CHAPTER XI.

BRACHIOPODA[128].

[128] The classification of the Brachiopoda adopted in the present chapter is shewn in the subjoined table:

I. Articulata. { _a._ Rhynchonellidæ. { _b._ Terebratulidæ. { _a._ Lingulidæ. II. Inarticulata. { _b._ Craniadæ. { _c._ Discinidæ.

The observations which have been made on the developmental history of the Brachiopoda have thrown very considerable light on the systematic position of this somewhat isolated group.

_Development of the Layers._

For our knowledge of the early stages in the development of the Brachiopoda we are almost entirely indebted to Kowalevsky[129] (No. 326). His researches extend to four forms, Argiope, Terebratula, Terebratulina, and Thecidium. The early development of the first three of these takes place on one plan, and that of Thecidium on a second plan.

[129] Kowalevsky's Memoir is unfortunately written in Russian. The account in the text is derived from an inspection of his figures, and from an abstract in Hoffmann and Schwalbe's _Jahresberichte_ for 1873.

In Argiope, which may be taken as typical of the first group, the ova are transported into the oviducts (segmental organs) where they undergo their early development. The segmentation leads to the formation of a blastosphere, which then becomes a gastrula by invagination. The blastopore gradually narrows, and finally closes, while at the same time the archenteric cavity (fig. 135 A) becomes divided into three lobes, a median (_me_) and two lateral (_pv_). These lobes next become completely separated, and the middle one forms the mesenteron, while the two lateral ones give rise to the body cavity, their outer walls forming the somatic mesoblast, and their inner the splanchnic (fig. 135 B). The embryo now elongates, and becomes divided into three successive segments (fig. 135 B), which are usually, though on insufficient grounds (_vide_ Thecidium), regarded as equivalent to the segments of the Chætopoda. The alimentary tract is not continued into the hindermost of them.

[FIG. 135. TWO STAGES IN THE DEVELOPMENT OF ARGIOPE. (After Kowalevsky.)

A. Late gastrula stage. B. Stage after the larva has become divided into three segments. _bl._ blastopore; _me._ mesenteron; _pv._ body cavity; _b._ temporary bristles.]

In Thecidium the ova are very large, and development takes place in a special incubatory pouch in the ventral valve. The embryos are attached by suspenders to the two cirri of the arms which immediately adjoin the mouth. There is a nearly regular segmentation, and a very small segmentation cavity is developed. There is no invagination; but cells are budded off from the walls of the blastosphere, which soon form a solid central mass, enclosed by an external layer--the epiblast. In this central mass three cavities are developed, which constitute the mesenteron and the two halves of the body cavity. Around these cavities distinct walls become differentiated. The body (Lacaze Duthiers, No. 327) soon after becomes divided into two segments, of which the posterior is the smaller. The hinder part of the large anterior segment next becomes constricted off as a fresh segment, and subsequently the remaining part becomes divided into two, of which the anterior is the smallest. The embryo thus becomes divided into four segments, of which the two foremost appear (?) together to correspond to the cephalic segment of Argiope; but these segments are formed not, as in Chætopoda and other truly segmented forms, by the addition of fresh segments between the last-formed segment and the unsegmented end of the body, but by the interpolation of fresh segments at the cephalic end of the body as in Cestodes; so that the hindermost segment is the oldest. Assuming the correctness[130] of Lacaze Duthiers' observations, the mode of formation of these segments appears to me to render it probable that they are not identical with the segments of a Chætopod. A suspender is attached to the front end of each embryo. Before the four segments are established the whole embryo is covered with cilia[131], and two and then four rudimentary eyes are developed on the anterior segment of the body.

[130] It should be stated that it is by no means clear from Kowalevsky's figures that he agrees with Lacaze Duthiers as to the succession of the segments.

[131] Kowalevsky in his figures leaves the penultimate lobe unciliated.

_The history of the Larva and the development of the organs of the Adult._

[FIG. 136. LARVA OF ARGIOPE. (From Gegenbaur, after Kowalevsky.)

_m._ mantle; _b._ setæ; _d._ archenteron.]

Articulata. The observations of Kowalevsky and Morse have given us a fairly complete history of the larval metamorphosis of some of the Articulata, while some of the later larval stages in the history of the Inarticulata have been made known to us from the researches of Fritz Müller, Brooks, etc. The embryo of Argiope, which may be taken as the type for the Articulata, was left (fig. 135 B) as a three lobed organism with a closed mesenteron and a body cavity divided into two lateral compartments. On the middle segment of the body dorsal and ventral folds, destined to form the mantle lobes, make their appearance, and on the latter two pairs of bundles of setæ are present (fig. 135 B). The setæ together with the mantle folds grow greatly, and the setæ resemble in appearance the provisional setæ of many Chætopods (fig. 152). On the hinder border of the mantle cilia make their appearance. The anterior or cephalic segment assumes a somewhat umbrella-like form, and round its edge is a circlet of long cilia, while elsewhere it is provided with a coating of short cilia. Two pairs of eyes also arise on its anterior surface (fig. 136).

[FIG. 137. TWO STAGES IN THE DEVELOPMENT OF ARGIOPE, SHEWING THE FOLDS OF THE MANTLE GROWING OVER THE CEPHALIC LOBE. (After Kowalevsky.)

_m._ mantle fold; _me._ mesenteron; _pd._ peduncle; _b._ provisional setæ.]

After swimming about for some time the larva becomes fixed by its hind lobe, and becomes gradually transformed into the adult. The hind lobe itself becomes the peduncle. After attachment the mantle lobes bend forward (fig. 137 A, _m_), and enclose the cephalic lobe. The valves of the shell are formed on their outer surface as two delicate chitinous plates (fig. 137 B). At a somewhat later stage the provisional bristles are thrown off, and are eventually replaced by permanent setæ round the edge of the mantle. The cephalic lobe becomes located in the dorsal valve of the shell, and the mouth is formed near the apex of the cephalic lobe immediately ventral to the eye-spots, by an epiblastic invagination. The permanent muscles are formed out of the muscles already present in the embryo.

Around the mouth there arises a ring of tentacles, very possibly derived from the ciliated ring visible in fig. 136[132]. The ring of tentacles is placed obliquely, and the mouth is situated near its ventral side. The tentacles appear to form a post-oral circlet, like that of Phoronis (Actinotrocha): they gradually increase in number as the larva grows older.

[132] In the abstract in Hoffman and Schwalbe Kowalevsky is made to state that the tentacles spring from the border of the mantle. This can hardly be a correct account of what he states, since it does not fit in with the adult anatomy of the parts. The figures he gives might lead to the supposition that they sprang from the edge of the cephalic lobe, or perhaps from the dorsal lobe of the mantle.

[FIG. 138. DIAGRAM OF A LONGITUDINAL VERTICAL SECTION OF AN ADVANCED EMBRYO OF LINGULA. (After Brooks.)

_a._ end of valves; _b._ thickened margin of mantle; _c._ mantle; _d._ dorsal median tentacle; _e._ lophophore; _f._ lip; _g._ mouth; _h._ mantle cavity; _i._ body cavity; _k._ wall of oesophagus; _l._ oesophagus; _m._ hepatic chamber of stomach; _n._ intestinal chamber of stomach; _o._ intestine; _q._ ventral ganglion; _r._ posterior muscle; _s._ dorsal valve of shell; _t._ ventral valve of shell.]

Some of the later stages in the development of the Terebratulidæ have been made known to us by the observations of Morse (No. 328-9) on Terebratulina septentrionalis.

The most interesting point in Morse's observations on the later stages is the description of the gradual conversion of the disc bearing the circlet of tentacles into the arms of the adult. The tentacles, six in number, first form a ring round the edge of a disc springing from the dorsal lobe of the mantle; in their centre is the mouth. In the later stages calcareous spicula become developed on the tentacles. When the embryo is far advanced the tentacles begin to assume a horse-shoe arrangement, which bears a striking, though probably accidental, resemblance to that of the tentacles on the lophophore of the fresh-water Polyzoa. The disc bearing the tentacles is prolonged anteriorly into two processes, the free ends of the future arms. By this change of shape in the disc the tentacles form two rows, one on the anterior and one on the posterior border of the disc, and eventually become the cirri of the arms. The mouth is placed between the two rows of tentacles, where the two arms of the lophophore meet behind. The position of the mouth was the original centre of the ring of tentacles before they became pulled out into a horse-shoe form. In front of the mouth is a lip. The arms grow greatly in length in the adult Terebratulina. In Thecidium the oral disc retains the horse-shoe form, while in Argiope the embryonic circular arrangement of the tentacles is only interfered with by the appearance of marginal sinuations.

The shell is deposited as to chitinous plates, which subsequently become calcified. It undergoes in the different genera great changes of form during its growth.

With reference to the larval stages of other Articulata, a few points may be noted.

The three-lobed larva of Terebratulina septentrionalis is provided with a special tuft of cilia at the apex of the front lobe. The arms appear to originate, in Terebratulina caput serpentis, as two processes at the sides of the mouth, on which the tentacles are formed.

Provisional setæ do not appear to be formed in the lobed embryos of Thecidium and Terebratulina, but they appear at a later stage at the edge of the mantle in the latter form. The third lobe of Thecidium gives rise to the dorsal and ventral mantle lobes.

Inarticulata. The youngest stages in the development of the Inarticulata are not known, and in the earliest stages observed the shell is already developed. The young larvæ with shells differ however from those of the Articulata in the fact that they are free-swimming, and that the peduncle is not developed.

The larva of Discina radiata has been described by Fritz Müller (No. 331). It resembles generally a larva of the Articulata shortly after the tentacles have become developed. Five pairs of long provisional setæ are present, of which all but the hindermost are seated on the ventral lobe of the mantle. Shorter setæ are also lodged on the edge of the dorsal lobe. The mouth is placed on the ventral side of a protrusible oral lobe. It is imperfectly surrounded by four pairs of tentacles, which form a swimming apparatus.

A fuller history of the development of Lingula has been recently supplied by Brooks (No. 325). The youngest larva is enveloped in two nearly similar plate-like valves, covering the two mantle lobes. The mouth is placed at the centre of a disc, attached to the dorsal valve, on the margin of which is a ring of ciliated tentacles. The general position of the disc and its relations may be gathered from fig. 138, which represents a diagrammatic longitudinal vertical section of the embryo.

With the growth of the embryo the tentacles increase in number, the new pairs being always added between the odd dorsal tentacle and the next pair. There is an axial cavity in the tentacles which, unlike the cavity in the tentacles of the Polyzoa, does not communicate with the perivisceral cavity. As the tentacles increase in number, the lateral parts of the tentacular disc grow out into the two lateral arms of the adult, while the dorsal margin forms the median coiled arm. These changes are not effected till the larva has become fixed.

The attachment of the larva was not observed; but the peduncle, of which there is no trace in the young stages, grows out as a simple prolongation of the hinder end of the body while the larva is still free. It had already reached a very great length in the youngest fixed larva observed.

_Development of Organs._

The alimentary tract after the obliteration of the blastopore forms a closed sack, which becomes subsequently placed in communication with the exterior by the stomodæal invagination. The liver is formed as a pair of dorsal outgrowths of the mesenteron. From Brooks' observations on Lingula it would appear that the primitive mesenteron forms the stomach of the adult only, and that the intestine grows out from this as a solid process: this eventually meets the skin, and here the anus is formed. In the Articulata the mesenteron is aproctous.

The origin of the body cavity as paired archenteric diverticula has already been described. Its somatic wall becomes in Lingula ciliated, and its cavity filled with a corpusculated fluid, as in many Chætopods. It is eventually prolonged into the dorsal and ventral mantle lobes as a pair of horn-like prolongations into each lobe, which communicate with the body cavity by large ciliated openings. Some incomplete observations of Brooks on the development of the nervous system in Lingula shew that it arises in the embryo as a ring round the oesophagus with a ventral sub-oesophageal (fig. 138 _q_), and two lateral ganglia, and two dorsal otocysts. The ventral ganglion is formed as a thickening of the epiblast, with which it remains in continuity for life. The remainder of the ring grows out from the ventral ganglion as two cords, which gradually meet on the dorsal side of the oesophagus.

_General observations on the Affinity of the Brachiopoda._

The larva of Argiope, as has been noticed by many observers, has undoubtedly very close affinities with the Chætopoda. It resembles, in fact, a mesotrochal larval Chætopod with provisional setæ (_vide_ Chapter on Chætopoda). Lacaze Duthiers' observations point to the lobes of the larva not being true segments, and certainly the mesoblast does not in the embryo become segmented as it ought to do were these lobes true segments. If this view is correct the larva is to be compared to an unsegmented Chætopod larva. In Rhynchonella, however, indications of two segments are afforded in the adult in the two pairs of segmental organs.

Though the larval Brachiopod resembles a mesotrochal Chætopod larva, it does not appear to resemble the trochosphere larvæ so far described, or the more typical larvæ of the Chætopoda, in that the ring of tentacles, which is probably, as already mentioned, derived from the ciliated ring shewn in fig. 137, is _post-oral_, and not _præ-oral_. The ring of tentacles is like the ring in Actinotrocha (the larva of Phoronis) amongst the Gephyrea. Although there is no doubt a striking resemblance between the tentacular disc of a larval Brachiopod and the lophophore of a Polyzoon, which has been pointed out by Lankester, Morse, Brooks, etc., their homology is rendered, to my mind, very doubtful (1) by the fact that the lophophore is præ-oral in Polyzoa[133] and post-oral in Brachiopoda; and (2) by the fact that the concave side of the lophophore is turned in nearly opposite directions in the two forms. In Brachiopods it is turned dorsalwards, and in phylactolæmatous Polyzoa ventralwards.

[133] For the ectoproctous Polyzoa it might be held that the ciliated ring of tentacles is post-oral, but the facts of development recorded in the previous chapter appear to me to shew that this view is untenable.

The view of Morse, that the Brachiopoda are degraded tubicolous Chætopods, is not so far supported by any definite embryological facts. The development of the tentacular ring as well as its innervation from the sub-oesophageal ganglion prohibit us, as has been pointed out by Gegenbaur, from comparing it with the tentacles of tubicolous Chætopoda.

BIBLIOGRAPHY.

(325) W. K. Brooks. "Development of Lingula." _Chesapeake Zoological Laboratory, Scientific Results of the Session of 1878._ Baltimore, J. Murphy and Co.

(326) A. Kowalevsky. "Development of the Brachiopoda." _Protocol of the First Session of the United Sections of Anatomy, Physiology, and Comparative Anatomy at the Meeting of Russian Naturalists in Kasan_, 1873. (Russian.)

(327) H. Lacaze Duthiers. "Histoire de la Thécidie." _Ann. Scien. Nat. etc._ Ser. 4, Vol. XV. 1861.

(328) Morse. "On the Early Stages of Terebratulina septentrionalis." _Mem. Boston Soc. Nat. History_, Vol. II. 1869, also _Ann. & Mag. of Nat. Hist._, Series 4, Vol. VIII. 1871.

(329) ---- "On the Embryology of Terebratulina." _Mem. Boston Soc. Nat. History_, Vol. III., 1873.

(330) ---- "On the Systematic Position of the Brachiopoda." _Proceedings of the Boston Soc. of Nat. Hist._, 1873.

(331) Fritz Müller. "Beschreibung einer Brachiopoden Larve." Müller's _Archiv_, 1860.