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The Sexual Development Ofsalpa Fusiformis (Cuvier)

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The Sexual Development Ofsalpa Fusiformis (Cuvier) The Sexual Development of Salpa fusiformis (Cuvier) Parti by MURIEL F. SUTTON1 From the Chelsea College of Science and Technology INTRODUCTION IN 1928 Brien wrote: 'L'embryogenese des Salpes quoique etudiee depuis long- temps, n'en est pas moins restee relativement obscure. Les interpretations les plus diverses, souvent contradictoires, ont ete emises.' The position has been altered but little by Brien's own work and by that of Berrill (1950) which merely claimed to have confirmed the observations made by Brooks (1893). The major discrepancies in the literature are summarized in the Table and can, without doubt, be attributed to two causes. The first is the peculiar nature of salp development. At an early stage the blastomeres become separated from each other by cells proliferated from the wall of the follicle in which the embryo begins its development. It is necessary for the later aggregation of the blastomeres to form the definitive embryo, that there should be spaces through and around which the blastomeres can move, a factor of salp development hitherto unrecognized. Later definitive body cavi- ties also appear within the developing oozooid. It has been found in the course of the present investigation that spaces formed by the degeneration of follicle cells provide blastomere migration routeways and that some of these spaces also become incorporated into the body cavities of the developing oozooid. Thus two types of cavity are produced as the result of follicle cell degeneration, those appearing at random—i.e. rarely in the same positions in any two embryos—and those which develop in almost identical positions in all embryos and which later become incorporated into the body cavities of the developing oozooids. Consider- able confusion in the identification of the two types of cavity is evident in the earlier accounts and almost certainly stems from the examination of too small a number of specimens. The examination of large numbers is essential. At no stage are any two specimens exactly alike, although all have certain features in common. To distinguish the significant from the relatively insignificant, e.g. in the nature of the future placental cavities, or the blastomere arrangement, 1 Author's address: Chelsea College of Science and Technology, Manresa Road, Chelsea, London, S.W. 3, U.K. [J. Embryol. exp. Morph. Vol. 8, Part 3, pp. 268-90, September 1960] M. F. SUTTON—SEXUAL DEVELOPMENT OF SALPA FUSIFORMIS 269 many animals must be examined at each stage. Berrill (1950) alone of all the authorities cited the number investigated. They range from a minimum of five of Salpa maxima to 47 of Thalia democratica. It seems possible that other authori- ties may similarly have examined only small numbers of specimens at many of the stages described. The second cause for confusion in the literature is a lack of material at certain critical stages of development. Thus, the earliest embryo examined by Korotneff (18966) was at the eight-cell stage; he, therefore, did not see the initiation of the immigration of the follicle cells ('calymmocytes', Salensky, 1876) between the blastomeres and so incorrectly identified the migrating calymmocytes as micro- meres, a criticism which he himself applied to Heider (1895):'... der Unterschied zwischen Blastomeren und Kalymmocyten von Heider nicht geniigend erkannt ist.' Both Korotneff and Heider confess to a lack of material; Korotneff came to the conclusion that the missing stages were 'nicht so besonders wichtig'; Heider, more circumspect, admitted that his material was limited and that, therefore, the conclusions to which he came, in particular that concerning the provenance of the cells forming the definitive oozooid, required further proof. The present in- vestigation has shown that Brien (1928) and Brooks (1893) would seem similarly to have lacked material of a critical nature. It was decided, therefore, that a re-investigation of the sexual development of a thecogone and of a gymnogone salp, S. fusiformis Cuvier and T. democratica Forskal, respectively, was desirable. The present work is an account of the early development of S. fusiformis. In its course more than 200 specimens were sec- tioned and an additional forty-two were subjected to tests while living or when freshly killed. Over 100 more have been examined for the later development, but there are still several stages lacking, and thus this part of the work is yet incom- plete. It is hoped that material recently received and promised will provide at least some if not all these stages, and that the account of the embryogenesis of S. fusiformis may soon be completed. MATERIAL AND METHODS The material for the present work was collected from the Atlantic Ocean (47° 20' N., 6° 23' W.) in May 1957, from the Straits of Messina in April 1955 and 1956, and a very small number was obtained from the Bay of Palermo in April 1956. Tests upon freshly killed or living material were performed at Palermo and Messina. The youngest blastozooids were obtained from the Atlan- tic Ocean, those rather older from all three sources. Specimens to be sectioned were preserved in Helly Zenker, aqueous Bouin, or in Du Boscq Brasil. From the great majority serial sections were cut at 2 fx and stained in Heidenhain's iron haematoxylin and counterstained with light green. The Feulgen test was applied to appropriate sections, and where positive results were confirmed by the use of Unna-Pappenheim (Brachet's technique, 1953) on identical sections, it has been assumed that desoxyribose nucleic acid 270 M. F. SUTTON—SEXUAL DEVELOPMENT OF SALPA FUSIFORMIS (DNA) was present. The distribution of glycogen was demonstrated by means of Best's carmine stain. Fresh material was vitally stained with neutral red, Janus green B, or was subjected to Mancuso's test for glutathione (1952). OBSERVATIONS There are two periods in the early development of S. fusiformis: (i) develop- ment within the follicle ('uterine sac', Brien, 1928) prior to the rupture of the atrial wall; and (ii) development of the blastophore from the rupture of the atrial wall to the period immediately after closure of the incubation fold. The development of the follicle prior to the rupture of the atrial wall Sawicki (1958) has described the development of the unfertilized egg in the chain salp. Unfortunately it has not been possible to obtain blastozooids in which the fertilized pre-cleavage egg is present, and thus the youngest embryo investi- gated in the course of the present work was at the two-cell stage of development. By the time two blastomeres are to be observed within the follicle the latter has reached its definitive position dorso-laterally and to the right, immediately posterior to the sixth muscle-band of the parent blastozooid. The sac lies close to the epithelium of a low fold of the atrial wall which, as a result, projects into the cloaca at this point. In this region the typical pavement epithelium lining the atrium becomes cubical or columnar. The follicle is bathed by the blood in a maternal blood-sinus. The sac is round and has a diameter of 008 mm. and within it, adjacent to the wall on one side, lie two relatively large contiguous blastomeres, bathed on their free surfaces by the follicular fluid. They are ovoid and slightly basophil. The cytoplasm contains granules of varying sizes, but there are few mitochondria. The nucleus is relatively small (Text-fig. 1). The second and third cleavages are normal. At the early eight-cell stage the blastomeres form a morula (Text-fig. 2) attached to the follicle wall by a small group of cells proliferated by the follicular epithelium. The blastomeres differ slightly in appearance from each other. For example, in one of my preparations those close to the attachment zone are flattened and the remainder round; while in others, although no such marked difference can be observed, the cells vary somewhat in shape. There is, however, no regularity in the arrangement and it is not possible to distinguish micro- from macromeres as Heider (1895) and Korotneff (18966) suggest. The variations in shape are undoubtedly due to com- pression by neighbouring blastomeres. During the eight-cell stage the first of the anomalies in salp development occurs. The follicle cells proliferate rapidly and the cells so produced insinuate themselves between the blastomeres in such a manner as to cover the morula completely and to enclose each blastomere in a single-layered sheath of flattened cells. Concurrently each blastomere becomes almost completely separated from M. F. SUTTON—SEXUAL DEVELOPMENT OF SALPA FUSIFORMIS 271 its sheath by a space. At one point alone are sheath and blastomere in contact (Text-fig. 3). Thus, while no evident blastula is formed, it is possible that the spaces separating the blastomeres from their sheaths represent an incipient blastocoel. The 'micromeres' described by Heider (1895) and Korotneff (1899) 005mm TEXT-FIG. 1. S. fusiformis: section through the follicle at the two-cell stage. Key to the text-figures All text-figures were drawn with the aid of a camera lucida. A. Atrium (cloaca). D.C.D. (B) Degenerating daughter cell, A.E. Atrial epithelium. within parent blastomere. A.Z. Attachment zone of follicle to D.C.F. Daughter cell forming. atrial epithelium. D.C.N. Nucleus of daughter cell. B. Blastomere. End. B. Endodermal blastomere. BI. Blastophore. F. Follicle. Bl.C. Cavity within the blastophore. F.C. Follicular cavity. Bl.-A.J. Junction between the blasto- F.E. Follicular epithelium. phore and the atrial epithe- F.S. Calymmocyte sheath. lium. i.e. Incubation cavity. Bl.E. Epithelium of blastophore. I.F. Incubation fold. B.(N-C). Neuro-chordal blastomeres. L.C. Lateral cavity. B.S. Maternal blood sinus. M.C. Maternal blood-corpuscle. C.
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