Notes on Echinoderm Morphology, No. XI. On the Development of the Apical Plates in Amphiura squamata

Ludwig took up the subject in 1881,² and made the very striking discovery that two rings of radially situated plates are developed around the dorsocentral. Those of the distal ring are carried outwards from the disc at the ends of the growing arms, and are known as the terminals (fig. I, T); while the five plates of the proximal ring (4) remain on the disc close to the dorsocentral (1), and with it develop into the rosette of six primary plates which is a prominent feature on the abactina. surface of many adult Ophiurids. In Amphiura squamata two more rings of plates, the intermediate plates of Ludwig, eventually appear between these radials and the dorsocentral; and I expressed my belief in 18821 that they respectively represent the under-basals and basals of the dicyclic Crinoids (fig. ii, 2, 3). Two years later I pointed out the presence of this dicyclic base in various adult Ophiurids2; while the important discovery was announced by Sladen that it likewise occurs in many Asterids, both larval and adult, and also that in this group, just as in the Ophiurids, there are primary radial plates which remain on the disc while the terminals are carried outwards on the growing arms.³

These primary radial plates of Asterids and Ophiurids, including Amphiura, were homologised by both Sladen and myself with the first radials of the Crinoidea, the correspondence of which with the ocular plates of the Urchins had been long ago pointed out by Agassiz, Lovén, and others. No one had questioned this latter comparison, and it appeared equally indisputable that the primary radials of Amphiura were also homologous with the ocular plates of an Urchin, despite the relation of the latter to the eye-spot, a relation which is not characteristic of the primary radials in either of the three groups of brachiate Echinoderms.

“The question which plates in the young Amphiura correspond to the oculars of sea-urchins, assumes a new phase in the light of what we know of the permanent retention of the radials in the abactinal hemisome of the body of Amphiura, and the relation of the terminals to the primitive tentacle. Now that we know that the primary radials of Amphiura are not pushed out to the extremity of the rays, but always remain in the disk, and that another set of plates (terminals) do suffer this change, we have this difficulty in a comparison of the young Echinoid with the young Amphiura. The terminals of Amphiura are independent centres of calcification from the radials. If terminals and radials in Amphiura lie in the same radius, how can the one or the other, especially the former, be the same as the oculars of the sea-urchin ?”

I must confess that I do not quite understand what “new” phase this question has assumed since I wrote on the subject in 1882. All the facts to which Fewkes refers in the above passage were then known, having been discovered by Ludwig in the previous year; and it was these very facts which led me to homologise the primary radials of Amphiura and of the Ophiurids generally with the oculars of an Urchin. Sladen has accepted this view, and I am not aware of its ever having been disputed.1 I fail to see therefore what the new phase of the question may be to which Fewkes refers; for the fact which he mentions, that the radials of Ophiurids are not perforated for the eye-spots, like the oculars of an Urchin, is familiar to all Echinoderm students.

The radials of a Crinoid are equally devoid of any relation to the ambulacral structures, and yet they have been always regarded as homologous with the oculars of an Urchin by every writer who has dealt with the subject; and Fewkes2 arrives at the same conclusion as Sladen and myself had previously done, that “it seems more natural to compare radials in Amphiura with oculars in sea-urchins, notwithstanding the position of the eye-spot.” One or two further arguments may be adduced in favour of this view.

1. The embryonic radials of Ophiurids always remain upon the abactinal surface of the adult in the neighbourhood of the dorsocentral, and in many species develope into large plates, the primaries, which form a closed ring around the dorsocentral, just as in the early stages of the young Amphiura (fig. I, 4), though they are sometimes separated from it by intermediate plates (fig. II, 2,3). The oculars of an Urchin are also confined to the abactinal surface, and are separated from the dorsocentral by one ring of plates; while in most Crinoids the radials form a closed ring as in the earliest Amphiura, sometimes with one and sometimes with two rings of plates within them, just as in the two subsequent stages of the development of Amphiura.

On the other hand, the terminals of Ophiurids never form a closed ring of plates, but are well separated laterally from their very first appearance, and become more and more separated as the growth of the arms carries them away from the disc.

2. Sladen has shown that there are both terminal and radial plates in the young Asterid, just as in the young Ophiurid, and, like all his predecessors, he regards the terminals of Asterids as homologous with those of Ophiurids, although the latter have no eye-spot. If this homology be admitted—and I do not know of its ever having been disputed—we have an exactly similar case to that of the Ophiurid radials and the oculars of an Urchin, the one set of plates being associated with an eye-spot and the other not, although they are mutually homologous.

We may then, I think, assert, without fear of contradiction, that the radial plates are mutually homologous in Ophiurids and Urchins, Asterids and Crinoids, and also that the relative time of their appearance is of no general morphological importance. They appear before the basais in the Ophiurids, but after them in the other three groups, being also anticipated in Asterids¹ and Crinoids, ² and probably in the Urchins as well, by the dorsocentral.

Thus then, so far as concerns the primary radial plates of the apical system, Fewkes’s views are those of his predecessors, as indeed he himself admits. But he adds a suggestion which he considers as a direct sequence of the homology of the primary radials in Ophiurids and Crinoids, respectively.1 It is this: “The homology of the radial shields of the Amphiura with the first brachials of the Crinoid would seem not unreasonable. The only paired plates of the arms with which they could be compared are the adambulacral. With these, however, they have little resemblance save in their double origin.” If, as I suppose, Fewkes uses the term “first brachials” to denote the lowest joints of the two arms which are borne upon the radial axillaries of Pentacrinus, Ante don, and most recent Crinoids, there are at least three objections to an homology between them and the radial shields of the Ophiurids.

1. Many Crinoids, e. g. Hyocrinus, Rhizocrinus, Eudiocrinus, Cupressocrinus, &c., have no paired first brachials at all, for there are only five arms, one on each primary radial.

2. In those Crinoids which have ten or more arms there may be from one to seven radial plates between the primary or calyxradials and the paired first brachials. The only genera in which the latter plates ever rest directly on the primary radials are the aberrant Allagecrinus and Tribrachiocrinus. But this is not the case all round the cup, so that there are never ten first brachials to correspond to the ten radial shields which are so constant in Ophiurids. Then, again, each of the two larger radials in Catillocrinus may support as many as thirty arms. Where are the homologues of the two radial shields among all these first brachials ?

3. The radial shields of Ophiurids are invariably present, but they have no permanent relations to the primary radials. It is not unlikely that they are always developed immediately outside the primaries, where they remain in many species. But, on the other hand, they are often separated from the primaries by a series of intermediate plates which exhibit no general constancy of arrangement, and cannot therefore be directly compared to the single row of outer radials which presents itself so frequently in the Crinoids. ¹

These three considerations seem to me to indicate pretty clearly that it is useless to seek for the homologues of the radial shields in Ophiurids among the post-radial plates of Crinoids, more especially as we have not yet been able to identify them in any Asterid; and I prefer to regard them, like the terminals of both Ophiurids and Asterids, as plates which have no representatives in the Crinoidea.

Fewkes also discusses the homology of those intraradial or adaxial plates in the young Amphiura which I have regarded as homologous with the basais of Crinoids (figs, i—in, 3); and he suggests some doubts as to whether these plates “are basais in preference to other interradial plates.” ²

The plates in question have an interradial position within the ring of radials, i. e. between them and the dorsocentral; and at one stage of development they are the only adaxial interradial plates (fig. in, 3). They thus correspond exactly to the basais of monocyclic Crinoids, and to the so-called genitals of Urchins and Asterids. In a large number of Ophiurids they develop into large plates which form a closed ring round the dorsocentral, with the radials immediately outside them, precisely as in the apex of an Urchin, or the calyx of a stemless Crinoid like Uintacrinus. Fewkes must surely be aware of this fact, for there are numerous figures illustrating it in Lyman’s report on the “Challenger” Ophiurids; and it has formed the subject of much discussion by Sladen and myself. He supports his doubts by no arguments whatever, and entirely overlooks the important fact that the interradials of a Crinoid never form a closed ring within the circle of radials; for the only inter-radially situated plates which occupy such a position are the basais. It was this fact which led me to suggest that these first formed plates between the radials and the dorsocentral of the young Amphiura are the homologues of the Crinoidal basais and of the so-called genitals in Urchins and Asterids; and the six years’ work by myself and others since this suggestion was made has only served to make me more confident of its truth.

Ludwig gave a very clear description¹of the appearance of these inter-radially placed basais in the young Amphiura, and he pointed out how at a later stage a set of radially situated plates appears between them and the dorsocentral. He illustrated both conditions by figs. 24 and 25 of his series, the latter showing five and the former ten plates between the dorsocentral and the radial primaries. Fig. 24, which I here repeat (fig. ii), was copied by myself for the purpose of demonstrating that plates corresponding in position to the under-basals of a Crinoid (2) were developed in the young Amphiura, as well as those corresponding to the basais (3). Fewkes1 thinks, however, that it would have been better “in considering the relationship of the basais in the young Amphiura and their homologues in the projection of the calyx of an Antedon larva” if I had copied Ludwig’s fig. 25 instead of his fig. 24, i. e. that showing the monocyclic and not the dicyclic stage of Amphiura. It is curious that he fails to see the reason why I copied the figure of the older, in preference to that of the younger stage. Homologues of the Crinoidal basais had long been recognised in the so-called genital plates of Urchins and Starfishes. But up to the time of the publication of Ludwig’s memoir, representatives of the under-basals of a Crinoid2 were not known to exist in any of the Echinozoa; and it was for the purpose of demonstrating their presence in Amphiura that I copied the figure of the older and dicyclic condition rather than that of the younger and monocyclic one, with the remark,8 “The plates in the outer ring (fig. ii, 3) are inter-radial, while those of the inner ring next the dorso-central are radial in position (fig. ii, 2). In these plates we have, I believe, the representatives of the diycyclic base of Marsupites and other Crinoids, viz. a proximal ring of under-basals hitherto unknown in any of the Echinozoa, and a distal ring of interradial plates corresponding to the basais of the Crinoid and the genitals of the Asterid or Urchin, which have not been previously discovered in an Ophiurid.”

The doubts which seem to have occurred to Fewkes respecting the homologies of the adaxial ring of interradial plates in the young Amphiura which I have described as basais (figs, ii, iii, 3) appear to me to be due to the fact that the sequence of development of the apical plates is not the same in the American as in the European variety of Amphiura squamata. According to the description and figures of Ludwig the order in the latter form is as follows:—i. Radials (4); ii. Dorsocentral (1); iii. Basais (3); iv. Primary interradials (i.), and Under-basals (2); and v. Radial shields (r. s.). The under-basals and primary interradials seem to develop almost contemporaneously, fig. m showing two under-basals (2) in two rays between the dorsocentral (1) and the radials (4), and two very unequal abaxial or primary interradials (I.) each of them between a basal (3) and what I take to be an oral (5). ¹

This figure also shows that the fifth pair of side arm-plates (adambulacrals, ad₅.) appear about the same time.1 It is evident therefore from fig. in that the basais (3) reach a comparatively large size before the appearance of either interradials (I.), under-basals (2), or radial shields, and that the latter do not appear till after the formation of two at least of the under-basals and interradials.

From Fewkes’s descriptions and figures, however, it would seem that the radial shields appear much earlier in the American variety, and that the developmental sequence is altogether different from that described by Ludwig for the European form. Fewkes’s account is a little difficult to follow, owing to a want of precision in his terminology. Thus, for example, he three times uses the names “basais” and “interradials” as if they were synonymous; though every previous writer upon the calyx of the Crinoids and its relation to that of other Echinoderms has regarded the interradials and basais as fundamentally distinct in their morphological relations.

The earliest plates to appear in the inter-radial areas are the orals (figs, i, in, 5) which, as Fewkes himself describes on p. 128, are “forced to the actinal surface of the disc before the interradials arise.” He speaks of the latter, the first interradials, as forming “on the periphery of the abactinal hemisome on interradii between contiguous radialia. They are triangular in shape, and occupy a triangular interspace between adjoining primary radials.” He calls them, however, abaxial basais or abaxial interradials, and they are designated in his figure by the letters rp². (fig. iv, I). But as they are situated on the periphery of the abactinal hemisome outside the closed ring of radial primaries, it is altogether incorrect to speak of them as “basais.” This term is only applicable to the ring of interradial plates which are situated adaxially to the primary radials, i. e. between them and the dorsocentral (figs, ii, in, 3). The basais of a monocyclic Crinoid, as implied in their name, which was given to them by Johannes

Müller, are the nearest to the vertical axis of the calyx of all the plates in the interradial areas; and the term abaxial basais is thus self-contradictory. The proximal ring of interradially situated plates or basals (figs, n, m, 3) cannot be called abaxial; and the interradial plates belonging to a distal or abaxial ring (fig. iv, I) are most certainly not basais. The term adaxial interradials is an expressive (but lengthy) name for the basais (3), as it implies that they lie within the ring of radials (4). But “abaxial basais” as a synonym for the interradial plates (I) beyond this ring is an impossibility; and the use of the term by a trained morphologist like Fewkes has surprised me considerably.

According to his description1 the true basais or adaxial interradials seem to be the second set of plates to be developed interradially in the apical system of the American Amphiura, arising “in the corners left between the dorsocentral and contiguous radialia.” But before this happens the radial shields and two upper arm-plates have made their appearance (fig. iv, r. s.; d\ d*.). At any rate this is how I should interpret Fewkes’s fig. 19, which is copied in fig. iv. But it has puzzled me considerably, as he has omitted to letter the two plates next to the radial primary of the ray which he figures. I have marked them (4), regarding them as the primaries of the adjoining rays. But from his remarks on p. 128, which I have just quoted, it seems possible that they may be his adaxial interradials, i.e. the true basais, which appear before the radial shields, and not after them, as I have—perhaps erroneously—supposed. On the other hand, he states on the same page that a third ring of interradials “arises between the last-formed interradials and the periphery of the dorsocentral.” Which does he consider as representing the Crinoidal basais ? The second, or the third ring which is the most adaxial ? There is not a single reference to his figures in the whole course of his description on p. 128 of the development of the plates in the interradial areas, and I have therefore found much difficulty in understanding it. I say this because I wish to apologise in advance if I have misinterpreted his statements.

The under-basals, which are formed comparatively early in the European Amphiura squamata, do not seem to appear in the American variety till the radial shields have reached some size. If we take the number of adambulacral plates as a criterion, we find that the European form with three of these plates (fig. in), has five basais, two under-basals, and two interradials,1 but no radial shields; while the American form at the same stage has small shields and large interradials, but neither basais (?) nor under-basals (fig. iv). The differences in the sequence of formation of the apical plates in the two types may be summarised as follows:

Curiously enough, this considerable difference in the order of formation of the principal apical plates in the American and European varieties of one and the same species does not seem to have attracted Fewkes’s attention. Had it done so, I cannot but think that several passages in his memoir would have been differently expressed. Thus, for example, in discussing the nature of the dorsocentral on p. 123, he says: “If, however, in Echinoids this plate forms before the ocular and genitals, and in Amphiura after the same, one is tempted to ask whether they are homologous. One might, of course, avoid the difficulty by the truism that the relative time of development is of little consequence, and that the appearance of the plate in Amphiura is simply retarded. Such an escape from the difficulty does not give much satisfaction, even if we remember the abbreviated development of Amphiura.” But since the under-basals (and basais ?) appear after the radial shields in the West Atlantic, and before them in the Mediterranean, the late appearance of the dorsocentral in Amphiura as compared with the Urchins, is no argument whatever against the view that this plate is homologous in the two groups; and in fact if the relative time of appearance of the Apical Plates is to be taken as a criterion of homologies, it is scarcely worth while for us to attempt to arrive at a general understanding of the Apical System of Echinoderms.

Another point of the same nature is the discrepancy between the descriptions given by Fewkes and Ludwig respectively of the relative times of formation of the radials and terminals. Ludwig1 thinks it probable that the terminals appear before the radials; while Fewkes₂ believes the reverse to be the case, from the comparative sizes of the plates, though he admits that he has never seen a young Amphiura “with radials and without terminals.” But if we may judge from the analogy of the under-basals and radial shields it would appear that both observers may be in the right.

This is still more probable with regard to the development of the upper arm-plates. Fewkes says on p. 145: “I am led to suppose that the dorsals have been inadvertently omitted in certain of the figures of a young Amphiura by Ludwig (pl. xi, figs. 21, 25), for he has not represented these plates in a young specimen in which three pairs of side arm-plates are represented (pl. xi, fig. 21, ad3., ad4., ad’.).1 In a young Amphiura of about the same age (pl. iii, fig. 19)s at least one dorsal plate is formed, and in another as old as that represented in his fig. 25 (same plate) the dorsals have increased in number.3 In none of Ludwig’s figures are dorsals represented, though in figs. 21, 25, they must have been already formed.” Fewkes makes substantially the same statement in his concluding summary on p. 147,,f Dorsals are omitted in all Ludwig’s figures of the arm from the abactinal side. My figure is younger than his (pl. xi, fig. 21), in which a dorsal ought to be represented.”

It was, however, expressly noted by Ludwig₄ that “In Stadien welche nicht älter sind ais das in fig. 21 gezeichnete, sind noch gar keine Dorsalplatten vorhanden, obgleicb schon drei freie Armglieder angelegt sind.”

This passage must have altogether escaped Fewkes’s notice, or he would otherwise have scarcely have hinted at an inadvertent omission on the part of Ludwig, or have written so positively as to what plates ought or ought not to be represented in a particular developmental stage; while he makes no reference on his own part to the differences in the time of appearance of the radial shields, which are revealed by a comparison of his own observations with those of Ludwig, a fact which may eventually turn out to be of very considerable interest.