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The Growth and Development of a Viviparous Compound Ascidian, Hypsistozoa Fasmeriana

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The Growth and Development of a Viviparous Compound Ascidian, Hypsistozoa Fasmeriana 435 The Growth and Development of a Viviparous Compound Ascidian, Hypsistozoa fasmeriana By BERYL I. BREWIN (From the Department of Zoology, University of Otago, New Zealand) With two plates (figs. 6 and 7) SUMMARY The viviparity recorded for this ascidian parallels that of placental mammals in reduction of the number and size of the eggs, the development of extra-embryonic membranes, and the prolongation of larval development with increase in the gesta- tion period. The ovum is alecithal, 25/J, in diameter; it develops within an oviducal brood pouch in which the lining cells become distinctly modified and which remains attached to the parent for 5^ months. Exposure of the embryo to the lumen of the pouch is brought about by rupture of the overlying follicle cells due to enzyme secretion by the dorsal-most cells of the blastula. Endodermal development is precocious. At the gastrula stage the future oesophageal region, the future stomach, and a pair of endodermal tubes are distinguishable. The paired endodermal tubes are unique in the ascidians. They are larval structures which disappear after metamorphosis and bear no relation to the functional stigmata of the oozooid. They resemble the branchial tubes of the Appendicularia, developing as blind outgrowths which later open through to the exterior; but in this species they open dorsally, not ventrally. They act as passive channels through which material from the pouch passes into the gut (a bolus being present from the gastrula stage onwards) and as anchoring strands for the ectotrophe. This extra-embryonic membrane formed by elevation of the dorsal ectoderm ulti- mately practically envelops the embryo and becomes apposed to the lining of the pouch. It is extremely simple, exhibits no vascularization, makes no actual liaison with the oviducal epithelium, and shows little cell differentiation. Extra-embryonic material reaches the embryo indirectly by diffusion across the ectotrophe (which unlike the remaining embryonic ectoderm secretes no test), and directly through the endodermal tubes. The latter method is the more important during early stages of development, the former during later stages. The production of an extremely large and complex tadpole with numerous buds at an advanced stage of organogenesis testifies to the success of this type of viviparity. INTRODUCTION TTYPSISTOZOA FASMERIANA (Michaelsen) is a compound as- _/ J_ cidian belonging to the sub-family Holozoinae (Berrill, 1950). Michael- sen in 1924, studying material collected during a month when gonads were not discernible, placed this species in the genus Distaplia Delia Valle. However, further investigations have shown that it does not belong to that genus and, in a survey of the Holozoinae (1953), the author erected the genus Hypsistozoa to house it. Four other members of the sub-family occur in New Zealand waters —Distaplia taylori Brewin (1950, 1951), D. marplesi Brewin (1952), and [Quarterly Journal of Microscopical Science, Vol. 97, part 3, pp. 435-454, September 1956.] 436 Brewin—The Development of a Viviparous Compound Ascidian D. knoxi Brewin (1954), all of which are endemic, and Sycozoa sigillinoides Lesson, which has a circum-south-polar distribution. As far as is known at present Hypsistozoa fasmeriana is endemic to New Zealand with a geographical range from Stewart Island in the south to Cape Kidnappers in the north (Michaelsen, 1924; Brewin, 1946, 1950, 1952a, 1953); it does not extend beyond the northern limits of sub-antarctic water (Deacon, 1937). It grows on coastal rocks about low-tide level in localities where water circulates freely and a good supply of both food and oxygen is available. Much of the material on which the present paper is based was collected in the vicinity of the Portobello Marine Biological Station, Otago Harbour, where observations have been made over the last 10 years, aquarium and laboratory facilities having made possible a survey of the complete life history. The greater part of the investigation, however, was carried out in the Depart- ment of Zoology, University of Otago. APPEARANCE OF COLONY AND STRUCTURE OF ZOOIDS The colonies are capitate (fig. 1, A), the plane of division between head and stalk being slightly off the horizontal. The test is a clear light brown and the FIG. 1. A, normal appearance of the colony. B, colony in late October with brood pouches projecting and some of the distal zooids in a state of regression, c, colony in November, after tadpole liberation, showing newly formed zooids and test near the stalk, regressing zooids, and test at the distal end. bodies of the purple zooids show through it by transparency. The zooids are arranged in branching systems which radiate around the common cloacal apertures, which are situated on the head region and mainly distally. The stalk of the colony contains the long posterior projections of the zooids, the vascular processes, and the buds derived from them. Throughout the sub-family Holozoinae the zooid structure is fairly uni- Brewin—The Development of a Viviparous Compound Ascidian 437 form. That of H. fasmeriana conforms to the general pattern as seen in the genera Distaplia and Sycozoa in form of the gut, position and mode of origin of the brood pouch, and structure and position of the cardiopericardium, but differs from it in shape and extent of the epicardium (a full description of which will be given in another paper) and in position of the gonads. In the Holozoinae the gonads are found typically in the abdominal region lying to the right side of the gut loop. A variation of this arrangement is seen in a small number of Distaplia species, the 'D. stylifera group', in which the gonads are FIG. 2. A, zooid with gonads and brood pouch; egg not yet liberated from the ovary, B, zooid in which gonads have regressed, showing the attached brood pouch containing an embryo at the gastrula stage, c, two-celled embryo with polar bodies attached. D, four-celled embryo with second polar body attached. contained in a sac-like diverticulum projecting from the abdominal region—a diverticulum which is quite independent of the vascular process. In Hypsis- tozoa fasmeriana a much more atypical arrangement is seen, the gonads lying not in the abdominal region but in the anterior end of the right side of the vascular process (fig. 2, A), and not in a sac-like diverticulum projecting into it as previously described (Brewin, 1946). Each zooid is hermaphrodite. The testis consists of 8 to 16 pear-shaped lobes and from it the sperm-duct runs up the dorsal side of the zooid to open near the atrial siphon. The ovary produces only one egg. The oviduct runs parallel and dorsal to the sperm-duct (fig. 2, A) but is shorter than it and opens at the base of the atrial cavity. A week or more before the egg leaves the ovary, the oviduct grows in length with the result that a short hairpin bend develops near the distal end. This projects outwards and causes a sac-like outgrowth of 438 Brewin—The Development of a Viviparous Compound Ascidian the zooid which appears on the right side close to the mid-dorsal line (fig. 2, A) and which acts as a brood pouch. ANNUAL RHYTHM IN THE COLONY Reproductive organs are not discernible throughout the year. The testis which ripens in May continues to produce sperms throughout June and July and finally undergoes dedifferentiation. The single egg, which is very small, passes up the oviduct late in May, in June, or occasionally early in July, eggs maturing first in the large zooids near the distal end of the head of the colony and later in the somewhat smaller zooids near the proximal end. Both fertiliza- tion of the egg and embryological development take place in the brood pouch (fig. 2, B), which grows considerably and retains its connexion with the parent zooid for approximately 5 months—about 5 \ months being the time taken for the fertilized egg to develop into an active tadpole. Three weeks or less before the end of embryonic development, dedifferentiation of the parent zooid begins. The anterior ends of the zooids are affected first and, as they become reduced in size, the test overlying them sinks in. Thus a pitting of the surface of the colony occurs, leaving only the portions of test overlying the brood pouches in their original position, and the colony attains the appearance shown in fig. 1, B. As dedifferentiation proceeds mesenchyme cells migrate towards the posterior ends of the zooids and accumulate in the lower halves of the vascular processes. At this season the processes become more opaque and are very easily seen through the transparent test of the stalk of the colony. Late in October or early in November the tadpoles become active and by their tail movements rupture the walls of the brood pouches, break through the overlying test, and swim off. Within the colony three processes are occurring, dedifferentiation of the parent zooids, liberation of the tadpoles, and formation of new zooids. (A full description of the origin and development of colonial buds will be given in a further paper.) Each bud gives rise to one zooid, the branchial aperture of which opens at the junction of the head and the stalk of the colony, and the ectoderm of which secretes test. Zooids and newly formed test are thus added to the proximal end of the colony (fig. 1, c), whilst the old test, which is practically all that is left of the distal end, is resorbed; and by a combination of these phenomena a new head is established. This is accomplished often within 2 weeks of tadpole liberation. Considerable increase in the size of the colony takes place during the summer months, when the metabolic rate of the zooids is high and growth occurs rather rapidly.
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