AETEOR'B ABBTaACT O? THIS PAPER IPEUED

B Y T E E BIBLIOQRAPHIC BERVICE 8EmEYBER.

THE EARLY DEVEIJOPMENT OF A STARFISH, PATERIA (ASTERINA) MINEATA

HAROLD HEATH From the Leland Stanjord Junior University, California

F I \ E FIGURE8

During the past summer a small number of gastrulae were dis-a covered in the plankton of Monterey Ray, California, which exhibited a unique combination of characters, relating them on one hand to the Echinodermata and on the other to the Enterop neusta. To discover their true relationship all were placed in balanced aquaria where they subsequently developed into bi- pinnariae. Ova of various species of shoredwelling starfishes were then artificially fertilized and reared for a sufficient length of time to show that the first captured specimens were the young of Pateria (Asterina) mineata.

,Judging from artificially fertilized material the segmentation and early blastula stages do not exhibit any especially note- worthy features, but beyond this point certain structures arise that have no known counterpart among starfishes. The fist of these unique organs is the apical plate. In the late blastula stage the cells about the animal pole commence to elongate and, in the gastrula, form a thickened area, more or less lens- shaped in form, having approximately one half the diameter of the transverse axis of the embryo. As indicated in the drawings (figs. 3, 5) its center is exactly opppsite to the blastopore and therefore i b strictly apical.

Sections show the component cells to possess a height fully three times that of the average ectoderm cell of the animal half of the embryo. Passing outwardly the altitude diminishes at a fairly uniform rate until the outer limits are reached. The nuclei are distally located and therefore similar in this respect

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to the ectodermal elements generally. Furthermore all of the cells of the apical plate are packed with granules, evidently yolk, and thus arc in marked contrast to the remaining ectoderm where the granulcs are relatively few and minute.

Generally speaking, this condition of affairs continues to the close of gastrulation. In specimens entering upon the initial stages of enterocele formation, where the walls of the blind end of the archenteron have grown thin, a few of the cells of the apical plate are usually to be seen in the act of migrating into the blastocele. As will be seen later these and other migrants from the apical plate form mesenchyme.

The formation of the enteroceles (hydroceles) proceeds in the typical fashion. In practically every case they arise independ- ently of each other, and from the outset the left is almost in- variably the larger of the two (fig. 1). Mesenchyme cells arise as usual from the walls of the enteroceles as well as from the intervening portion of the archenteric wall. 'l'hcir numbers, when compared with those in hsterias ocracea for example, are relatively small, and, in comparison with the migrating cells of the apical plate, they are distinctly smaller and far more hyaline in appearsncc -features which enable one to distinguish the two types of mesenchyme (ectodermal and entodermal) though- out the stages described in this paper.

In fully 50 per cent of the specimens in hand a few of the mesen- chyme cells arising from the blind end of the archenteron, be- tween the enterocele pouches, unite to form a srrmll vesicle (fig. 1 , nu). This usually occurs after the enterocele pouches are well differentiated though not completely cut off. In a relatively short space of time this anterior, unpaired vesicle is rapidly enlarged by the addition of other mesenchyme cells from the archenteron, and ultimately attains a diameter equal to that of the gut,. In a few surface views it is clearly seen to be entirely enclosed, with walls everywhere complete, and, though it is closely attached to the distal wall of the archenteron, it is never- theless distinctly separated from it. In other ca6es the vesicle is so closely applied to the archenteric wall that it is not pos- sible to determine whether the vesicular walk are complete. In

EARLY DEVELOPMEAT OF A STARFISH 463

every instance, however, the distal wall of the archenteron is con- tinuous, and the evidence is perfect that this anterior vesicle is entirely formed from mesenchyme and not as an outpouching of the archenteric wall.

By the time that the anterior vesicle has attained a diameter equal to that of the archenteron the mesenchyme migration from the apical plate is at its height. Many cells in sections are seen to have become entircly free, while others are in the act of slipping past what are to become the final ectodermal elements, and are making their way into the blastocele. In several larvae they come in contact with the anterior vesicle (fig. l), and cover it like a roof. Where the mesenchyme is more scattered, a relatively small number of cells rest upon the vesicle, while the others pass around it, especially in the region of the future oesophagus.

Beyond this stage in the development, the walls of the anterior vesicle usually disappear, the mesenchymal elements separating and migrating to other regions. In the oldest stage where the vesicle hw been found to ekist the stomodaeum had completely formed, and the enterocele pouches had severed their connec- tion with the gut. The vesicle in question showed slight signs of disintegration on its posterior face, but, as figure 4 indicates, it is fairly complete, and has a diameter approximately equal to that of the middle section of the body. Here i t is a question whether jt has a complete wall next to the gut, but there is no doubt whatever about its lack of communication with the digestive tract.

Surface views under fairly high magnification show the wall of the vesicle to be made up of a relatively small number of cells. These possess highly ramified pseudopodial processes which appear to form an extremely delicate granular meshwork. Whether the meshes are bridged by a non-granular ectoplasm or by some intercellular material has not been determined, but it is evident that the bounding wall, as a whole, is fairly com- plete, since neither the pseudopodia of other cells nor minute granules which appear to have escaped from some of the apical cells make their way into the cavity of the vesicle. In some

464 HAROLD HEATH

specimens the blastocele contains a ground substance distinctly stained by Delafield’s haematoxylin, and is to. that extent in contrast with the fluid contained in the vesicle, which has only a slight affinity for dyes of this character.

After cells of the anterior vesicle have separated and migrated into the blastocele, many of thc mesenchyme elements from the apical plate move to the wall of the gut, especially in the region of the oesophagus. In the oldest larvae in ~riy possession (about twenty hours later than the stage represented in figure 2) a few of these apical mesenchyme cells, more or lem bipolar in form, rest upon the wall of the anterior half of the oesophagus at right angles to its long axis. Between this point and the stomach other mesenchyme cells of entodcrmal origin are taking up similar positions. Both types of mesenchyme doubtless become trans- formed into circular muscles.

The left hydrocele, after separating from the archenteron, is not only larger than the right, but its subsequent growth is more rapid, and it soon develops a pore .canal and hydropore which have no counterparts on the opposite side; at least none have been discovered in the material at hand.

A posterior enterocele pouch (fig. 4) arises from the left side of the gut at about the middle of the future stomach. It is a hollow outgrowth, nearly &s thick-walled as the gut itself, and after severing its connection with the digestive tract, it be- comes a flattened vesicle wedged in between the stomach and body wall. In a stage slightly older than the one represented in figure 2 the left hydrocele forms a diverticulurri at its posterior end which ultimately comes in contact with the posterior en- terocele pouch and fuses with it. Before this fusion takes place the posterior enterocele vesicle, in several larvae, assumes the form of a rather narrow ellipsc with its long axis extending from a point slightly behind the left hydrocele to the btwe of the intestine. Nothing is known regarding its subsequent history.

Comparisons. Since the year 1869, when Metschnikoff first called attention to the resemblance between the echinoderms and Balanoglosrms a vast amount of data has accumulated. This tends to support the original theory that the two groups in ques-

EARLY DEVELOPME-W O F A STARFISH 465

tion are genetically related, but the interpretation of certain details is not completcly satisfactory. For example there is a lack of agreement relating to the homologies of the coelomic cavities. I t will be remembered that Balanoglosuus develops five pouches, an anterior unpaired vesicle and two succeeding pairs which become the proboscis, collar and trunk coelom re- spectively. In Balanoglossus clavigerus, according to Heider ('09) the anterior vesicle arises as a diverticulum from the distal end of the archenteron, and after separating completely, forms the future proboscis pore, before coming in contact with the apical plate. After a time the vesicle withdraws from the plate, though retaining its connection by means of a muscular strand, while mesenchyme cells from the strand and undetermined neigh- boring regions nugate to the oesophageal region where they become transformed into circular muscles.

The resemblance in the behavior of the anterior vesicle in Balano- glossus clavigerus and Pateria mineata is decidedly striking. In thc starfish the vesicle arises in the form of mesenchyme cells which subsequently unite; in Balanoglossus it originates as a direct outgrowth of the archenteron. In Asterias rubens and a few other species of starfishes Gemmill (14) has described the rudiments of posterior enterocele pouches which either fuse with the left hydrocele or break up into mesenchyme (and possibly unite later with the hydrocele, though this is not indicated). In other words it is well known from this and numerous other instances that there is no fundamental difference be tween a vesicle formed a6 an outpouching of the gut and the precocious deveIop ment of mesenchyme with subsequent fusion. In Pateria mine- ata the anterior vesicle soon disappears, thc component mesen- chyme cells wandering off into the blastocele, but before its dis- appearance it hss come into close contact with wandering cells from the apical plate. No pore unites this anterior vesicle with the exterior, but its behavior is such that I am convinced it is the homologue of the proboscis coelom of the Enteropneusta.

There is, 00 far aa I know, no other starfish which develops a distinct, independent anterior vesicle. In several species the blind end of the archenteron becomes expanded, thin-walled and

466 HAROLD HEATH

develops laterally the two well known enteroceles, so that the median section between the pouches may possibly be considered an incipient unpaired vesicle as certain authors have suggested. On the other hand it is equally possible that some of the mesen- chyme cells migrating from the distal end of the archenteron represent the anterior vesicle though they may never actually fube. In Pateria mineata, for example, not over 50 per cent of the cmbryos form a complete vesicle; in a few cases, rela- tively, it is imperfect, and it appears probable that in the others it is represented by isolated mesenchyme cells which arise in the proper position but never unite. Furthermore, it is a signifi- cant fact that in all of these cases,.even where the anterior vesicle is perfectly formed, the enterocele pouches are separated by a thin section of archenteric wall which therefore can scarcely be regarded as representing the anterior vesicle.

Gemmill’s discovery of a pair of posterior enterocele pouches in the starfish is of the highest importance. They have the same origin as the trunk coelom in Balanoglossus, and as Gemmill states “We have here, I think, rudiments of a paired posterior enterocoelic outgrowth, which in the common ancestor of Balanoglossus and the Echinoderms gave rise to the coelom of the body or trunk.” In some of the species studied by Gemmill “this rudiment takes no part, or only a small part, in the forma- tion of the wall of the posterior coeloms, but it still retains the function of producing mesenchyme.” In Pateria mineata, on the other hand, it is a relatively large vesicle, present on the left, side only, and in the future an attempt will be made to de- termine its fate. It is possible that, in this species and in the others where it forms mesenchyme, this posterior outgrowth does play a more or less important part in the history of the left cntero- cele from which the hydrocele arises, and that some of the diffi- culties in homologizing this last named cavity are due to its compound character.

To sum up: I am strongly inclined to look upon the anterior vesicle in Pateria mineata as the homologue of the proboscis coelom of Balanoglossus, while the posterior outgrowth corre- sponds to the trunk coeloni, and the intermediate pair of vesicles

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in the echinoderms, often with two hydropores in certain species, is the equivalent of the collar coelom.

A word remains to be said regarding the apical plate. In certain crinoids and echinoids it becomes a well developed organ in fairly old larvae, in which definite ganglion cells appear. As the adult nervous system arises from the ectoderm in close proximity to the hydrocele, it would appear that these embryonic nerve cells play no part in the process. Whether they degener- ate or become mesenchyme remains undetermined. It is fairly certain, however, that they furnish a strong bit of evidence in favor of the theory that the apical plate of the trochophore h a and of the echinoderm larva are homologous structures.

In Pateria mineata it has been shown that many of the cells of the apical plate completely lose their connection with the ectoderm and, as mesenchyme, migrate through the blastocele to the oesophageal section of the gut where they probably be- come transformed into circular muscles. All signs that they ever functioned as nervous elements appear to be wholly lost. In this connection one calls to mind the work of Katschenko (%), Platt ('94) and others who find that numerous cells leave the neural crest in the head region of various vertebrate embryos and become mesenchyme. It is possible that such cells represent ganglionic elements in the primitive ancestor which formerly innervated preotic structures now vanished or rudimentary. The matter, however, remains unsettled for the vertebrates; such is emphatically the case with the echinoderms where the species studied are fcw indeed and the data far too scanty to enable one to draw trustworthy conclusions.

LITERATURE CITED

GEMMILL, J. F. 1914 The development and certain points in the adult structure of the starfish hterias rubens. Phil. Trans. Royal SOC., v. 205, Series B.

HEIDER, I<. 1909 Zur Entwicklung von BnlanoglossuR elavigerus. Zool. Am., Bd. 34, 1903

KATSCHENKO, N. 1888 Zur Entwicklungsgeeschiehte des Yelachierembryos. Anat Anz., Bd 3

P u m , J. B. 1894 Ontogenetieche Differenzirung des Ectoderms in Necturus. Arch. mikr. Anat , Bd. 43.

PLATE 1

EXPLANATION OF FIGURE8

1 Lnte gastrula or early bipinnaria stage showing mesenchyme migrating from the apical plate (up) and corning in contact with the anterior vesicle (au) . The archentcrun bears the usual two enterocele pouches nnd a single left poste- rior one.

2 Anterior end 'of bipinnaria showing the completion of the mesenchyme formation a t the apical pole and its migration t o the esophageal region. The left hydmcele is provided with pore canal and hydropore. Zp left posterior vesicle.

3 Section of gastrula showing apical plate with signs of mesenchyme formation.

4 BipinnaFia showing mesenchyirie migrating past the anterior vesicle (nu) t o the esophagus. The left hydrocele has severed its connection with the archen- teron.

6 fjnrface view of gastrula immediately before mesenchyme development from apical plate.

l p left posterior vesicle in process of formation.

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EARLY DEVELOPMENT OF A STARFISH HAROLD HEATH

PLATE 1

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