The Formation and Fate of the Operculum and Gill-chambers in the tadpole of Rana temporaria.

Transcription

1 The Formation and Fate of the Operculum and Gill-chambers in the tadpole of Rana temporaria. By Gwendolen T. Brock, M.Sc, D.PM1. (Oxon.). With 16 Text-figures. THIS work has been undertaken with the object of establishing the exact method of formation of the operculum and gillchambers in the tadpole. It is also intended to follow up a suggestion of 0. H. Latter (1923) that branchial respiration continues after metamorphosis by means of paired apertures immediately in front of the bases of the freed anterior limbs. It is generally known that a fold of skin, the operculum, appears in front of the gill clefts shortly after hatching and grows back over the clefts, enclosing the gills in a gill-chamber. In Rana the right and left chambers communicate with one another ventrally, and the only opening to the exterior is a funnel-like opening on the left side of the tadpole. Text-book accounts, Balfour's ' Comparative Embryology ', for instance, are very vague in denning how the communication between right and left chambers is effected, and in what way the right opening is obliterated. An exact account, in outline, is given by Milnes Marshall. He says that the operculum grows backwards and fuses with the body-wall along the ventral surface and on the right side, leaving an opening on the left side which communicates with both chambers. This account I have found to be quite correct. I have examined a large number of serial sections of tadpoles, transverse and vertical, varying in age from the newly hatched tadpole to the metamorphosed frog, with four limbs, lungs, and external nares.

2 336 GWENDOLEN T. BROOK Text-figs. 1, 2, and 3 represent transverse sections through a young tadpole, soon after hatching. The operculum is forming. TEXT-FIGS our a.l., anterior limb; b.c, branchial cavity; co., coracoid; ect., ectoderm ; e.g., external gills ; g., gills; int., integument; l.a.l., left anterior limb ; l.g.c-, left gill-chamber ; o., operculum ; o.c, operculum complete; o.f., opercular fold ; o.v.f., opercular ventral fold; p.g., pectoral girdle; r.a.l., right anterior limb; r.g.c, right gill-chamber ; s.a.l., spiracular aperture, left; s.b.a., secondary branchial aperture; v.c.c, ventral communicating channel. Text-fig. 1, the most anterior section, shows separate right and left cavities, closed off from the exterior by the lateral folds.

3 OFERCULUM OF TADPOLE 337 A few sections further back, Text-fig. 2, the fold has extended towards the mid-ventral line, while in Text-fig. 3, a ventral fold of skin lies below and separate from the body-wall. Tracing this ventral fold backwards in the sections, it is found to end freely. TEXT-FIGS. 4-6 Both right and left cavities are wide open posteriorly. The operculum, then, must arise as a single fold of skin stretching in a convex sweep from the sides of the head right across the ventral surface of the body (Text-fig. 7 A). The lateral portions grow back much more rapidly than the ventral. Text-figs. 4, 5, 6 are sections of a slightly older tadpole in NO. 290 Z

4 338 GWENDOLEN T. BROCK which the operculum is completely formed. The most anterior section, Text-fig. 4, again shows separate right and left cavities. In Text-fig. 5 these are joined by a ventral communicating space, and in Text-fig. 6 the ventral fold has fused again with the body-wall behind the communicating channel. Text-fig. 6 passes through the funnel-like left opening. The cavity on the right side, when traced back in the sections, is obliterated without any opening to the exterior. A median vertical section, Text-fig. 11, shows the ventral TEXT-FIG. 7. communicating channel. The opercular fold of skin arises anteriorly, closes off the branchial channel, and fuses again with the body-wall. Text-fig. 7 A, B, c, D of tadpoles seen from the ventral surface illustrate the formation of the operculum as determined from these sections. In A the gills are uncovered, but the incipient fold is suggested by the dotted line. In B the lateral portions of the folds have grown back rapidly and partially cover the gills. In c the lateral portions have extended still farther posteriorly; the left has outdistanced the right, and a tiny fold has arisen across the whole ventral surface. The complete opercular fold is free and unfused with the body-wall posteriorly. In D the operculum has fused with the body-wall, ventrally and on the right; a small opening remains on the left, drawn out into a funnel-like opening. It is shown in Text-fig. 8, a lateral

5 OPEECULUM OF TADPOLE 389 view of the same tadpole. Thus the branchial cavity consists of right and left chambers with a ventral communicating space, the whole cavity having been cut off from the exterior by the opercular fold of skin. Since the branchial opening is at one time a single wide sweep from side to side across the ventral surface of the body, it is easy to understand that the definitive position may vary in different forms. Bombinator has a single ventral spiracle. otr sal TEXT-FIGS. 8, 9. It would be expected that the fusion of the operculum with the body-wall would extend along the fold, converging from both extremities and leaving a ventral opening instead of one on the left side. In Daetylethra there are right and left openings according to Huxley (Balfour). It is possible that one might find the ventral communication as well, but it seems more probable that the extension of the opercular fold ventrally and the formation of the ventral communicating channel is correlated with the single branchial opening in R a n a. One would, therefore, scarcely expect to find the ventral channel in Dactylethra. The anterior limb-buds form on the walls of the gill-chambers. They protrude into the cavity, Text-fig. 10, the epidermis of the Z2

6 340 GWENDOLEN T. BROCK limb being continuous with the lining of the gill-chamber. The lining of the whole branchial cavity is ectodermal in origin, but has become a single layered epithelium. As the limb-buds TEXT-FIG. 11. develop their epithelial covering assumes again the nature of a stratified epidermis. The buds grow into complete limbs within the gill-chambers. Text-fig. 12 is a transverse section of a tadpole shortly before metamorphosis. The tips of the digits and the elbows press against the wall of the operculum,

7 OPERCULUM OF TADPOLE 341 and it seems probable that both limbs at metamorphosis will break through the operculum. Milnes Marshall states that the right limb breaks through the operculum, but that the left emerges through the spiracle. 0. M. Helff (1926) describes paired perforations due to histolysis of the operculum, but does TEXT-FIGS not say whether the spiracle shares in the freeing of the left anterior limb, or whether it closes independently. 0. H. Latter (1923) observed that tadpoles continue to breathe by means of gills, as well as by lungs, even after the forelimbs have appeared at metamorphosis, until the tail is completely absorbed. He observed paired crescentic openings with thickened lips, immediately in front of the bases of the freed anterior limbs, Text-fig. 13, and found that a branchial current passed in at the nostrils and out through these crescentic apertures. My observations confirm those of Latter. Text-fig. 13 is a vertical section through a tadpole in which metamorphosis has taken place and the anterior limbs are freed. The section passes

8 342 GWENDOLEN T. BROCK through the left crescentic aperture, showing its thickened epidermal lip. The aperture commences immediately anteriorly to the base of the forelimb, but extends towards the mid-ventral line of the body. The apertures vary in size in different speci-,'ps TEXT-FIGS mens and on different sides of the same specimen. In no metamorphosed specimen is there a recognizable spiracle apart from the crescentic apertures. At the lateral extremity of each crescentic aperture the operculum fuses with the skin of the limb, the outer surface of the opercular fold forming a continuous epidermal layer with the integument of the limb, Text-fig. 15 A, B, C. Helff (1926) described the continuity of the operculum with the integument of the limb after the atrophy of a shelf of integument which projects from the anterior surface of the limb as a result of the perforation process. Helff, however, regards the openings in

9 OPERCULUM OF TADPOLE 343 the opercular wall as purely perforations for the freeing of the anterior limbs and does not recognize them as functional respiratory apertures. At the medial extremity the crescentic apertures appear to be gradually closing. The anterior and posterior lips in Text-fig. 16 A, have come together and fused, and in Text-fig. 16 B, in a slightly more medial position, a small core of isolated epidermal cells may be observed below the surface of the body-wall. The outer surface of the operculum here forms the surface of the body-wall. The ectoderm of the lining of the branchial cavity is single layered, and the volume of the branchial cavity is being diminished by the growing together of the medial and lateral walls of the cavity. Median sections of this tadpole show that the ventral communicating channel, present before metamorphosis, has been entirely obliterated in this manner. It would seem very likely then that the outer surface of the operculum persists as the permanent body-wall, and that the branchial cavity is obliterated by the sinking inwards of the operculum and the fusion of its inner surface with the inner wall of the branchial cavity, that is, with the original body-wall of the tadpole. This work was carried out in the Department of Zoology and Comparative Anatomy, University Museum, Oxford. LITERATURE CITED. Balfour, F. M. (1881). ' Comparative Embryology', vol. ii. Helff, 0. M. (1928). " Studies on Amphibian Metamorphosis. I. Formation of the Opercular Leg Perforation ", ' Journ. Exp. Biol.', vol. 45. Latter, 0. H. (1923). " An Overlooked Feature in the Four-legged Tadpole of Rana temporaria ", ' Nature ' (February 1923). Milnes Marshall, A. (1902). ' The Frog. An Introduction '.