parts of two of the germinal layers. Many glands for instance have a lining of hypoblast which is coated by a mesoblastic layer.
[FIG. 55. DIAGRAM OF A GASTRULA. (From Gegenbaur.)
a. blastopore; b. archenteron; c. hypoblast; d. epiblast.]
The processes by which the germinal layers take their origin are largely influenced by the character of the segmentation, which, as was shewn in the last chapter, is mainly dependent on the distribution of the food-yolk. When the segmentation is regular, and results in the formation of a blastosphere, the epiblast and hypoblast are usually differentiated from the uniform cells forming the wall of the blastosphere in one of the two following ways.
(1) One-half of the blastosphere may be pushed in towards the other half. A two-layered hemisphere is thus established which soon elongates, while its opening narrows to a small pore (fig. 55). The embryonic form produced by this process is known as a gastrula. The process by which it originates is known as embolic invagination, or shortly invagination. Of the two layers of which it is formed the inner one (c) is known as the hypoblast and the outer (d) as the epiblast, while the pore leading into its cavity lined by the hypoblast is the blastopore (a). The cavity itself is the archenteron (b).
(2) The cells of the blastosphere may divide themselves by a process of concentric splitting into two layers (fig. 56, 3). The two layers are as before the epiblast and hypoblast, and the process by which they originate is known as delamination. The central cavity or archenteron (F) is in the case of delamination the original segmentation cavity; and not an entirely new cavity as in the case of invagination. By the perforation of the closed two-walled vesicle resulting from delamination an embryonic form is produced which cannot be distinguished in structure from the gastrula produced by invagination (fig. 56, 4). The opening (M) in this case is not however known as the blastopore but as the mouth.
[FIG. 56. DIAGRAM SHEWING THE FORMATION OF A GASTRULA BY DELAMINATION. (From Lankester.)
Fig. 1. Ovum. Fig. 2. Stage in segmentation. Fig. 3. Commencement of delamination after the appearance of a central cavity. Fig. 4. Delamination completed, mouth forming at M. In fig. 1, 2 and 3 Ec. is ectoplasm, and En. is entoplasm. In fig. 4 Ec. is epiblast and En. hypoblast.]
When segmentation does not take place on the regular type the processes above described are as a rule somewhat modified. The yolk is usually concentrated in the cells which would, in the case of a simple gastrula, be invaginated. As a consequence of this, these cells become (1) distinctly marked off from the epiblast cells during the segmentation; and (2) very much more bulky than the epiblast cells. The bulkiness of the hypoblast cells necessitates a modification of the normal process of embolic invagination, and causes another process to be substituted for it, viz. the growth of the epiblast cells as a thin layer over the hypoblast. This process (fig. 57) is known as epibolic invagination. The point where the complete enclosure of the hypoblast cells is effected is known as the blastopore. All intermediate conditions between epibolic and embolic invagination have been found.
[FIG. 57. TRANSVERSE SECTION THROUGH THE OVUM OF EUAXES DURING AN EARLY STAGE OF DEVELOPMENT. (After Kowalevsky.)
ep. epiblast; ms. mesoblastic band; hy. hypoblast.]
[FIG. 58. TWO STAGES IN THE DEVELOPMENT OF STEPHANOMIA PICTUM. (After Metschnikoff.)
A. Stage after the delamination. ep. epiblastic invagination to form pneumatocyst.
B. Later stage after the formation of the gastric cavity in the solid hypoblast. po. polypite; t. tentacle; pp. pneumatophore; ep. epiblastic invagination to form pneumatocyst; hy. hypoblast surrounding pneumatocyst.]
In delamination, when the segmentation is not uniform, or when a solid morula is formed, the differentiation of the epiblast and hypoblast is effected by the separation of the central solid mass of cells from the peripheral cells (fig. 58 A).
In the case of epibolic invagination as well as in that of the type of delamination just spoken of, the archenteric cavity is in most cases secondarily formed in the solid mass of hypoblast (fig. 58 B).
In ova with a partial segmentation there is usually some modification of the epibolic gastrula.
Many varieties are found in the animal kingdom of the types of invagination and delamination just characterized, and in not a few forms the layers originate in a manner which cannot be brought into connection with either of these processes.
[FIG. 59. EPIBOLIC GASTRULA OF BONELLIA. (After Spengel.)
A. Stage when the four hypoblast cells are nearly enclosed. B. Stage after the formation of the mesoblast has commenced by an infolding of the lips of the blastopore. ep. epiblast; me. mesoblast; bl. blastopore.]
The mesoblast usually originates subsequently to the two primary layers. It then springs from one or both of the other layers, but its modes of origin are so various that it would be useless to attempt to classify them here. In cases of invagination it often arises at the lips of the blastopore (fig. 57 and 59), and in other cases part of it springs as paired hollow outgrowths of the walls of the archenteron. Such outgrowths are shewn in fig. 60, B and C at pv. The cavity of the outgrowths forms the body cavity, and the walls of the outgrowths the somatic and splanchnic layers of mesoblast (fig. C. sp. and so.). The archenteron is in part always converted into a section of the permanent alimentary tract and the section of the alimentary tract so derived is known as the mesenteron. There are however usually two additional parts of the alimentary tract, known as the stomodaeum and proctodaeum, derived from epiblastic invaginations. They give rise respectively to the oral and anal extremities of the alimentary tract.
[FIG. 60. THREE STAGES IN THE DEVELOPMENT OF SAGITTA. (A and C after Bütschli and B after Kowalevsky.) The three embryos are represented in the same positions.
A. Represents the gastrula stage. B. Represents a succeeding stage in which the primitive archenteron is commencing to be divided into three parts, the two lateral of which are destined to form the mesoblast. C. Represents a later stage in which the mouth involution (m) has become continuous with alimentary tract, and the blastopore has become closed.
m. mouth; al. alimentary canal; ae. archenteron; bl. p. blastopore; pv. perivisceral cavity; sp. splanchnic mesoblast; so. somatic mesoblast; ge. generative organs.]
BIBLIOGRAPHY.
(107) K. E. von Baer. "Ueb. Entwicklungsgeschichte d. Thiere." Königsberg, 1828-1837.
(108) C. Claus. Grundzüge d. Zoologie. Marburg und Leipzig, 1879.
(109) C. Gegenbaur. Grundriss d. vergleichenden Anatomie. Leipzig, 1878. Vide also Translation. Elements of Comparative Anatomy. Macmillan and Co., 1878.
(110) E. Haeckel. Studien z. Gastræa-Theorie. Jena, 1877, and also Jenaische Zeitschrift, Vols. VIII. and IX.
(111) E. Haeckel. Schöpfungsgeschichte. Leipzig. Vide also Translation. The History of Creation. King and Co., London, 1876.
(112) E. Haeckel. Anthropogenie. Leipzig. Vide also Translation. Anthropogeny (Translation). Kegan Paul and Co., London, 1878.
(113) Th. H. Huxley. The Anatomy of Invertebrated Animals. Churchill, 1877.
(114) E. R. Lankester. "Notes on Embryology and Classification." Quart. J. of. Micr. Science, Vol. XVII. 1877.
(115) A. S. P. Packard. Life Histories of Animals, including Man, or Outlines of Comparative Embryology. Holt and Co., New York, 1876.
(116) H. Rathke. Abhandlungen z. Bildung und Entwicklungsgesch. d. Menschen u. d. Thiere. Leipzig, 1833.
IV. DICYEMIDÆ AND ORTHONECTIDÆ
DICYEMIDÆ.
The structure and development of these remarkable parasites in the renal organs of the Cephalopoda have recently been greatly elucidated by the researches of E. van Beneden; and although a male element has not been discovered, yet the embryos originate from bodies which have a close similarity to ordinary ova.
Van Beneden has shewn that Dicyema consists in the adult state of (1) a single layer of ciliated epiblast cells, somewhat modified anteriorly to form a cephalic enlargement; and of (2) one large nucleated hypoblast cell enclosed within the epiblast. There are two kinds of embryo, both developed from germs which originate in the hypoblast cell. The two kinds of embryo arise in individuals of somewhat different forms. The one kind, called by Van Beneden the vermiform embryo, arises in the more elongated and thinner examples of Dicyema which have been named Nematogens. These embryos pass directly into the parent form without metamorphosis.
The second kind of embryo, called infusoriform, is very different from the parent, and has a free existence. Its eventual history is not known. It originates in the shorter and thicker individuals of Dicyema; which have been called Rhombogens.
The Vermiform Embryos. The germs or cells which give rise to the vermiform embryos originate endogenously in the protoplasmic reticulum of the axial hypoblast cell. They appear as small but well-defined spheres, with a minute body in the centre. In these spheres a cortical layer becomes differentiated, which gradually increases in thickness and gives rise to the body of a cell, the nucleus and nucleolus of which are respectively formed from the inner part of the original sphere and the minute central body. These germs can originate in all parts of the hypoblast cell and are frequently very numerous.
[FIG. 61. A. GASTRULA STAGE OF DICYEMA TYPUS. B. VERIFORM EMBRYO OF DICYEMA TYPUS. (From Gegenbaur, after E. van Beneden.)]
The germ when completely formed undergoes a segmentation very similar to that of an ordinary ovum. It divides first into two and then into four approximately equal segments. Of the four segments one, however, remains passive for the remainder of the development. The other three divide and arrange themselves so as partially to enclose in a cup-like fashion the passive cell (fig. 61 A). The six cells resulting from their division again divide, giving rise to twelve cells, which nearly enclose the passive cell, leaving only a small aperture at one point. The whole process by which the central cell becomes enclosed is, as E. van Beneden points out, identical with a gastrula formation by epibole, and the space where the central cell is left uncovered is the blastopore. The central cell itself gives origin to the hypoblast cell of the adult, and the peripheral cells to the epiblast.
By this time the embryo has assumed an oval form, and the blastopore is situated at the pole of the long axis of the oval where the cephalic enlargement is eventually formed.
The subsequent development consists mainly in the closure of the blastopore, and an increase in the number of the epiblast cells. Before the development is completed, and while the embryo is still in the body of the parent, two germs, destined themselves to give rise to fresh embryos, appear in the hypoblast cell, one on each side of the nucleus (fig. 61 B). The embryo continues to elongate, while the anterior cells become converted into the polar cells. Cilia appear simultaneously over the general surface, and the embryo makes its way out of the body of the parent, usually at the cephalic pole, and becomes itself parasitic in the renal organ of the host in which it finds itself. At the time of birth the embryo may contain a number of germs and sometimes even developing embryos.
Infusoriform Embryos. The infusoriform embryos are capable of living in sea-water and almost certainly lead a free existence. In their most fully developed condition so far known they have the following rather complicated structure (fig. 62 D, E, F, G).
The body is somewhat pyriform, with a blunt extremity which is directed forwards in swimming, and a more pointed extremity directed backwards. The former may be spoken of as the anterior, and the latter as the posterior extremity or tail. At the anterior extremity are situated a pair of refractive bodies (r) which lie above an unpaired organ which may be called the urn.
The structure of the urn, the refractive bodies, and the tail may be dealt with in succession.
The urn consists of three parts: (1) a wall (u), (2) a lid (l), and (3) contents (gr). The wall of the urn is hemispherical in form, and composed of two halves in apposition (fig. F). Its concavity is directed forwards, and in its edge are imbedded a number of rod-like corpuscles which appear as a ring near the surface in a full-face view (fig. D). The lid has the form of a low pyramid with its apex directed outwards. It is made up of four segments (fig. D). The contents of the urn, which completely fill up its cavity, are four polynuclear cells arranged in the form of a cross which appear with low powers as granular bodies (fig. F). They are frequently ejected, apparently at the will of the embryo.
The refractive bodies (r), two in number, one on each side of the middle line, are composed of a material which is not of a fatty nature, and which is passive to the majority of reagents. Each is enveloped in a special capsule, and at times more than one refractive body is present in each capsule. The tail is a conical structure formed of ciliated granular cells.
No plausible guess has been made as to the function either of the urn or of the refractive bodies.
The infusoriform embryos originate from germs, which have however a different origin to the germs of the vermiform embryos. One to five cells appear in the axial hypoblast cell, in a way not clearly made out, and each of them gives rise by an endogenous process to several generations of cells, all of which develop into infusoriform embryos.
[FIG. 62. INFUSORIFORM EMBRYO OF DICYEMA.
A. B. C. Three of the later stages in the development. D. E. F. Three different views of the full-grown larva. D. from the front, E. from the side, and F. from above. G. side view of urn. u. wall of urn; l. lid of urn; r. refractive bodies; gr. granular bodies filling the interior of the urn.]
The primitive cell is called by Van Beneden a Germogen. In its protoplasm a number of germs first appear endogenously, but the nucleus of the germogen does not assist in their formation. They eventually become detached from the parent cell, around which they are concentrically arranged. A second and then a third generation of germs are formed in the same way, till the whole of the protoplasm of the primitive cell is absorbed in the formation of these germs, and nothing of it remains but the nucleus. The germs so formed are arranged in about three concentric layers, of which the innermost is the youngest. One to five masses of germs may be present in a single Rhombogen. The germs undergo a division, in the course of which their nuclei exhibit very beautifully a spindle modification. In the course of the segmentation the embryo gradually assumes its permanent form, and four of the cells composing it can be distinguished from the remainder by their greater size (fig. 62 A, u). The two largest of these give rise to the wall of the urn, and also give origin to four smaller cells (fig. 62 B, gr) which eventually become polynuclear and constitute the four granular cells in the urn. The two other cells become the lid of the urn. The parts of the urn lie at first side by side, but in the course of development the cells which form the wall of the urn travel inwards, and the four granular cells are carried into their concavity. At the same time the cells which form the lid of the urn alter their position so as to overlie the wall of the urn. The two cells immediately above the urn give rise to the refractive bodies (fig. 62 A, B, C, r) and the remainder of the cells of the embryo become the tail (fig. 62 C). The embryo becomes ciliated, and attains its nearly full development before leaving the parental tissues. It usually passes out at the cephalic extremity.
As has already been stated, it is probable that the infusoriform embryos leave the renal organs of their host and lead a free existence. What becomes of them afterwards is not however known, though there can be little doubt that they serve to carry the species to new hosts.
Till the further development of the infusoriform embryo is known it is not possible to arrive at a definite conclusion as to the affinities of this strange parasite. Van Beneden is anxious to form it, on account of its simple organization, into a group between the Protozoa and the Metazoa. It appears however very possible that the simplicity of its organization is the result of a parasitic existence; a view which receives confirmation from the common occurrence of the process of endogenous cell formation in the axial hypoblast cell. It has been clearly shewn by Strasburger that endogenous cell formation is secondarily derived from cell division; so that the occurrence of this process in Dicyema probably indicates that the hypoblast was primitively multicellular. It is not improbable that the enigmatical infusoriform embryo may develop into a sexual form, the progeny of which are destined to complete the cycle of development by becoming again parasitic in the renal organ of a Cephalopod.
BIBLIOGRAPHY.
(117) E. van Beneden. "Recherches sur les Dicyemides." Bull. d. l'Académie roy. de Belgique, 2e sér. T. XLI. No. 6 and T. XLII. No. 7, 1876. Vide this paper for a full account of the literature.
(118) A. Kölliker. Ueber Dicyema paradoxum den Schmarotzer der Venenanhänge der Cephalopoden.
(119) Aug. Krohn. "Ueb. d. Vorkommen von Entozoen, etc." Froriep Notizen, VII. 1839.
ORTHONECTIDÆ.
A number of minute parasites infesting various Nemertines, Turbellarians, and Ophiuroids have recently been studied by Giard and Metschnikoff, the former of whom has placed them in a special group which he calls the Orthonectidæ. They were first discovered by W. C. McIntosh.
In the adult state they are[66] (Metschnikoff) somewhat pear-shaped bodies formed of a kind of plasmodium of cells with irregular lobate processes. In the interior of this body are eggs in all stages of development. In the type observed by Metschnikoff (Intoshia gigas) the ova undergo a regular segmentation, resulting in the formation of a blastosphere in which an inner layer is subsequently formed by delamination. A smaller and a larger kind of embryo are formed; but all the embryos in each female belong to one type. The larger become females and the smaller males.
[66] This at any rate holds true for the type investigated by Metschnikoff. The full history of other forms is not yet known.
The female embryos are ovoid. The outer layer of cells or epiblast becomes ciliated, and divided into nine segments, of which the second is marked off from the remainder by the absence of cilia, and by being provided with refractive corpuscles. The inner layer which surrounds a central cavity, and might be supposed to be the hypoblast, becomes according to Metschnikoff converted into ova.
The male embryos are more elongated than the female, from which they further differ in only having six segments. The cells of the inner layer eventually divide up into spermatozoa.
The larvæ probably become free, and while in the free state impregnation would appear to be effected. When the female larvæ become parasitic they undergo a metamorphosis, the stages of which have not been observed; but in the course of which the epiblast cells probably unite into a plasmodium.
The observations of Giard are in several points irreconcilable with those of Metschnikoff, but from the statements of the latter it appears possible that Giard has made two genera from the males and females of one species; and that Giard's account of an unequal segmentation followed by an epibolic gastrula, in one of his species, has arisen from two segmenting ova temporarily fusing together. Giard has given a description of internal gemmiparous reproduction, upon the accuracy of which doubts have been thrown by Metschnikoff. The affinities of the Orthonectidæ are as obscure as those of the Dicyemidæ; though there can be but little doubt that their organization has been much simplified in correlation with their parasitic habits. The origin of the genital products in the axial tissue is a feature they have in common with the Dicyemidæ.
BIBLIOGRAPHY.
(120) Alf. Giard. "Les Orthonectida classe nouv. d. Phylum des Vers." Journal de l'Anat. et de la Physiol., Vol. XV. 1879.
(121) El. Metschnikoff. "Zur Naturgeschichte d. Orthonectidæ." Zoologischer Anzeiger, No. 40-43, 1879.
[Ch. Julin. "Rech. sur l'organization et le devel. d'Orthonectides." Arch. Biol. Vol. III. 1882.
E. Metschnikoff. "Untersuchungen üb. Orthonectidæ." Zeit. f. Wiss. Zoologie, Vol. XXXV. 1881.
For general account of Orthonectidæ, vide Spengel. Biolog. Centralblatt, No. 6.]
V. PORIFERA
Although within the last few years greater advances have probably been made in our knowledge of the development of the Porifera than of any other group, yet there is much that is still very obscure, and it is not possible to make general statements applying to the whole group.
Calcispongiæ. The form which has so far been most completely worked out is Sycandra raphanus, one of the Calcispongiæ (Metschnikoff, Nos. 132 and 134, F. E. Schulze, Nos. 139 and 142), and I shall commence my account with the life history of this species.
The ovum in Sycandra as in other Spongida has the form of a naked amoeboid nucleated mass of protoplasm. From the analogy of the other members of the group, there is no doubt that it is fertilized by a male spermatic element, though this has not as yet been shewn to be the case--and the changes which accompany fertilization are quite unknown.
[FIG. 63. SUCCESSIVE STAGES IN THE SEGMENTATION OF SYCANDRA RAPHANUS. (Copied from F. E. Schulze.)
A. stage with eight segments still arranged in pairs, from above. B. side view of stage with eight segments. C. side view of stage with sixteen segments. D. side view of stage with forty-eight segments. E. view from above of stage with forty-eight segments. F. side view of embryo in the blastosphere stage, eight of the granular cells which give rise to the epiblast of the adult are present at the lower pole.
cs. segmentation cavity; ec. granular cells which form the epiblast; en. clear cells which form the hypoblast.]
The segmentation and early stages of development take place in the tissues of the parent. The segmentation is somewhat peculiar, though a modification of a regular segmentation. The ovum divides along a vertical plane, first into two, and then into four equal segments. But even when two segments are formed, each of them has one end pointed and the other broader. The pointed ends give rise to the ciliated cells of the future larva, and the broad ends to the granular cells. Instead of the next division taking place, as is usually the case, in a horizontal (equatorial) plane, it is actually effected along two vertical planes intermediate in position between the two first planes of segmentation. Eight equal segments are thus formed, each of which has the form of a pyramid. All the segments are situated in a single tier, and are so arranged as to give to the whole ovum the form of a flat cone, the apex of which is formed by the pointed extremities of the constituent segments (fig. 63 B). The apices of the segments do not however quite meet, but they leave a central space, which is an actual perforation (fig. 63 A) through the axis of the ovum, open at both ends. The first indications of this perforation appear when only four segments are present, and it is to be regarded as the homologue of the segmentation cavity of other ova. The next plane of division is horizontal (equatorial), and the apices of the eight cells are segmented off as a tier of small cells. At the completion of this division (fig. 63 C), the ovum is formed of sixteen cells arranged in two superimposed tiers. The ovum now assumes somewhat the form of a biconvex lens, in the axis of which the central perforation is still present. At the close of the next stage, forty-eight cells are present arranged in four tiers (fig. 63 D and E), the two outer tiers containing eight cells each, and the two inner sixteen. The two inner tiers probably arise by the simultaneous appearance of two equatorial furrows dividing the original tiers into two, and by the subsequent simple division of the cells of the two inner of the tiers so formed. At the close of the stage the eight basal cells become granular (fig. 63 F). At the same time the central part of the segmentation cavity becomes enlarged, while its terminal apertures become narrowed and finally, shortly after the end of this stage, closed. The axial perforation thus acquires the character of a closed segmentation cavity. While the ovum itself becomes at the same time a blastosphere.
[FIG. 64. LARVA OF SYCANDRA RAPHANUS AT PSEUDOGASTRULA STAGE, IN SITU IN THE MATERNAL TISSUES. (Copied from F. E. Schulze.)
me. mesoblast of adult; hy. collared cells forming hypoblast of the adult; en. clear cells of larva which eventually become involuted to form the hypoblast; ec. granular cells of larva which give rise to the epiblast, which at this stage are partially involuted.]
This stage nearly completes the segmentation: in the next one, the cells of the poles of the blastosphere increase in number, and the cells of the greater part of the blastosphere become columnar and ciliated, (fig. 64 en.) while the granular cells (ec.) increase to about thirty-two in number and appear to be (partially at least) involuted into the segmentation cavity, reducing this latter to a mere slit. This stage forms the last passed by the embryo in the tissues of the parent. The general position of the embryo while still in this situation may be gathered from fig. 64, representing the embryo in situ. The embryo is always placed close to one of the radial canals. From this situation it makes its way through the lining cells into a canal and is thence transported to the surrounding water. By the time the larva has become free, the semi-invaginated granular cells have increased in bulk and become everted so as to project very much more prominently than in the encapsuled state. To the gastrula stage, if it deserves the name, passed through by the embryo in the tissues of the parent, no importance can be attached.
[FIG. 65. TWO FREE STAGES IN THE DEVELOPMENT OF SYCANDRA RAPHANUS. (Copied from Schulze.)
A. Amphiblastula stage. B. A later stage after the ciliated cells have commenced to become invaginated. cs. segmentation cavity; ec. granular cells which will form the epiblast; en. ciliated cells which become invaginated to form the hypoblast.]
The larva, after it has left the parental tissues, has an oval form and is transversely divided into two areas (fig. 65 A). One of these areas is formed of the elongated, clear, ciliated cells, with a small amount of pigment near their inner ends (en.), and the other and larger area of the thirty-two granular cells already mentioned (ec.). Fifteen or sixteen of these are arranged as a special ring on the border of the clear cells. In the centre of the embryo is a segmentation cavity (c.s.) which lies between the granular and the clear cells, but is mainly bounded by the vaulted inner surface of the latter. This stage is known as the amphiblastula stage. During the later periods of the amphiblastula stage a cavity appears in the granular cells dividing them into two layers. After the larva has for some time enjoyed a free existence, a remarkable series of changes take place, which result in the invagination of the half of it formed of the clear cells, and form a prelude to the permanent attachment of the larva. The entire process of invagination is completed in about half an hour. The whole embryo first becomes flattened, but especially the ciliated half, which gradually becomes less prominent (fig. 65 B); and still later the cells composing it undergo a true process of invagination. As a result of this invagination the segmentation cavity is obliterated, and the larva assumes a compressed plano-convex form, with a central gastrula cavity, and a blastopore in the middle of the flattened surface. The two layers of the gastrula may now be spoken of as epiblast and hypoblast. The blastopore becomes gradually narrowed by the growth over it of the outer row of granular cells. When it has become very small the attachment of the larva takes place by the flat surface where the blastopore is situated. It is effected by protoplasmic processes of the outer ring of epiblast cells, which, together with the other epiblast cells, now become amoeboid. They become at the same time clearer and permit a view of the interior of the gastrula. Between the epiblast cells and the hypoblast cells which line the gastrula cavity there arises a hyaline structureless layer, which is more closely attached to the epiblast than to the hypoblast, and is probably derived from the former. A view of the gastrula stage after the larva has become fixed is given in fig. 66.
[FIG. 66. FIXED GASTRULA STAGE OF SYCANDRA RAPHANUS. (Copied from Schulze.)
The figure shews the amoeboid epiblast cells (ec.) derived from the granular cells of the earlier stage, and the columnar hypoblast cells, lining the gastrula cavity, derived from the ciliated cells of the earlier stage. The larva is fixed by the amoeboid cells on the side on which the blastopore is situated.]
There would seem according to Metschnikoff's observations (No. 134) to be a number of mesoblast cells interposed between the two primary layers, which he derives from the inner part of the mass of granular cells.
After invagination the cilia of the hypoblast cells can no longer be seen, and are probably absorbed; and their disappearance is nearly coincident with the complete obliteration of the blastopore, an event which takes place shortly after the attachment of the larva.
Not long after the closure of the blastopore, calcareous spicules make their appearance in the larva as delicate unbranched rods pointed at both extremities. They appear to be formed on the mesoblast cells situated between the epiblast and hypoblast[67]. The larva when once fixed rapidly grows in length and assumes a cylindrical form (fig. 67 A). The sides of the cylinder are beset with calcareous spicules which project beyond the surface, and, in addition to the unbranched forms, spicules are developed with three and four rays as well as some with a blunt extremity and serrated edge. The extremity of the cylinder opposite the attached surface is flattened, and, though surrounded by a ring of four-rayed spicules, is itself free from them. At this extremity a small perforation is formed leading into the gastric cavity, which rapidly increases in size and forms an exhalent osculum (os.). A series of inhalent apertures is also formed at the sides of the cylinder. The relative times of appearance of the single osculum and the smaller apertures are not constant for the different larvæ. On the central gastrula cavity of the sponge becoming placed in communication with the external water, the hypoblast cells lining it become ciliated afresh (fig. 67 B, en.) and develop the peculiar collar characteristic of the hypoblast cells of the Spongida (vide fig. 64, hy.). When this stage of development is reached we have a fully formed sponge of the type made known by Haeckel as Olynthus.
[67] Metschnikoff was the first to give this account of the development of the spicules in Sycandra, but Prof. Schulze has informed me by letter that he has arrived at the same result.
[FIG. 67. THE YOUNG OF SYCANDRA RAPHANUS SHORTLY AFTER THE DEVELOPMENT OF THE SPICULA. (Copied from Schulze.)
A. View from the side. B. View from the free extremity. os. osculum; ec. epiblast; en. hypoblast composed of ciliated cells. The terminal osculum and lateral pores are represented as oval white spaces.]
When young examples of Sycandra come in contact shortly after their attachment they appear to fuse together temporarily or else permanently. In the latter case colonies are produced by their fusion.
Amongst other calcareous sponges the larva of Ascandra contorta (Haeckel No. 126, Barrois No. 122) presents the typical amphiblastula stage, and so probably does that of Ascandra Lieberkühnii (Keller No. 128). In Leucandra aspera (Keller No. 128, Metschnikoff No. 134) the larva passes through an amphiblastula stage, but the characters of the cells of the two halves of the larva do not differ to nearly the same extent as in Sycandra.
Although the majority of calcareous sponges appear to agree in their mode of development with Sycandra, nevertheless the concordant researches of O. Schmidt (No. 138) and Metschnikoff (No. 134) have shewn that this is not true for the genus Ascetta (As. primordialis, clathrus and blanca).
The larvæ of these forms are very differently constituted to those of Sycandra. They have an oval form and are composed of a single row of ciliated columnar cells: their two extremities only differ in the cells at one extremity being longer than those at the other. Especially at the pole where the shorter cells are situated (Schmidt) a metamorphosis of the cells takes place. One after the other they lose their cilia, become granular, and pass into the interior of the vesicle. Here they become differentiated into two classes (Metschnikoff); one of larger and more granular cells, and the other of smaller cells with clearer protoplasm. Cells of the former class are mainly found at one of the poles. When the larva becomes free the cells in the interior of the vesicle increase in number and nearly fill up its central cavity. After a short free existence the larva becomes fixed, and the epiblast cells lose their cilia and become flattened. At a later period the large granular cells assume a radiate arrangement round a central cavity and become clearly marked out as the hypoblast cells. The smaller cells become placed between the epiblast and hypoblast and constitute the mesoblast.
Myxospongiæ. In this group Halisarca has been investigated by Carter (No. 123), Barrois (No. 122), Schulze (No. 141) and Metschnikoff (No. 134). The ova develop in the mesoblast, and when ripe occupy special chambers lined by a layer of epithelial cells. Schulze has found the spermatozoa of this genus of sponge and has been able to shew that the sexes may be distinct, though many species of Halisarca are hermaphrodite.
The segmentation is, roughly speaking, regular, and a segmentation cavity is early formed, which is never, as in Calcispongiæ, open at the poles. When the larva leaves the parent it is an oval vesicle formed of a single layer of columnar ciliated cells. Slight differences may be observed between the two extremities of the larvæ of most species. One of these--the hinder extremity--is directed backwards in swimming.
The further history of the larva has been investigated by Metschnikoff. He has found that the interior of the vesicle becomes gradually filled with mesoblast cells of a peculiar type, called by him rosette-cells, which are probably derived from the walls of the vesicle.
When the metamorphosis commences, the larva assumes a flattened form, and cells of a new type, viz. normal amoeboid cells, grow in amongst the rosette cells. The new cells are also derived from the epiblast. The larvæ appear to fix themselves by the hinder extremity. The cilia gradually disappear, and the epiblast cells flatten out and form a kind of cuticle. For some time the larva remains in the two-layered condition, but gradually canals (? ciliated chambers) lined by hypoblast cells become formed. They appear as closed spaces with walls of ciliated cells derived from the amoeboid cells, and the different parts of the system of chambers are established independently. In H. pontica the ciliated chambers are formed before the attachment of the larva. The development was not followed up to the formation of the pores placing the canal system in communication with the exterior.
The young sponges at a somewhat later stage have been studied by Schulze and Barrois. They are formed of an external layer of flattened cells, not clearly ciliated as in the adult, within which are a normal mesoblastic tissue, and several spherical chambers lined by ciliated cells exactly like the ciliated chambers of the full-grown sponge. Irregular invaginations of the epiblast give to the young sponge a honeycombed structure. The ciliated chambers in the youngest condition of the sponge are closed; but in slightly older examples they come into communication with the passages lined by hypoblast, and so indirectly with the external medium.
Ceratospongiæ. Amongst the true Ceratospongiæ the embryos of two of the Aplysinidæ, and of Spongelia and Euspongia have been to some extent worked out by Barrois and Schulze. The form worked out by Barrois is called by him Verongia rosea. The segmentation is nearly regular, but from the first the segments may be divided according to their constitution into two categories. At the close of segmentation the embryo is oval and covered by a single layer of columnar ciliated cells; these cells may however be divided into two categories, corresponding with those observable during the segmentation. A certain number are coloured red and form a definite circular mass at one pole, while the remainder, which constitute the major part of the embryo, have a pale yellowish colour. Those at the red pole lose their cilia in the free larva, but around the area formed by them is a special ring of long cilia. The chief peculiarity of the embryo (made known by Schulze) consists in the fact that the layer of cells which covers the embryo does not, as in other sponge embryos, simply enclose a space, but the interior of the embryo is formed of a mass of stellate cells like the normal mesoblast of full-grown sponges.
This feature is also characteristic of the embryos of Spongelia and Euspongia.
The embryo of the Gummineæ (Gummina mimosa) has been investigated by Barrois (No. 122), and has been shewn closely to resemble the typical larvæ of calcareous sponges; one-half being formed of elongated ciliated cells and the other of rounded granular ones.
Silicispongiæ. The development of marine silicious sponges is but very imperfectly understood. The larvæ of various forms--Reniera (Isodyctia), Esperia (Desmacidon), Raspailia, Halichondria, Tethya--have been described. Barrois has shewn that the egg segments regularly and that in the earlier stages a segmentation cavity is present. In the later stages the embryo appears to become solid. Externally there is a layer of ciliated cells, and within a mass of granular matter in which the separate cells cannot be made out. The granular matter projects at one pole, and forms a prominence possibly equivalent to the granular cells of Sycandra. In some forms, e.g. Reniera, the edge of the unciliated granular prominence may be surrounded by a row of long cilia. In later stages the granular material may project at both poles or even at other points. One remarkable feature in the development of the Silicispongiæ is the appearance of spicula between the ciliated cells and the central mass, while the larva is still free.
Professor Schulze has informed me that these spicula are developed in mesoblast cells; while the horny fibres of the sponge are developed as cuticular products of special mesoblast cells (spongioblasts).
The attachment and accompanying metamorphosis are so diversely described that no satisfactory account can be given of them. The general statements are in favour of the attachment taking place by the posterior extremity where the granular matter projects.
Carter especially gives a very precise account, with figures, of the attachment of the larva in this way. He also figures the appearance of an osculum at the opposite pole[68].
[68] Keller (No. 129) has recently given an account of the development of Halichondria (Chalinula) fertilis. He finds that there is an irregular segmentation, followed by a partial epibolic invagination, the inner mass of cells remaining exposed at one pole and forming there a prominence, equivalent to the granular prominence in the larvæ of other Silicispongiæ. The free-swimming larva resembles the larva of other Silicispongiæ in the possession of spicula, etc., and after becoming laterally compressed attaches itself by one of the flattened sides. A central cavity is formed in the interior with ciliated chambers opening into it, and is subsequently placed in communication with the exterior by the formation of an aperture which constitutes the osculum.
A very elaborate account of the development of Spongilla has been published in Russian by Ganin, of which a German abstract has also appeared (No. 124).
The ovum undergoes a regular segmentation and becomes a solid ova morula. An epiblast of smaller cells is early differentiated, and in the interior of the inner cells an archenteron becomes subsequently formed. The inner cells next become divided into an hypoblastic layer lining the archenteron, and a mesoblastic layer between this and the now ciliated epiblast. At the narrow hinder end of the embryo the mesoblast becomes thickened, and largely obliterates the archenteron. In this part of the mesoblast silicious spicula are formed. The larva becomes attached by its hinder extremity, and in the course of this process flattens itself out to a disc-like form. From the nearly obliterated archenteric cavity outgrowths take place which give rise to the ciliated chambers. These are not placed directly in communication with the exterior, but open, if I understand Ganin rightly, into a space in the mesoblast, which subsequently acquires an exterior communication--the primitive osculum. The subsequent pores and oscula are also formed as openings leading into the mesoblastic cavity, which communicates in its turn with the ciliated chambers.
It appears that in the present unsatisfactory state of our knowledge the larvæ of the Porifera may be divided into two groups: viz. (1) those which have the form of a blastosphere or else of a solid morula; (2) those which have the amphiblastula form.
In the former type the mesoblast and hypoblast are formed either from cells budded off from the outer cells of the blastosphere or from the solid inner mass of cells; while the outer ciliated cells become the epiblast. This type of larva, which is found in the majority of sponges, is very similar in its general characters and development to many Coelenterate planulæ.
The second type of larva is very peculiar, and though in its fully developed form it is confined to the Calcispongiæ, where it is the usual form, a larval type with the same characters is perhaps to be found in other sponges, e.g. amongst the Gumminæ, and amongst the Silicispongiæ where one-half of the embryo is without cilia, though in the case of the Silicispongiæ the cells of the ciliated part of the embryo correspond to the granular cells of the larva of Sycandra.
The later stages in the development of the larvæ of the Porifera are not similar to anything we know of in other groups.
It might perhaps be possible to regard sponges as degraded descendants of some Actinozoon type such as Alcyonium, with branched prolongations of the gastric cavity, but there does not appear to me to be sufficient evidence for doing so at present. I should rather prefer to regard them as an independent stock of the Metazoa.
In this connection the amphiblastula larva presents some points of interest. Does this larva retain the characters of an ancestral type of the Spongida, and if so, what does its form mean? It is, of course, possible that it has no ancestral meaning but has been secondarily acquired; but, assuming that this is not the case, it appears to me that the characters of the larva may be plausibly explained by regarding it as a transitional form between the Protozoa and Metazoa. According to this view the larva is to be considered as a colony of Protozoa, one-half of the individuals of which have become differentiated into nutritive forms, and the other half into locomotor and respiratory forms. The granular amoeboid cells represent the nutritive forms, and the ciliated cells represent the locomotor and respiratory forms. That the passage from the Protozoa to the Metazoa may have been effected by such a differentiation is not improbable on a priori grounds.
While the above view seems fairly satisfactory for the free-swimming stage of the larval sponge, there arises in the subsequent development a difficulty which appears at first sight fatal to it. This difficulty is the invagination of the ciliated cells instead of the granular ones. If the granular cells represent the nutritive individuals of the colony, they, and not the ciliated cells, ought most certainly to give rise to the lining of the gastrula cavity, according to the generally accepted views of the morphology of the Spongida. The suggestion which I would venture to put forward in explanation of this paradox involves a completely new view of the nature and functions of the germinal layers of adult Spongida.
It is as follows:--When the free-swimming ancestor of the Spongida became fixed, the ciliated cells by which its movements used to be effected must have to a great extent become functionless. At the same time the amoeboid nutritive cells would need to expose as large a surface as possible. In these two considerations there may, perhaps, be found a sufficient explanation of the invagination of the ciliated cells, and the growth of the amoeboid cells over them. Though respiration was, no doubt, mainly effected by the ciliated cells, it is improbable that it was completely localized in them, but they were enabled to continue performing this function through the formation of an osculum and pores. The collared cells which line the ciliated chambers, or in some cases the radial tubes, are undoubtedly derived from the invaginated cells, and, if there is any truth in the above suggestion, the collared cells in the adult sponge must be mainly respiratory and not digestive in function, while the epiblastic cells, which in most cases line the inhalent passages through its substance[69], ought to be employed to absorb nutriment. The recent researches of Metschnikoff (No. 134) on this head shew that the nutriment is largely carried into the mesoblast cells, which in Sycandra appear to be derived from the granular cells, and also that it is taken up by the cells which line the passages, though not by the superficial epiblast cells. Whether the collared cells generally absorb nutriment is not clear from his statements: but he finds that they do not do so in Silicispongiæ.
[69] That the greater part of the flat cells which line the passages of most Sponges are really derived from epiblastic invaginations appears to me to be proved by Schulze's and Barrois' observations on the young fixed stages of Halisarca. Schulze's (No. 140) observations have however proved that the flat cells lining the axial gastric chamber of Sycandra are hypoblastic in origin, and the observations of Keller (No. 129) and Ganin (No. 124) have led to the same result for the flat epithelium lining part of the passages of the Silicispongiæ.
Professor Schulze has informed me by letter that he finds the collared cells to be respiratory in function, while the cells derived from the granular cells in Sycandra are nutritive. Carter[70], on the contrary, from his observations on Spongilla, has fully satisfied himself that the food is absorbed by the cells lining the ciliated chambers.
[70] "On the Nutritive and Reproductive Processes of Sponges." Ann. and Mag. of Nat. Hist., Vol. IV. Ser. V. 1879.
If it is eventually proved by further experiments on the nutrition of sponges, that digestion is mainly carried on by the general cells lining the passages and the mesoblast cells, and not for the most part by the ciliated cells, it is clear that the epiblast, mesoblast and hypoblast of sponges will not correspond with the similarly named layers in the Coelenterata and other Metazoa. The invaginated hypoblast will be the respiratory layer and the epiblast and mesoblast the digestive and sensory layers; the sensory function being probably mainly localized in the epithelium on the surface, and the digestive one in the epithelium lining the passages and in the mesoblast. Such a fundamental difference in the primary function of the germinal layers between the Spongida and the other Metazoa, would necessarily involve the creation of a special division of the Metazoa for the reception of the former group.
BIBLIOGRAPHY.
(122) C. Barrois. "Embryologie de quelques éponges de la Manche." Annales des Sc. Nat. Zool., VI. ser., Vol. III. 1876.
(123) Carter. "Development of the Marine Sponges." Annals and Mag. of Nat. Hist., 4th series, Vol. XIV. 1874.
(124) Ganin[71]. "Zur Entwicklung d. Spongilla fluviatilis." Zoologischer Anzeiger. Vol. I. No. 9, 1878.
(125) Robert Grant. "Observations and Experiments on the Structure and Functions of the Sponge." Edinburgh Phil. J., Vol. XIII. and XIV., 1825, 1826.
(126) E. Haeckel. Die Kalkschwämme, 1872.
(127) E. Haeckel. Studien zur Gastræa-Theorie. Jena, 1877.
(128) C. Keller. Untersuchungen über Anatomie und Entwicklungsgeschichte einiger Spongien. Basel, 1876.
(129) C. Keller. "Studien üb. Organisation u. Entwick. d. Chalineen." Zeit. f. wiss. Zool., Bd. XXVIII. 1879.
(130) Lieberkühn. "Beitr. z. Entwick. d. Spongillen." Müller's Archiv, 1856.
(131) Lieberkühn. "Neue Beiträge zur Anatomie der Spongien." Müller's Archiv, 1859. (132) El. Metschnikoff. "Zur Entwicklungsgeschichte der Kalkschwämme." Zeit. f. wiss. Zool., Bd. XXIV. 1874.
(133) El. Metschnikoff. "Beiträge zur Morphologie der Spongien." Zeit. f. wiss. Zool., Bd. XXVII. 1876.
(134) El. Metschnikoff. "Spongeologische Studien." Zeit. f. wiss. Zool., Bd. XXXII. 1879.
(135) Miklucho-Maklay. "Beiträge zur Kenntniss der Spongien." Jenaische Zeitschrift, Bd. IV. 1868.
(136) O. Schmidt. "Zur Orientirung über die Entwicklung der Schwämme." Zeit. f. wiss. Zool., Bd. XXV. 1875.
(137) O. Schmidt. "Nochmals die Gastrula der Kalkschwämme." Archiv für mikrosk. Anat., Bd. XII. 1876.
(138) O. Schmidt. "Das Larvenstadium von Ascetta primordialis und Asc. clathrus." Archiv für mikrosk. Anatomie, Bd. XIV. 1877.
(139) F. E. Schulze. "Ueber den Bau und die Entwicklung von Sycandra raphanus." Zeit. f. wiss. Zool., Bd. XXV. 1875.
(140) F. E. Schulze. "Zur Entwicklungsgeschichte von Sycandra." Zeit. f. wiss. Zool., Bd. XXVII. 1876.
(141) F. E. Schulze. "Untersuchung üb. d. Bau, etc. Die Gattung Halisarca." Zeit. f. wiss. Zool., Bd. XXVIII. 1877.
(142) F. E. Schulze. "Untersuchungen üb. d. Bau, etc. Die Metamorphose von Sycandra raphanus." Zeit. f. wiss. Zool., Bd. XXXI. 1878.
(143) F. E. Schulze. "Untersuchungen ü. d. Bau, etc. Die Familie Aplysinidæ." Zeit. f. wiss. Zool., Bd. XXX. 1878.
(144) F. E. Schulze. "Untersuchungen ü. d. Bau, etc. Die Gattung Spongelia." Zeit. f. wiss. Zool., Bd. XXXII. 1878.
[71] There is a Russian paper by the same author, containing a full account, with clear illustrations, of his observations.
VI. COELENTERATA[72]
[72] I. HYDROZOA. 1. Hydromedusæ. {Hydroidea. {Trachymedusæ. 2. Siphonophora. {Calycophoridæ. {Physophoridæ. 3. Acraspeda. II. ACTINOZOA. 1. Alcyonaria. (Octocoralla.) 2. Zoantharia. (Hexacoralla.) III. CTENOPHORA.
Hydroidea. The most typical mode of development of the Hydroidea is that in which the segmentation leads directly to the formation of a free ciliated two-layered larva, known since Dalyell's observations as a planula. The planula is characteristic of almost all the Hydromedusæ with fixed hydrosomes including the Hydrocoralla (Stylasteridæ and Millepora), the most important exceptions being the genus Tubularia and one or two other genera, and the fresh-water Hydra.
In a typical Sertularian the segmentation is approximately regular[73] and ends according to the usual accounts in the formation of a solid spherical mass of cells. A process of delamination now takes place, which leads to the formation of a superficial layer of cubical or pyramidal cells, enclosing a central solid mass of more or less irregularly arranged cells.
[73] For a detailed description of the development of a single species the reader referred to Allman's description of Laomedia flexuosa, No. 149, p. 85 et seq.
The embryo, in the cases in which it is still contained within the sporosack, now begins to exhibit slight changes of form, and one extremity of it begins to elongate. It soon becomes free, and rapidly assumes an elongated cylindrical form, while a coating of cilia, by means of which it moves sluggishly about, appears on its outer surface. A central cavity appears in the interior, and the inner cells form themselves into a definite hypoblast. The larva has now become a planula, and consists of a closed sack with double walls. It continues for some few days to move about, but eventually drops its cilia, and becomes dilated at one extremity, by which it then becomes attached. The base of attachment becomes gradually enlarged so as to form a disc, which spreads out and is frequently divided by fissures into radiating lobes. The free extremity becomes enlarged to form the eventual calyx.
Over the whole exterior a delicate pellicle--the future perisarc--now becomes secreted. Round the edge of the anterior enlargement a row of tentacles makes its appearance. These, in the embryos of the Tubularian genera, lie some little way behind the apex of the body. After a certain time the perisarc, which has hitherto been continuous, becomes ruptured in the region of the calyx, and the tentacles become quite free. At about the same period a mouth is formed at the oral apex.
[FIG. 68. THREE LARVA STAGES OF EUCOPE POLYSTYLA. (After Kowalevsky.)
A. Blastosphere stage with hypoblast spheres becoming budded off into the central cavity. B. Planula stage with solid hypoblast. C. Planula stage with a gastric cavity. ep. epiblast; hy. hypoblast; al. gastric cavity.]
The development of Eucope polystyla (fig. 68), one of the Campanularidæ, deviates according to Kowalevsky (No. 147) in somewhat important points from the usual type. The whole development takes place after the deposition of the ovum. The segmentation results in the formation of a single-walled blastosphere with a large central cavity (fig. 68 A). This cavity, somewhat as in Ascetta, becomes filled up with a not clearly (?) cellular material derived from the walls of the blastosphere, which must be regarded as the hypoblast (fig. 68 B). The larva elongates and becomes ciliated, and the epiblast at its two extremities becomes thickened, and is stated by Kowalevsky also to become divided into two layers. The alimentary cavity appears as a slit in the middle of the hypoblast (fig. 68 C). The cilia after a time disappear, and the larva then becomes fixed by one extremity. It flattens itself out into a disc-like form, becomes divided into four lobes, and covered by a cuticle (perisarc). From the disc the stalk grows out which dilates at its free extremity into the calyx.
[FIG. 69. LONGITUDINAL SECTION THROUGH A LARVA OF TUBULARIA MESEMBRYANTHEMUM WHILE STILL IN THE GONOPHORE. The lower end is the oral one.
ep. epiblast; hy. hypoblast of tentacle; en. enteric cavity.]
In both the groups (Tubularia and Hydra) which are exceptional in not having a ciliated planula stage, its absence may be put down to an abbreviation of the development, and in fact a two-layered quiescent stage, through which the embryo passes, may be regarded as representing the planula stage.
The development of Tubularia, which has been described in detail by Ciamician, takes place in the gonophore[74]. The segmentation is irregular and leads to the formation of an epibolic gastrula, four large central cells constituting the hypoblast[75]. The larva now elongates, and grows out laterally into two processes which constitute the first pair of tentacles. At this stage it closely resembles the larvæ of some Medusæ. Additional tentacles are soon formed; and a central cavity appears in the hypoblast, the cells of which have in the meantime become more numerous (fig. 69). The tentacles are directed towards the aboral side, which is considerably more prominent than the oral one. They contain a hypoblastic axis. The aboral end continues to grow and the tentacles gradually assume a horizontal position. A constriction now appears, dividing the larva into an aboral portion which will eventually form the stalk, and an oral portion. At the apex of the latter a row of short tentacles--the future oral tentacles--now appears. The larva has at this stage the form known as Actinula. In this condition it becomes hatched, and shortly afterwards it becomes fixed by the aboral end and grows into a colony.
[74] Vide Ciamician, Zeit. f. wiss. Zool., Bd. XXXII. 1879.
[75] In examining the segmentation by means of sections I have failed to detect an epibolic gastrula or such irregularity as is described by Ciamician. Prof. Kleinenberg informs me that he has been equally unsuccessful.
The development of Myriothela (Allman, No. 150) takes place on the Tubularian type. The ovum invested by a delicate capsule becomes freed by the rupture of the gonophore, and is then taken up by the remarkable claspers characteristic of the genus. In the claspers it becomes fecundated and undergoes its further development. After segmentation a gastric cavity is formed, and provisional tentacles arise as a series of conical involutions which subsequently become evoluted. Permanent tentacles are formed as conical papillæ on a truncated oral process. After hatching it has a few days' free existence, and then becomes attached, and loses its provisional tentacles.
Although Hydra itself constitutes the simplest type of Hydrozoon, its development, which has been fully investigated by Kleinenberg (No. 161), is in some respects a little exceptional. The segmentation is regular, but a segmentation cavity is not formed. The peripheral layer of cells gradually becomes converted into a chitinous membrane, which is perhaps homologous with the perisarc of marine forms. Between the membrane and the germ a second pellicle makes its appearance. The above changes require about four days for their completion, but there next sets in a period of relative quiescence which lasts for some 6-8 weeks. During this period the remaining development is completed. The cells of the germ first fuse together. In the interior of the protoplasm a clear excentric space arises, which gradually extends itself and forms the rudiment of the gastric cavity. The outer shell in the meantime becomes less firm, and is finally burst and thrown off, owing to the expansion of the embryo within.
The outermost layer of the protoplasm becomes, relatively to the inner layer, clear and transparent, and there thus arises an indication of a division of the walls of the archenteric cavity into two zones, or layers. These layers, which form the epiblast and hypoblast, are definitely established on the appearance of cells with contractile tails[76] in the clear outer zone, between which the interstitial epiblast cells subsequently arise.
[76] These cells are the so-called nerve-muscle cells. Their nature is discussed in the second part of this work.
The embryo, still forming a closed double-walled sack, elongates itself, and at one pole its wall becomes very thin. And at this point a rupture takes place which gives rise to the mouth. Simultaneously with the mouth the tentacles become formed as hollow processes, according to Mereschkowsky two being formed first and subsequently the others in pairs. Very shortly afterwards the hitherto uniform hypoblast becomes divided up into distinct cells. The thin inner pellicle which persists after the rupture of the outer membrane becomes in the meantime absorbed. With these changes the embryo practically acquires the characters of the adult.
Trachymedusæ. Amongst the Trachymedusæ, which as has now been satisfactorily established develop directly without alternations of generations, the embryology of species both of the Geryonidæ and the Æginidæ has been studied.
In all the types so far investigated the hypoblast is formed by delamination, and there is a more or less well-marked planula stage.
[FIG. 70. DIAGRAMMATIC FIGURE SHEWING THE DELAMINATION OF THE OVUM OF GERYONIA. (Copied from Fol.)
cs. segmentation cavity; a. endoplasm; b. ectoplasm. The dotted lines shew the course of the next planes of division.]
The development of Geryonia (Carmarina) hastata has been studied by Fol (No. 155) and Metschnikoff (No. 163)[77]. The ovum, when laid, is invested by a delicate vitelline membrane and mucous covering. Its protoplasm is formed of an outer granular and dense layer, and a central mass of a more spongy character. The segmentation is complete and regular, and up to the time when thirty-two segments have appeared each segment is composed of both constituents of the protoplasm of the ovum. A segmentation cavity appears when sixteen segments are formed, and becomes somewhat larger at the stage with thirty-two. At this stage the process of delamination commences. Each of the thirty-two segments, as shewn in the accompanying diagram (fig. 70), becomes divided into two unequal parts. The smaller of these is formed almost entirely of granular material; the larger contains portions of both kinds of protoplasm. In the next segmentation the thirty-two large cells only are concerned, and in each of these the line of division passes between the granular and the transparent protoplasm. The sixty-four lenticular masses of granular protoplasm thus formed constitute an outer closed epiblastic vesicle, within which the thirty-two masses of transparent protoplasm form an hypoblastic vesicle. The embryo at this stage is shewn in optical section in fig. 71.
[77] In the succeeding account I have followed Fol, who differs in some minor points from Metschnikoff.
The epiblastic vesicle now grows rapidly, while the hypoblastic vesicle remains nearly passive and becomes somewhat lens-shaped. At one point its wall comes in close contact with the epiblast. Elsewhere a wide cavity is developed between the two vesicles which becomes filled with gelatinous tissue. At this period cilia appear on the surface, and the larva becomes a planula.
[FIG. 71. EMBRYO OF GERYONIA AFTER DELAMINATION. (After Fol.)
ep. epiblast; hy. hypoblast.]
The succeeding changes lead rapidly to the formation of a typical Medusa. Where the epiblast and hypoblast are in contact the former layer becomes thickened and forms a disc-shaped structure. The centre of this becomes somewhat protuberant, fuses with the hypoblast and then becomes perforated to form the mouth (fig. 72 o). The edge of the disc forms a thickened ridge, the rudiment of the velum (v), which is entirely formed of epiblast. At its edge six tentacles (t) arise, into which are continued solid prolongations of the wall of the now somewhat hexagonal gastric chamber. The hypoblastic axes of the tentacles soon lose their connection with the gastric wall.
[FIG. 72. OPTICAL SECTION THROUGH THE ORAL POLE OF GERYONIA AFTER THE APPEARANCE OF THE GELATINOUS TISSUE OF THE DISC. (After Fol.)
o. mouth; v. velum; t. tentacle. The shaded part represents the gelatinous tissue.]
Up to this time the larva has retained a more or less spherical form, and the cavity on the under side of the umbrella has not yet become developed. The latter now becomes established by the whole disc assuming a vaulted form with the concavity directed downwards. The lining of the cavity so formed is derived from the epiblast of the disc already spoken of.
The exact mode of formation of the gastrovascular canals has not been worked out. It has however been established by the researches of the Hertwigs (No. 146) and Claus (No. 153) that the radial and circular vessels of this system are connected together in adult Medusæ by an hypoblastic lamella; so that these canals would seem to be the remnants of an once-continuous gastric cavity. This mode of formation is established in the case of the medusiform buds; and it would therefore seem, as pointed out by the Hertwigs, a fair deduction that it occurs in the larva--a conclusion which is confirmed by the primitive extension of the gastric cavity to the edge of the disc at the time when its walls give rise to the solid axes of the tentacles. In the course of the subsequent retirement of the gastric cavity from the edge of the disc the gastrovascular canals probably take their origin, though Fol was unable to follow the changes which result in their formation.
On the completion of the above changes the larva has become a fully formed Medusa, but it undergoes a not inconsiderable metamorphosis before the attainment of the adult state.
[FIG. 73. A THREE-DAYS' LARVA OF ÆGINOPSIS WITH TWO TENTACLES. (After Metschnikoff.)
m. mouth; t. tentacle.]
Two species of Æginidæ have been studied by Metschnikoff (163), viz. Polyxenia leucostyla (Ægineta flavescens), and Æginopsis mediterranea. In both of these forms the segmentation results in the formation of an elongated two-layered ciliated planula, without a central cavity. The two ends of this grow out into two long processes--the rudiments of a pair of at first aborally directed arms--which contain a solid hypoblastic axis (fig. 73). At this stage the larva closely resembles the larva of Tubularia. An alimentary cavity is hollowed out in the centre of the hypoblast which soon opens by a wide oral aperture (m). A second pair of arms becomes formed, which are at first much shorter than the original pair; with their formation a radial symmetry is acquired. Sense organs become at the same time developed, and the whole embryo assumes a medusiform character. Fresh tentacles arise, the velum and cavity of the umbrella become established, but these changes do not involve any points of very special interest.
Siphonophora. The development of the Siphonophora has been the subject of careful investigation by Haeckel (158) and Metschnikoff (163). The ova are large and usually (except Hippopodius) without a membrane.
They are formed of a peripheral denser layer of protoplasm and a central spongy mass. They usually undergo their entire development in the water. In some instances they have been successfully reared by artificial impregnation.
As an example of the Calycophoridæ I shall take Epibulia aurantiaca, a form allied to Diphyes, the development of which has been studied by Metschnikoff[78].
[78] In my description of the development of the Siphonophora I employ Huxley's terminology.
[FIG. 74. THREE LARVAL STAGES OF EPIBULIA AURANTIACA. (After Metschnikoff.)
A. Planula stage. B. Six-days' larva with nectocalyx (nc) and tentacle (t). C. Somewhat older larva with gastric cavity. ep. epiblast; hy. hypoblast; so. somatocyst; nc. nectocalyx; t. tentacle; c. large yolk cells; po. polypite.]
There is a regular segmentation, unaccompanied by the formation of a segmentation cavity. At its close the ovum becomes a spherical ciliated embryo. This embryo soon becomes elongated, and its cells differentiate themselves into a central and a peripheral layer--the epiblast and the hypoblast (fig. 74 A). At this stage the larva has the typical planula form. The epiblast is especially thickened at a pole, which may be called the oral pole, and towards the side of this, which will be spoken of as the ventral side. Adjoining this thickened layer of epiblast a special thin layer of hypoblast becomes differentiated, which in opposition to the main mass of large nutritive cells forms the true hypoblastic epithelium (fig. 74 B, hy). On this thickening two prominences make their appearance (fig. 74 B). The oral of these is the rudiment of a tentacle (t), and the aboral of a nectocalyx (nc).
[FIG. 75. AN ADVANCED LARVA OF EPIBULIA AURANTIACA WITH ONE LARGE NECTOCALYX. (After Metschnikoff.)
so. somatocyst; nc. second imperfectly developed nectocalyx; hph. hydrophyllium; po. polypite; t. tentacle.]
The former of these elongates itself in succeeding stages into a process of both epiblast and hypoblast. The central part of the nectocalyx on the other hand appears to originate from a thickening of the epiblast in which the cavity of the bell becomes subsequently hollowed out. Between this part and the external epiblast which gives origin to the outermost layer of the nectocalyx a layer of hypoblast is interposed. When the nectocalyx has become to a certain extent established a cavity--the commencement of the primitive gastrovascular cavity of the adult--appears in the general hypoblast between the epithelial and nutritive layers in the immediate neighbourhood of its attachment. This cavity becomes prolonged into the nectocalyx to form the four gastrovascular canals; while the hypoblast at the upper end of the nectocalyx forms the somatocyst (fig. 74 C, so). The primitive enteric cavity once formed rapidly extends, especially in an oral direction (fig. 74 C), and forms a widish cavity in the oral part of the embryo. At the pole of this part (fig. 74, po) is eventually formed the opening of the mouth, and the contained cavity becomes in a special sense the gastric cavity. This region of the embryo may be spoken of as the polypite. The nectocalyx grows with great rapidity and soon forms by far the most prominent part of the larva (fig. 75). The true gastric region or polypite (fig. 75, po) continues also to grow, and a mouth becomes formed at its extremity. The aboral end of the original body of the embryo gradually atrophies.
At the junction of the nectocalyx and polypite the coenosarc becomes formed, and rudiments of a second nectocalyx (nc) and second polypite early become visible; while a hydrophyllium is formed as a bud which covers over the first polypite and tentacle (hph). With the development of the hydrophyllium the first segment, if the term may so be used, is complete. The second segment of which a rudiment is already present as a second polypite is intercalated between the first segment and the nectocalyces.
[FIG. 76. TWO STAGES IN THE DEVELOPMENT OF STEPHANOMIA PICTUM. (After Metschnikoff.)
A. Stage after the delamination. ep. epiblastic invagination to form pneumatocyst. B. Later stage after the formation of the gastric cavity in the solid hypoblast, po. polypite; t. tentacle; pp. pneumatophore; ep. epiblastic invagination to form pneumatocyst; hy. hypoblast surrounding pneumatocyst.]
Amongst the Physophoridæ there is a considerable range of variation in development; though the variations concern for the most part not very important points. The simplest type hitherto observed is that of Stephanomia (Halistemma) pictum. The segmentation and formation of a two-layered planula (fig. 76) take place in the usual way. Between the solid central mass of nutritive hypoblast cells and the epiblast an epithelial hypoblastic layer becomes interposed which undergoes a special thickening at the aboral pole. At this pole a solid involution of epiblast next becomes formed, to which a layer of hypoblast becomes applied. The structure so formed is the rudiment of the pneumatocyst (ep). In the next stage the air-cavity of the pneumatocyst becomes established within the epiblast.
The gastrovascular cavity is formed in the midst of the nutritive hypoblast cells, which then become rapidly absorbed leaving the gastrovascular cavity entirely enclosed by the epithelial layer of hypoblast (fig. 76 B).
By the above changes the more important organs of the larva have become established. The one end forms the pneumatophore, and the other, the oral part, the polypite. Between the two there is already present the rudiment of a tentacle, and a second tentacle soon becomes formed. The mouth arises as a perforation at the oral end of the larva.
The pneumatophore contains a prolongation of the gastrovascular cavity, the fluid in which bathes the outer hypoblastic wall of the pneumatocyst. It has however no communication with the enclosed cavity of the pneumatocyst. In the later developmental stages the size of the pneumatophore becomes immensely reduced in comparison with the remainder of the larva.
The development of Physophora agrees closely with that of Stephanomia except in one somewhat important point, viz. in the development of a provisional hydrophyllium. This arises as a prominence at the aboral pole, containing a prolongation of the gastrovascular cavity. Between the epiblast and hypoblast of the prominence gelatinous tissue becomes deposited, and the hydrophyllium is thus converted into a large umbrella-like organ enclosing the polypite. The two together have a close resemblance to an ordinary Medusa, the polypite forming the manubrium, and the hydrophyllium the umbrella. The hydrophyllium is eventually thrown off.
An important type of Physophorid development is exemplified in Crystalloides, a genus closely allied to Agalma. In this type the greater part of the original ovum, instead of directly giving rise to the polypite, becomes a kind of yolk-sack, from which the polypite is secondarily budded (fig. 77, yk). Agalma sarsii is in this respect intermediate between Crystalloides and Physophora. Both these types are remarkable for developing a series of provisional hydrophyllia (fig. 77, h.ph.). In both genera the first of these develops as in Physophora, and for a long time is the only one functional.
The conclusions to be drawn from the above description may be summed up as follows. In all the Siphonophora, so far observed, the starting point for further development is a typical ciliated two-layered planula. The inner layer or hypoblast is mainly formed of large nutritive cells. From these cells an epithelial hypoblastic layer becomes secondarily differentiated, the exact relations of which differ somewhat in the various types. The nutritive cells themselves do not appear to become directly converted into the permanent hypoblastic tissues. The development of the adult from the planula commences by the thickening of the epiblastic layer, usually at one pole (the future proximal or aboral pole), and the formation at this pole of a series of bud-like structures (in the growth of which both embryonic layers have a share), which become converted into the hydrophyllia, nectocalyces etc. The main oral part of the planula becomes generally converted into the polypite, though in some instances (Crystalloides) it remains as a yolk-sack, and only secondarily gives rise to a polypite.
Two very different views have been taken as to the nature of the various component parts of the Siphonophora, and the embryological evidence has been appealed to by both sides in confirmation of their views. By Huxley and Metschnikoff the various parts--nectocalyces, hydrophyllia, hydrocysts, polypites, generative gonophores etc. are regarded as simple organs, while by Leuckart, Haeckel, Claus etc. they are regarded as so many different individuals forming a compound stock. The difference between these two views is not merely as to the definition of an individual[79]. The question really is, are these parts originally derived by the modification of complete zooids like the gonophores and trophosomes of the fixed Hydrozoa stocks, or are they structures derived from the modification of the tentacles or some other parts of a single zooid?
[79] From the expressions used by Huxley, Anatomy of Invertebrated Animals, p. 149, it appears to me possible that his opposition to Leuckart's view is mainly as to the nature of the individual.
[FIG. 77. LARVA OF CRYSTALLOIDES, (After Haeckel.)
h.ph. hydrophyllium; h. hydrocyst; t. tentacle; pp. pneumatophore; po. polypite; yk. yolk-sack.]
The difficulty of deciding this point on embryological evidence depends on the fact that ontologically a tentacle and a true bud arise in the same way, viz. as papilliform outgrowths containing prolongations of both the primitive germinal layers. The balance of evidence is nevertheless in my opinion in favour of regarding the Siphonophora as compound stocks, and the views of Claus on this subject (Zoologie, p. 271) appear to me the most satisfactory.
The most primitive condition is probably that like Physophora in an early stage with an hydrophyllium enclosing a polypite (cf. Haeckel and Metschnikoff). In this condition the whole larva may be compared to a single Medusa in which the primitive hydrophyllium represents the umbrella of the Medusa, and the polypite the manubrium. The tentacle which appears so early is probably not to be regarded as a modified zooid, but as a true tentacle. The absence of a ring of tentacles is correlated with the bilateral symmetry of the Siphonophora.
The primitive zooid of a Siphonophora stock is thus a Medusa. Like Sarsia and Wilsia this Medusa must be supposed to have been capable of budding. The ordinary nectocalyces by their resemblance to the umbrellas of typical Medusæ are clearly such buds of the medusiform type. The same may be said of the pneumatophore, which, as pointed out by Metschnikoff, is identical in its development with a nectocalyx. Both are formed by a solid process of epiblast in which a cavity--the cavity of the nectocalyx or pneumatocyst--is eventually hollowed out. Around this there appears a double layer of hypoblast containing a prolongation of the gastrovascular cavity; and this is in its turn enclosed by a layer of epiblast which forms the covering of the convex surface of the nectocalyx and the external epiblast of the pneumatophore.
The generative gonophores are clearly also zooids, and the hydrophyllia are probably a rudimentary form of umbrella. In many cases (Epibulia, Stephanomia, Halistemma etc.) the hydrophyllium of the primitive polypite (manubrium) is absent. In such instances it is necessary to suppose that the umbrella of the primitive zooid of the whole colony has become aborted. Leuckart originally took a somewhat different view from the above in that he regarded the starting point of the Siphonophora to be a compound fixed Hydrozoon stock, which became detached and free-swimming.
Acraspeda[80]. The embryonic development of several of the forms of the Acraspeda has been investigated by Kowalevsky (No. 147) and Claus (No. 153). Their observations seem to point to an invaginate gastrula being characteristic of this group.
[80] I use this term for the group, often known as the Discophora, which includes the Pelagidæ, Rhizostomidæ, and Lucernaridæ.
Amongst the forms with alternations of generations and a fixed larval form Chrysaora and Cassiopea have been most fully investigated. The ovum of the former undergoes the first embryonic phases while still in the ovary. In the latter it is enclosed amongst the oral processes. A complete and more or less regular segmentation leads to the formation of a single-walled blastosphere with a small segmentation cavity. The wall of the blastosphere next becomes invaginated, giving rise to an archenteron (fig. 78 A). The blastopore soon closes up, and the archenteron is converted into a closed sack completely isolated from the epiblast (fig. 78 B). The surface of the larva becomes in the meantime covered with cilia. The free larval stage thus reached is similar to the ordinary Hydrozoon planula. After the closure of the blastopore the larva becomes elongated, and one end becomes narrowed. By this narrowed extremity the larva soon attaches itself, and at the opposite and broader end a fresh involution of the epiblast appears (fig. 78 C); this gives rise to the stomodæum, which is placed in communication with the archenteron on the absorption of the septum dividing them. The relation of the stomodæum to the original blastopore has not been determined.
At the point of attachment there is developed a peculiar pedal disc, and around the mouth there appears a fold of epiblast which gives rise to an oral disc (fig. 78 D). Two tentacles first make their appearance, but one of these is primarily much the largest, though eventually the second overtakes it in its growth. A second pair of tentacles next becomes formed, giving to the larva a 4-radial symmetry. Between these four new tentacles subsequently sprout out, and in the intermediate planes four ridge-like thickenings of the hypoblast, projecting into the cavity of the stomach, make their appearance. They imperfectly divide the stomach into four chambers, to each of which one of the primary tentacles corresponds; they may be regarded as homologous with the mesenteries of the Actinozoa. The number of tentacles goes on increasing somewhat irregularly up to sixteen. All the tentacles contain a solid hypoblastic axis. Muscular elements are developed from the epiblast.
[FIG. 78. FOUR STAGES IN THE DEVELOPMENT OF CHRYSAORA. (After Claus.)
A. Gastrula stage. B. Stage after closure of blastopore. C. Fixed larva with commencing stomodæum. D. Fixed larva with mouth, short tentacles, etc. ep. epiblast; hy. hypoblast; st. stomodæum; m. mouth; bl. blastopore.]
With the above changes the so-called Hydra tuba or Scyphistoma form is reached (vide fig. 85). The peculiar strobilization of this form is dealt with in the section devoted to the metamorphosis.
Aurelia is stated by Kowalevsky to develop in the same way as Cassiopea; and the one stage of Rhizostoma observed is that in which it has a (probably invaginate) gastrula form.
In Pelagia the ovum directly gives rise to a form like the parent. The segmentation and the invagination take place nearly as in Cassiopea, but the archenteric cavity is relatively much smaller, and the large space between it and the epiblast becomes filled with the gelatinous tissue which forms the umbrella. The blastopore does not appear to close but to become directly converted into the mouth. As in Cassiopea the larva takes a somewhat four-sided pyramidal form. The mouth is placed at the base. The pyramid becomes subsequently flatter, and at the four corners four tentacles grow out which increase to eight by division. The flattening continues till the larva reaches a form hardly to be distinguished from the Ephyra resulting from the strobilization of the fixed Scyphistoma form of other Acraspeda.
Alcyonidæ. In the Alcyonidæ the segmentation appears always to lead to the formation of a solid morula, which becomes a planula by delamination. The true enteric cavity is formed by an absorption of the central cells, but the axial portion of the gastric cavity and mouth are formed by an epiblastic invagination.
The development of these types has been mainly studied by Kowalevsky (147), and my knowledge of his results is derived from German abstracts of the original Russian memoirs.
In Alcyonium palmatum the impregnation is external. The segmentation is very exceptional in character. It commences with the formation of a series of irregular prominences on the surface of the ovum, which become segmented off to form a superficial layer of epiblast cells. The inner mass of protoplasm then divides up into polygonal cells to form the hypoblast, which would thus seem to be formed by a kind of delamination. In Clavularia crassa (No. 168) there is a complete segmentation followed by a delamination. The larva of Al. palmatum elongates and becomes ciliated, and so assumes the characters of a typical planula. The central hypoblast is formed of an outer granular stratum with imperfectly differentiated cells--the true hypoblast--and an inner homogeneous mass with vacuoles.
Some of the larvæ become fixed, while others coalesce together and form a large mass, the fate of which has not been further studied. An invagination of epiblast takes place at the free end of the fixed larva, which gives rise to the so-called gastric cavity, i.e. the axial portion of the general enteric cavity, which would appear to be in reality a kind of stomodæum. Around the gastric cavity the hypoblast forms eight mesenteries, the chambers between which are filled with the homogeneous material which occupied the centre of the ovum in the previous stage. It is to be presumed, though not stated, that by an absorption of the blind end of the stomodæal invagination the gastric chamber is placed in free communication with the spaces between the mesenteries[81]. During the next stage the young Alcyonium also acquires eight tentacles, which arise as hollow papillæ opening into the eight mesenteric chambers. By this stage also the matter filling up the mesenteric chambers is nearly absorbed.
[81] The German abstract is very obscure as to the formation of the mouth.
Between the epiblast and hypoblast there is formed an homogeneous membrane, which penetrates in between the two layers of hypoblast which form the mesenteries. On the outer side of this membrane, and therefore presumably derived from the epiblast, is a layer of connective-tissue cells, which eventually gives rise to the abundant gelatinous tissue (coenenchyma) in which the skeletal elements are deposited. In Sympodium coralloides Kowalevsky (No. 168) has shewn still more completely the derivation of the stellate mesoblast cells from the epiblast. He finds that the calcareous spicula develop in these cells as in the mesoblast cells of sponges. The branched gastrovascular canals in this tissue are outgrowths of the primitive enteric cavity. A layer of circular muscles is formed at a late period from the epiblast, but the longitudinal muscles of the mesenteries on the inner side of the homogeneous membrane are regarded by Kowalevsky as hypoblastic.
A ciliated planula with delaminated hypoblast is also found in Gorgonia and Corallium rubrum. In the former genus at the time when the larva becomes fixed, the hypoblast is formed of two strata, an outer one of columnar cells, and an inner one of round ciliated cells lining a central enteric cavity. The inner layer is believed by Kowalevsky to become eventually absorbed and to be homologous with the inner granular mass of Alcyonium.
Zoantharia. Amongst the Zoantharia several forms have been investigated by Kowalevsky (147) and Lacaze Duthiers (170), of which some are stated by the former author to pass through an invaginate gastrula stage, while in other instances the hypoblast is probably formed by delamination.
To the first group belongs an edible form of Sea Anemone found near Messina, Cerianthus, and perhaps also Caryophyllium. In the first of these segmentation results in the formation of a blastosphere. A normal invagination obliterating the segmentation cavity then ensues, and the blastopore narrows to form the mouth. The borders of the mouth bend inwards and so give rise to the gastric cavity (stomodæum) which as in the Alcyonidæ is lined by epiblast. Simultaneously with the formation of the mouth there appear the two first mesenteries.
In Cerianthus the segmentation is unequal, the early stages are the same as in the Actinia just described, but the hypoblast cells give rise to a mass of fatty material filling up the enteric cavity, which becomes eventually absorbed.
In the majority of the Zoantharia so far investigated, including species of Actinia, Sagartia, Bunodes, Astroides, Astræa, the segmentation, which is often unequal[82] and not accompanied by the formation of a segmentation cavity, results in a solid two-layered ciliated planula. In these forms the impregnation takes place in the ovary, and the early stages of development are passed through in the maternal tissues.
[82] I have this on the authority of Kleinenberg. The existence of an unequal segmentation probably indicates an epibolic gastrula.
One end of the planula becomes somewhat oval and develops a special bunch of cilia. At the other end a shallow depression appears, which becomes deeper and forms an involution lined by epiblast. This involution is the stomodæum, and becomes the so-called gastric cavity. The true enteric cavity lined by hypoblast is for some time filled with yolk material. The larva always swims with the aboral end directed forwards.
Between the two embryonic layers a homogeneous membrane is formed, similar to that already described in the Alcyonidæ.
The further development of the larvæ especially concerns the formation of mesenteries, tentacles and calcareous skeleton. With reference to this subject the observations of Lacaze Duthiers are especially valuable and striking.
In the adult it is usually possible to recognise in the tentacles a symmetry of six. There are six primary tentacles, six secondary, twelve tertiary, twenty-four quaternary, etc. In the hard septa of the skeleton the same law is followed up to the third cycle, but beyond that, in the cases where the point can be verified, there appear to be only twelve septa in each additional cycle. The observations of Lacaze Duthiers have shewn that this symmetry is only secondarily acquired and does not in the least correspond with the succession of the parts in development.
His observations were conducted on three species of Zoantharia without a skeleton, viz. Actinia mesembryanthemum, Sagartia, and Bunodes gemmacea; while Astroides calycularis served as the type for his investigations on the corallum. It will be convenient to commence with his results on Actinia mesembryanthemum which served as his type.
The free cylindrical embryo, with the aboral end directed forwards in swimming, first becomes somewhat flattened and the mouth elongated. A bilateral symmetry is thus brought about. Two mesenteries now make their appearance transversely to the long axis of the mouth, which divide the enteric cavity into two unequal chambers. The mesenteries consist of a fold of hypoblast with a prolongation of the epiblast between the two limbs of the fold. The larger chamber next becomes divided by two fresh mesenteries into three, and a similar division then takes place in the smaller chamber. The stage with six chambers is almost immediately succeeded by one with eight, owing to the appearance of two fresh mesenteries in the second-formed set of chambers. At the stage with eight chambers there is a marked period of repose. The number of chambers is increased to ten by the division of the third-formed set of chambers, and to twelve by the division of the fourth-formed set. It will be observed that the number of the chambers increases in arithmetical progression by the continual addition of two, alternately cut off from the primitive large and small chambers. The freshly formed chambers are always formed immediately on one side of the primitive mesenteries. The stages with six and ten are of very short duration. The two primitive chambers are necessarily at the ends of the long axis of the mouth. After the division of the enteric cavity into twelve chambers, these chambers become about equal in size, and the formation of the tentacles commences. The law regulating the appearance of the tentacles is nearly the same as that for the mesenteries, but is not quite so precise. One tentacle makes its appearance for each chamber. The most remarkable feature in the appearance of the tentacles is due to the fact that the tentacle surmounting the primitive largest chamber arises before any of the others, and long retains its supremacy (fig. 80 A). This fact, coupled with the inequality of the two primitive chambers, supplies some grounds for speculating on a possible descent of the Coelenterata from bilaterally symmetrical forms with distinctly differentiated dorsal and ventral surfaces. The supremacy of the first-formed tentacle is not confined to the Actinozoa, but as has already been indicated, is also found in the Scyphistoma (p. 166) of the Acraspeda.
[FIG. 80. TWO STAGES IN THE DEVELOPMENT OF ACTINIA MESEMBRYANTHEMUM. (After Lacaze Duthiers.)
In the younger ciliated embryo A, viewed from the side, only one tentacle is developed. m. mouth.
The older larva B is viewed from the face when 24 tentacles have just become established. The letters shew the true order of succession of the tentacles; but e and f are transposed.]
After the twelve tentacles have become established they become secondarily divided into two cycles of six respectively larger and smaller tentacles, which alternate with each other. The two tentacles pertaining to the two original chambers belong to the cycle of larger tentacles. The mesenteric filaments appear first of all on the primary pair of septa. The increase in the number of tentacles and chambers from 12 to 24 has been found to take place in a very remarkable and unexpected way. The law is expressed by Lacaze Duthiers as follows. "The appearance of the new chambers is not, as has been believed, a consequence of the production of a single chamber between each of the twelve already existing chambers, but of the birth of two new chambers in each of the six elements (chambers) of the smaller cycle." The result of this law is that a pair of tentacles of the third cycle is placed in every alternate space, between a large and a small tentacle, of the two already existing cycles, which may conveniently be called the first and second cycles (fig. 80 B).
The twenty-four tentacles formed in the above manner are obviously at first very irregularly arranged (fig. 80 B), but they soon acquire a regular arrangement in three graduated cycles of 6, 6 and 12. The first cycle of the six largest tentacles is the large cycle of the previous stage, but the two other cycles are heterogeneous in their origin, each of them being composed partly of the twelve tentacles last formed, and partly of the six tentacles of the second cycle of the previous stage.
The further law of multiplication has been thus expressed by Lacaze Duthiers: "The number of chambers and still later that of the corresponding tentacles is carried from 24-48 and from 48-96 by the birth of a pair of elements in each of the 12 or 24 chambers, above which are placed the smallest tentacles which together constitute the fourth or fifth cycle. Since, after the formation of each fresh cycle, the arrangement of the tentacles again becomes symmetrical, it is obvious that all the equal sized cycles except the first are formed of tentacles entirely heterogeneous as to age."
The fixation of the free-swimming larva takes place during the period when the tentacles are increasing from 12 to 24.
The general formation of the chambers in Bunodes and Sagartia is nearly the same as in Actinia.
In the two types of Actinozoa with an embolic gastrula stage the laws as to the formation of the tentacles do not appear to be the same as those regulating the forms observed by Lacaze Duthiers.
In Cerianthus four tentacles are formed simultaneously at the period when only four chambers are present. In Arachnitis (Edwarsia) the succession of the tentacles is stated (A. Agassiz, 166) to resemble that in Cerianthus. There are originally four tentacles, and at one extremity of the long axis of the mouth are the oldest tentacles, while at the other tentacles are constantly added in pairs. An odd tentacle is always found at the extremity of the mouth opposite the oldest tentacles.
In the other species with an embolic gastrula eight tentacles would seem to appear simultaneously at the period when eight chambers are present; though on this point Kowalevsky's description is not very clear. The presence of such a stage would seem to indicate a close affinity to the Alcyonidæ.
Amongst the sclerodermatous Actinozoa, except Caryophyllium, the embryo closely resembles that of the delaminate Malacodermata. The first stages occur in the ovary, and the larva is dehisced into the body cavity as a two-layered ciliated planula.
The laws affecting the formation of the first twelve tentacles and septa appear to be nearly the same as for the Malacodermata. The hard parts begin as a rule to be formed when twelve tentacles have appeared, at which period also the fixation of the larva takes place. On fixation the larva becomes very much flattened.
The first parts of the corallum to appear are twelve of the septa, which arise simultaneously in folds of the enteric wall in the chambers between the mesenteries, and correspond therefore with the tentacles and not, as might be supposed, with the mesenteries. Each septum is formed by the coalescence of three calcareous plates which originate in separate centres of calcification. The concrescence of the three produces a Y-shaped plate with the single limb directed inwards and the two limbs outwards (fig. 81). The theca does not arise till after the septa have become formed, and is at first a somewhat membranous cup quite distinct from the septa. The columella is formed still later by the coalescence of a series of nodules which are formed in a central axis enclosed by the inner ends of the septa.
[FIG. 81. LARVA OF ASTROIDES CALYCULARIS SHORTLY AFTER IT HAS BECOME ATTACHED. (After Lacaze Duthiers.)
The figure shews the development of the Y-shaped septa in the intervals between the mesenteries. The position of the latter is indicated by the faint shading. The theca has become developed externally.]
After the formation of the theca the septa become divided into two cycles by the predominant growth of six of them. On the coalescence of the septa with the theca the space between the two limbs of the Y becomes filled up with calcareous tissue. The law of the formation of the third cycle of septa (12-24) has not been worked out, so that it is not possible to state whether it follows the peculiar principles regulating the growth of the tentacles.
The whole of the skeletal parts occupy a position between the epiblast and hypoblast, and are exactly homologous in this respect with the skeleton of the Alcyonidæ. By Lacaze Duthiers they are however believed to originate in the hypoblast, but from the observations of Kowalevsky there be little doubt that they arise in the connective tissue between the two embryonic layers which is probably epiblastic in origin.
A peculiar larva, probably belonging to the Actinozoa, has been described by Semper[83]. It has an elongated form and is provided with a longitudinal ridge of cilia. There is a mouth at one end of the body and an anus at the opposite extremity. The mouth leads into an oesophagus, which opens freely into a stomach with six mesenteries. In the skin are numerous thread-cells. A mesotrochal worm-like larva, also provided with thread-cells, and found at the same time, was conjectured by Semper to be a younger form of this larva.
[83] "Ueb. einige tropische Larven-formen." Zeit. f. wiss. Zool., vol. XVII. 1867.
Ctenophora. The ovum of the Ctenophora is formed of an outer granular protoplasmic layer and an inner spongy mass with fatty spherules. It is enveloped in a delicate vesicle, the diameter of which is very much greater than that of the contained ovum. This vesicle appears to be filled with sea-water, in which the ovum floats.
Fertilized ova may usually be easily obtained by keeping the captured adults in water from 12-24 hours. The two main authorities on the development of these forms (Kowalevsky, No. 147 and 178 and Agassiz, No. 172) are unfortunately at variance on one or two of the most fundamental points. It seems however that the embryonic layers are formed by a kind of epibolic gastrula; while the true gastric cavity, as distinct from the gastrovascular, is formed by an invagination, and deserves therefore to be regarded as a form of stomodæum.
[FIG. 82. FIVE STAGES IN THE DEVELOPMENT OF IDYIA ROSEOLA. (After Agassiz.)
The protoplasmic layer of the ovum is represented in black.]
The early stages are very closely similar in all the types so far observed. Segmentation commences by the outer layer of the ovum, which throughout behaves as the active layer, forming a protuberance at one pole, which may be called the formative pole. Close below this protuberance is placed the nucleus. In the median line of the protuberance a furrow appears (fig. 82 A), which gradually deepens till it divides the ovum into two. The granular layer follows the furrow so that each of the fresh segments, like the original ovum is completely invested by a layer of granular protoplasm. Each segment contains a nucleus. A second similar division at right angles to the first gives rise to four segments (fig. 82 B), and the segments so formed become again divided into eight (fig. 82 C). In the division into eight, which takes place in a vertical plane, the segments formed are of unequal size, four of them being much smaller than the others. The eight segments are arranged in the form of a slightly curved disc round a vertical axis--the future long axis of the body;--and there is a cavity in this axis which, like the segmentation cavity of Sycandra raphanus, is open at both extremities. The disc with its concavity on the side of the formative pole has the shape sometimes of an ellipse (fig. 82 C) and sometimes of a rectangle, in which the four small spheres occupy the poles of the longer axis. A bilateral symmetry is thus even at this stage clearly indicated.
In the next phase of segmentation the granular layer surrounding each segment again forms a protuberance at the formative pole, but, instead of each segment becoming divided into two equal parts, the protoplasmic protuberance alone is divided off from the main segment. In this way sixteen spheres become formed, of which eight are large and are formed mainly of the yolk material of the inner part of the ovum, and eight are small and entirely composed of the granular protoplasm. The eight small spheres form a ring on the formative surface of the large spheres (fig. 82 D).
The small spheres now increase very rapidly (fig. 82 E), partly by division and partly by the formation of fresh cells from the large spheres; and spread over the large spheres, forming in this way an epibolic gastrula. They constitute a layer of epiblast. (fig. 83 A.) The large cells in the meantime remain relatively passive, though during the process they divide, in some cases more or less irregularly, while in Eucharis they divide into sixteen. The axial segmentation cavity would seem during the process to become obliterated.
There is an important discrepancy between the statements of Kowalevsky and Agassiz as to the course of the growth of the small cells. According to Agassiz the small cells grow most rapidly at the formative pole and cover this before they meet at the opposite pole. The reverse statement is made by Kowalevsky. It would seem that the above discrepancy is due to an interchange on the part of the one or the other of these authors of the two poles of the embryo, in that according to Agassiz the formation of the mouth takes place at the formative pole, and according to Kowalevsky at the pole opposite to this.
Without attempting to decide between the above views, we shall speak of the pole at which the mouth is formed as the oral pole.
[FIG 83. FOUR STAGES IN THE DEVELOPMENT OF IDYIA ROSEOLA. (After Agassiz.)
s.c. sense capsule; st. stomodæum.]
The formation of the alimentary cavity commences shortly after the complete investiture of the embryo by the epiblast cells. At the oral pole an invagination of epiblast cells takes place (fig. 83 B), which makes its way towards the opposite pole. More especially from the figures given by Agassiz, and from the explanation of his plates, it would seem that a large chamber is formed in the hypoblast at the end of the invaginated tube, into which this tube soon opens (fig. 83 C). The invaginated tube would seem to give rise to the so-called stomach, while the chamber at its aboral extremity is no doubt the infundibulum, which as may be gathered from Kowalevsky's statements, is lined by a flattened epithelium. At a later period the gastrovascular canals grow out from the infundibulum as four pouches, which are surrounded by, and grow at the expense of, the large central cells, which have in the meantime arranged themselves in four masses, and appear to serve as a kind of yolk. The nuclei of these large cells according to Kowalevsky disappear, and the cells themselves break up into continually smaller masses.
The main difficulty in the above description of Agassiz is the origin of the infundibulum. In the absence of definite statements on this head it seems reasonable to conclude that it arises as a space hollowed out in the central cells, and that its walls are formed of elements derived from the yolk cells[84]. On this interpretation the alimentary canal of the Ctenophora would consist, as in the Acraspedote Medusæ and Actinozoa, of two sections: (1) A true hypoblastic section consisting of the infundibulum and the gastrovascular canals derived from it; and (2) an epiblastic section--the stomodæum--forming the stomach.
[84] Chun (No. 174) gives a short statement of his observations, which accords with the interpretation in the text.
The observations of Kowalevsky on the alimentary system do not wholly tally with those of Agassiz. He finds that the oral side of the embryo becomes hollowed out, and that the hollow, lined by flattened cells, becomes constricted off as the infundibulum, from which the radial canals subsequently grow out. To the infundibulum there leads a narrow canal lined by a columnar epithelium which becomes the gastric cavity.
While the alimentary canal is becoming formed a series of important changes takes place in other parts of the embryo. The rows of locomotive paddles first appear as four longitudinal equidistant linear thickenings of the epiblast near the aboral pole (fig. 83 D). On the projecting surface of these ridges stiff cilia appear which coalesce together to form the paddles. While the embryo is still within the egg the rows of paddles are quite short and also double. There are in Pleurobrachia about eight or nine pairs of paddles in each row. Each double row eventually separates into two.
In all the forms except the Eurostomata (Beroe) two tentacles grow out as thickenings of the epiblast (fig. 84 B, t.). They are placed at the opposite poles of the long transverse axis of the embryo.
A process of the contractile gelatinous tissue of the body, the origin of which is described below, makes its way, according to Kowalevsky, into the tentacles.
The central apparatus of the nervous system and the otoliths are formed at the aboral pole from a thickening of the epiblast, but the full details of their formation have not been elucidated. It may be well to preface my account of their development with a short statement of their adult structure.
They consist in the adult of a vesicle with a ciliated lining situated at the bifurcation of the two anal tubes, and of certain structures connected with this vesicle. From the floor of the vesicle is suspended a mass of otoliths by four leaf-like bodies known as suspenders. The roof is very delicate and has the form of a four-sided pyramid. Six openings lead into the vesicle. Through four of these, placed at the four corners, there pass out four ciliated grooves continuous with the suspenders. These grooves, after leaving the otolithic vesicle, bifurcate and pass to the eight rows of paddles. At the two sides the walls of the vesicle are continuous with two thickened ciliated plates with swollen edges, opposite the centres of which are two lateral openings into the vesicle, completing the six openings. Through the lateral openings the sea-water is driven by the action of the cilia of the plates.
The development of these parts is as follows--In the aboral thickening of epiblast a cavity makes its appearance, the walls of which constitute the rudiment of the otolithic vesicle (fig. 83 B and C, s.c.). The roof of the cavity is extremely delicate. On each side of it a thickening of cells becomes established, regarded by Kowalevsky as the rudiment of the nervous ganglia. These thickenings appear to give origin to the lateral ciliated plates. The otoliths arise from cells at four separate points at the corners of the ciliated plates opposite the rows of paddles (fig. 84 A, ot.).
[FIG. 84. TWO STAGES IN THE DEVELOPMENT OF PLEUROBRACHIA RHODODACTYLA. (After Agassiz.)
ot. otolith; t. tentacle.]
In Pleurobrachia there is at first only one otolith at each corner. The otoliths are gradually transported towards the centre of the vesicle (fig. 84 B, ot.) and are there attached, though the four leaf-like suspenders do not arise till very late. The otoliths go on increasing in number throughout life.
The gelatinous tissue of the Ctenophora appears as a homogeneous layer between the epiblast and the yolk cells, and is probably homologous with the layer formed in the same situation in all other coelenterate forms. Into the layer a number of anastomosing cells, mainly derived from the epiblast, though according to Chun (No. 174) also in part from the hypoblast, make their way. These cells would appear to be mainly, if not entirely (Chun), of a contractile nature. It is probable that the great mass of the gelatinous tissue of the adult is an intercellular substance derived from these cells.
The whole of the above changes are completed while the embryo is still enclosed in the egg-capsule. During their accomplishment the oro-anal axis, which was originally very short, increases greatly in length (fig. 83), so that the embryo acquires an oval form similar to that of the adult.
The exact period of leaving the egg does not appear to be very constant but the hatching never takes place till the embryo has practically acquired all the organs of the adult.
In the majority of types the differences between the just hatched larva and the adult are inconsiderable, and in all cases the larva has a somewhat oval form. In the case of the Tæniatæ (Cestum, etc.), the larva has the characteristic oval form, and the subsequent changes amount almost to a metamorphosis.
The larva of the Lobatæ, such as Eucharis, Bolina, etc., can hardly be distinguished from Pleurobrachia, and undergoes therefore considerable changes after hatching.
Eucharis multicornis while still in the larval condition is stated by Chun to become sexually mature.
The new genus Ctenaria recently described by Haeckel, which is intermediate between the Ctenophora and the Medusæ clearly proves that the Ctenophora are more closely related to the Medusæ than to the Actinozoa but their development, especially the presence of a stomodæum, shews that they have affinities (in spite of the rudimentary velum of Ctenaria) with the Acraspedote as well as with the Craspedote Medusæ; and it may be noted that the Acraspeda have undoubted affinities with the Actinozoa.
Summary and general considerations.
Even in the adult condition the lower forms of Coelenterata do not rise in complexity much beyond a typical gastrula. Ontogeny nevertheless brings clearly to light the existence of a larval form--the planula--which recurs with fair constancy amongst all the groups except the Ctenophora.
We are probably justified in assuming that the planula is a repetition of a free ancestral form of the Coelenterata. The planula, as it most frequently occurs, is a two-layered ciliated nearly cylindrical organism, with at most a rudimentary digestive cavity hollowed out in the inner layer, and as a rule no mouth. In the outer layer are numerous thread-cells.
How many of these characters did the ancestral planula possess? I think it is not unreasonable to assume that the only two characters about which there can be much doubt are the rudimentary condition of the digestive cavity and the absence of a mouth. Paradoxical as it may seem, it appears to me not impossible that the Coelenterata may have had an ancestor in which a digestive tract was physiologically replaced by a solid mass of amoeboid cells. This ancestor was perhaps common to the Turbellarians also. The constant presence of thread-cells in the inner layer of their epiblast fits in with their derivation from a form similar to the planula. While the solid parenchymatous digestive canal of Convoluta and Schizoprora and other forms amongst the Turbellarians, though very probably secondary, may perhaps be explained by such a view of their origin.
The planula in its primitive condition is not bilaterally symmetrical, but frequently, as amongst the Actinozoa, it becomes flattened on two sides before undergoing its conversion into the adult form. Perhaps the bilateral form of planula is the starting point both for the Coelenterata and the Turbellaria. In this connection the peculiar unilateral development of a tentacle in Scyphistoma and Actinia should be noted.
The planula occurs in the majority of sessile forms of Hydrozoa except the Tubularidæ and Hydra. It is also characteristic of the Trachymedusæ and Siphonophora. Amongst the Acraspeda it is also present, but has an exceptional mode of ontogeny which is discussed in connection with the germinal layers.
It is characteristic both of the Octocoralla and Hexacoralla, but is not found in the Ctenophora.
In the Tubularidæ and in Hydra an abbreviated development leads no doubt to the absence of a free planula stage, and the absence of a larval form amongst the Ctenophora may, as has already been stated, be probably explained in the same way.
The Coelenterata of all the Metazoa are characterized by the greatest simplicity in the arrangement of their germinal layers; and for this reason very considerable interest attaches to the mode of formation of the layers amongst them. Two germinal layers are constantly found, which correspond in a general way to the epiblast and hypoblast. It might have been anticipated that a certain amount of uniformity would have existed in the mode of formation of the layers. This however is not the case. In perhaps the majority of forms they become differentiated by a process of delamination, but in a not inconsiderable minority the two layers owe their origin to an invagination.
Delamination is constant (with the doubtful exception of some Tubularidæ) amongst the Hydromedusæ and Siphonophora. It is perhaps in the main characteristic of the Actinozoa.
Invagination by embole takes place, so far as is known, constantly amongst the Acraspeda and frequently amongst the Actinozoa; and an epibolic invagination is characteristic of the Ctenophora.
If confidence is to be placed in the recorded observations on which this summary is founded, and there is no reason why in a general way it should not be so placed, the conclusion is inevitable that of the above modes of development the one must be primitive and the other a derivative from it, for, if this conclusion be not accepted, the absolutely inadmissible hypothesis of a double origin for the Coelenterata would have to be adopted.
Two questions arise from these considerations:--
(1) Which is the primitive, delamination or invagination?
(2) How is the one of these to be derived from the other?
There is a great deal to be said in favour of both delamination and invagination; but it will be convenient to defer all discussion of the question to the general chapter on the formation of the layers throughout the animal kingdom.
The hypoblast cells are often filled with yolk material, and secondary modifications are thus produced in the development. The most important examples of such modifications are found in the Siphonophora and Ctenophora.
In the simplest forms amongst the Hydrozoa there is no trace of a third layer or mesoblast. The epiblast is typically formed, as was first shewn by Kleinenberg, of an epithelial layer and a subepithelial interstitial layer of cells. The cells of the former are frequently produced into muscular or nervous tails, and those of the latter give rise to the thread-cells and generative organs and in some cases to muscles[85]. In many cases, amongst all the Coelenterate groups, and constantly amongst the Ctenophora the epiblast is simplified and reduced to a single layer. The hypoblast undergoes in most cases no such differentiation but simply forms a glandular layer lining the gastric chamber and its prolongations into the tentacles; but in the Actinozoa it appears to give rise to muscles, and strong evidence has been brought forward to shew that in some groups it gives rise to the generative organs.
[85] The questions relating to the generative organs of the Coelenterata are dealt with in the second part of this work.
Between the epiblast and hypoblast a structureless lamella appears always to be interposed.
In many Coelenterata further differentiations of the epiblast are present. In many forms the layer gives rise to a hard external skeleton. This is most widely spread amongst the Hydrozoa, where in the majority of cases it takes the form of the horny perisarc, and in the Hydrocoralla (Millepora and Stylasteridæ) of a hard calcareous skeleton. The skeleton in these forms, though closely resembling the mesoblastic skeleton of the Actinozoa, has been shewn by Moseley (164) to be epiblastic.
In the Actinozoa an epiblastic skeleton is exceptional, and according to most authorities absent. Quite recently however Koch (167) has found that the axial branched skeleton of most of the Gorgonidæ, viz. the Gorgoninæ and Isidinæ, is separated from the coenosarc by an epithelium, which he believes to be epiblastic, and to which no doubt the axial skeleton owes its origin. A similar epithelium surrounds the axis of the Pennatulidæ.
In the Medusæ the epiblast also gives rise to a central nervous system, which however continues to form a constituent part of the layer, and to the organs of special sense[86].
[86] The differentiation of the nervous and muscular systems in the Hydrozoa is treated of in the second part of this work.
A special differentiation of the hypoblast is found in the solid axis of the tentacles. This axis replaces the gastric prolongation found in many forms, and the cells composing it differentiate themselves into a chorda-like tissue, which has a skeletal function, and is no longer connected with nutrition. This axis is placed by many morphologists amongst the mesoblastic structures.
In all the higher Coelenterata certain tissues become interposed between the epiblast and hypoblast, which may be classified together as the mesoblast.
The most important of these are:
(1) The various distinct muscular layers. (2) The gelatinous tissue of the Medusæ and Ctenophora. (3) The skeletogenous tissue of the Actinozoa.
In most cases the muscular fibres are connected with epithelial cells, but in certain forms amongst the Medusæ and in the majority if not all the Actinozoa they constitute a distinct layer, sometimes separated from the epiblast by a structureless membrane, Æquorea Mitrocoma. Such layers when on the outer side of the membrane separating epiblast and hypoblast are undoubtedly epiblastic in origin, but in some cases amongst the Actinozoa they adjoin the hypoblast, and are very probably derived from this layer.
The origin of the gelatinous tissue is still involved in much obscurity.
It originates as a homogeneous layer between epiblast and hypoblast, which in the Hydromedusæ never becomes cellular though traversed by elastic fibres.
In the Acraspeda it contains anastomosing cells in the main apparently (Claus) derived from the hypoblast, and in the Ctenophora it is richly supplied with muscular stellate cells for the most part of epiblastic origin, though some are stated by Chun to come from the hypoblast. On the whole it seems probable, that the gelatinous tissue may be regarded as a product of both layers; and there are some grounds for thinking that it is an immense development of the membrane always interposed between the two primary layers. It must however be borne in mind that a membrane, regarded by the Hertwigs as the equivalent of the ordinary membrane between the epiblast and hypoblast, can be usually demonstrated on both surfaces of the gelatinous tissues in Medusæ. The skeletogenous layer of the Actinozoa is probably the morphological homologue of the gelatinous tissue; but the evidence we have is on the whole in favour of the connective-tissue cells it contains being epiblastic in origin. It gives rise to the skeleton of the Hexacoralla, to the spicular skeleton of Alcyonium, the axial skeleton of Corallium, and the skeleton of the Helioporidæ and Tubiporidæ.
Alternations of generations.
Alternation of generations is of common occurrence amongst the Hydrozoa, and something analogous to it has been found to take place in Fungia amongst the Actinozoa. It is not known to occur in the Ctenophora.
The chief interest of its occurrence amongst the Hydromedusæ and Siphonophora is the fact that its origin can be traced to a division of labour in the colonial systems of zooids so characteristic of these types.
In the Hydromedusæ an interesting series of relations between alternation of generations and the division of the zooids into gonophores and trophosomes can be made out. In Hydra the generative and nutritive functions are united in the same individual. The generative swellings in these forms cannot, as has been ably argued by Kleinenberg, be regarded as rudimentary gonophores, but are to be compared to the generative bands developed in the Medusæ around parts of the gastro-vascular system. A condition like that of Hydra, in which the ovum directly gives rise to a form like its parent, is no doubt the primitive one, though it is not so certain that Hydra itself is a primitive form. The relation of Hydra to the Tubularidæ and Campanularidæ may best be conceived by supposing that in Hydra most ordinary buds did not become detached, so that a compound Hydra became formed; but that at certain periods particular buds retained their primitive capacity of becoming detached and subsequently developed generative organs, while the ordinary buds lost their generative function.
It would obviously be advantageous for the species that the detached buds with generative organs should be locomotive, so as to distribute the species as widely as possible, and such buds in connection with their free existence would naturally acquire a higher organization than the attached trophosomes. It is easy to see how, by a series of steps such as I have sketched out, a division of labour might take place, and it is obvious that the embryos produced by the highly organized gonophores would give rise to a fixed form from which the fixed colony would be budded. Thus an alternation of generations would be established as a necessary sequel to such a division of labour. To test the above explanation it is necessary to review the main facts with reference to alternations of generations amongst the Hydromedusæ.
Hydromedusæ[87]. In many instances amongst the Tubularidæ, Sertularidæ and Campanularidæ medusiform buds are produced which become detached and develop sexual organs.
[87] For a full account of this subject the reader is referred to the beautiful memoir of Allman (No. 149).
Such Medusæ are divided into two great groups, the Ocellata and Vesiculata, according to the characters of the marginal sense organs. In the Ocellata the sense organs have the form of eyes, and in the Vesiculata of auditory vesicles. The latter seem to be usually budded off from the Campanularia stocks, and the generative organs extend in folded bands over the radial canals. These bands have been regarded by Allman as composed of rudimentary gonophores, and he called the Medusæ which give rise to them blastochemes. He regards them as representing a more complicated type of alternation of generations with three instead of two generations in the series. The Hertwigs have brought what appear to me conclusive grounds for rejecting this view, and have demonstrated that the generative organs of these types resemble those of ordinary Medusæ.
In many forms the medusiform buds though fully developed do not become detached; whether detached or not they are known as phanerocodonic gonophores. In other forms again buds which begin as if they were going to form Medusæ never reach that condition but remain permanently in an undeveloped state. They have been called by Allman adelocodonic gonophores.
In all the above cases two generations at the least interpose between the successive sexual periods, viz.:--
(1) A trophosome produced directly from the ovum. (2) A gonophore budded from this.
In a very large number of types the gonophores do not develop directly on the hydroid stem, but arise on specially modified zooids resembling rudimentary trophosomes which have been named blastostyles by Allman. On the sides of each blastostyle a series of gonophores usually becomes developed. The blastostyles either remain exposed as in all the Gymnoblastic or Tubularian Hydroids, or as in all the Calyptoblastic Hydroids (Sertularidæ and Campanularidæ) they become invested by a special case--known as the gonangium--which is formed of perisarc lined by epiblast. In the forms with blastostyles three generations interpose between the successive stages of sexual reproduction, (1) the trophosome developed directly from the ovum, (2) the blastostyle budded from this, (3) the gonophore budded from the blastostyle.
Such being the main facts, in order to prove that the existing condition of polymorphism amongst the Hydromedusæ is to be explained as hypothetically suggested above, it is still necessary to shew that (1) the free medusiform gonophores are really only modified trophosomes, or rather that the trophosomes and gonophores are both modifications of some common type, and (2) that the fixed so-called adelocodonic gonophores are retrograde derivatives of the free medusiform gonophores. Unless these points can be established it might be maintained that the Medusæ were special zooids, developed de novo and not by a modification of trophosome zooids. To demonstrate these propositions at length would carry me too far into the region of simple Comparative Anatomy, and I content myself with referring the reader to a discussion of the Hertwigs (No. 146, p. 62) where the first point appears to me fully established. With reference to the second point I will only say that the structure and development of the adelocodonic gonophores can only be explained on the assumption that they are retrograde forms of the phanerocodonic gonophores, and that the opposite view, that the phanerocodonic gonophores are derived from the adelocodonic, leads to a series of untenable positions.
The Trachymedusæ, as has been shewn above, develop directly. They are probably derived from gonophores in which the trophosome has disappeared from the developmental cycle.
To sum up, three types of development are found amongst the Hydromedusæ.
(1) No alternations of generations. Permanent form, a sexual trophosome. Ex. Hydra.
(2) Alternations of generations. Trophosome fixed, gonophore free or attached. Ex. Gymnoblastic and Calyptoblastic Hydroids, and Hydrocoralla.
(3) No alternations of generations. Permanent form, a sexual Medusa. Ex. Trachymedusæ.
Siphonophora. In the Siphonophora alternations of generations take place in the same way as in the Hydromedusæ, but the starting point appears to be a Medusa. The gonophores may remain fixed or become detached.
Acraspeda. With the exception of Pelagia and Lucernaria, in which the development involves a simple metamorphosis, all the Acraspeda undergo a form of alternations of generations. The ovum, as already described, develops into a fixed form--the Scyphistoma--which increases asexually by normal budding, and can even form a permanent colony.
[FIG. 85. THREE STAGES IN THE ALTERNATIONS OF GENERATIONS OF AURELIA AURITA. (From Gegenbaur.)
A. Polype stage. B. Commencing strobilization. C. Completed strobilization.]
The formation of the sexual Medusa form takes place by a kind of strobilization of the body of the fixed Scyphistoma. A series of transverse constrictions becomes formed round the body below the mouth, dividing it up into corresponding rings, each of which eventually gives rise to a Medusa known as an Ephyra (fig. 85). In each of these rings is a dilation of the stomach, and a section of each of the four rudimentary mesenteries described in connection with the development of the Scyphistoma. As the constrictions become deeper the segments of the body between them become disc-like, and their edges are produced into eight lobes containing prolongations of the gastric cavity (fig. 85 C). The lower surface of each disc, which forms the future aboral surface of the Medusa, becomes convex, in part owing to the development of gelatinous tissue. On the opposite surface a muscular layer becomes developed. During the above process the body of the Scyphistoma gradually grows in length and continues to be segmented, so that a series of Ephyræ are uninterruptedly formed, of which those near the base are the youngest. The original terminal ring of tentacles of the Scyphistoma gradually atrophies.
In the further development of the Ephyræ each of their eight lobes becomes bifid at its extremity.
As the Ephyræ successively reach this condition they become detached, and by a series of remarkable changes, amounting almost to a metamorphosis, and accompanied by an enormous growth in size, reach the adult condition.
The alternation of generations in the Acraspeda cannot be quite so simply explained as in the Hydromedusæ, though the principle is probably the same in the two cases.
Actinozoa. Amongst the Actinozoa there occurs in Fungia a peculiar process which is, as shewn by Semper (171), in many ways analogous to alternations of generations[88]. From the larva a nurse-stock is developed, at the end of which a cup-like coral resembling the adult is formed as a bud. The bud becomes detached and then gives rise to a permanent sexual Fungia. From the nurse-stock there is formed however a fresh bud at the centre of the scar left on the detachment of the old one. The fresh bud eventually becomes separated from the nurse-stock leaving a small portion of its stem behind; each succeeding bud similarly leaves a small portion of its stem, so that the nurse-stock eventually acquires a jointed appearance. In the above process we clearly have, as in the Hydromedusæ, a non-sexual form--the nurse-stock--produced directly from the larva, giving rise by budding to a sexual form; all the conditions of an alternation of generations are therefore fulfilled. It seems however possible that the nurse-stock itself may eventually become sexual.
[88] Vide also Moseley. Notes by a Naturalist of the Challenger, pp. 524 and 525.
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