Advertisement

Marine Biology

, Volume 36, Issue 2, pp 169–182 | Cite as

Origin and development of the amoebocytes of Nicolea zostericola (Polychaeta: Terebellidae) with a discussion of their possible role in oogenesis

  • K. J. Eckelbarger
Article

Abstract

Three types of amoebocytes are present at different stages in the life history of Nicolea zostericola (Grube, 1860): a granular amoebocyte or “spindle cell” and 2 agranular amoebocytes, designated Type I and Type II. The agranular amoebocytes originate from specific sites on the lateral parietal peritoneum of the coelomic cavity in all the thoracic and a few abdominal segments. The origin of the granular amoebocyte is unknown. In juvenile worms the Type I amoebocyte enters the coelomic fluid and accumulates lipid and glycogen, presumably derived from reserves stored in the parietal peritoneum. Near the beginning of the vitellogenic phase of oogenesis, the Type I amoebocyte disappears and a Type II form is produced by the peritoneum. Type II cells differ cytologically from the Type I form by containing extensive rough ER (endoplasmic reticulum), Golgi complexes and free ribosomes; they appear to synthesize protein for export. At the end of vitellogenesis and near spawning, amoebocytes undergo alterations which include the migration of the nucleus to a central position, the formation of stacks and whirls of rough ER cisternae, and the appearance of vacuoles throughout the cytoplasm. It is suggested that the agranular amoebocytes obtain nutrients from food reserves stored in the parietal peritoneum and transfer them to the oocytes for use in yolk synthesis. The function of the granular amoebocytes is unknown.

Keywords

Polychaete Dense Granule Peritoneal Cell Parietal Peritoneum Coelomic Fluid 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Literature Cited

  1. Baskin, D.G.: The coelomocytes of nereid polychaetes. In: Contemporary topics in immunobiology, Vol. 4. pp 55–64. Ed. by E.L. Cooper, New York: Plenum Press 1974CrossRefGoogle Scholar
  2. Beams, H.W. and S.S. Sekhon: Electron microscope studies on the oocyte of the fresh-water mussel (Anodonta) with special reference to the stalk and mechanism of yolk deposition. J. Morph. 119, 447–502 (1966)CrossRefGoogle Scholar
  3. Bondi, C. and L. Facchini: Observations on the oocyte ultrastructure and vitellogenesis of Branchiobdella pentodonta Whitman. Acta Embryol. exp. 1, 225–241 (1972)Google Scholar
  4. Claparède, E.: Les annélides chétopodes du Golfe de Naples. Mém. Soc. Phys. Hist. nat. Genève 19, 313–584 (1868)Google Scholar
  5. —: Recherches sur la structure des annélides sédentaires. Mém. Soc. Phys. Hist. nat. Genève 22, 1–200 (1873)Google Scholar
  6. Clark, R.B.: Endocrinology and the reproductive biology of polychaetes. Oceanogr. mar. biol. A. Rev. 3, 211–255 (1965)Google Scholar
  7. Cuénot, L.: Études sur le, sang et le glandes lymphatiques dans la serie animale. Archs Zool. exp. gén. 9, 365–475 (1891)Google Scholar
  8. Dales, R.P.: The reproduction and larval development of Nereis diversicolor Müller. J. mar. biol. Ass. U.K. 29, 321–360 (1950)CrossRefGoogle Scholar
  9. —: Preliminary observations on the role of the coelomic cells in food storage and transport in certain polychaetes. J. mar. biol. Ass. U.K. 36, 91–110 (1957)CrossRefGoogle Scholar
  10. —: The coelomic and peritoneal cell systems of some sabellid polychaetes. Q. Jl microsc. Sci. 102, 327–346 (1961)Google Scholar
  11. —: Annelids, 200 pp. London: Hutchinson & Co. 1963Google Scholar
  12. —: The coelomocytes of the terebellid polychaete, Amphitrite johnstoni Malmgren. Q. Jl microsc. Sci. 105, 263–274 (1964)Google Scholar
  13. — and J.S. Pell: Cytological aspects of haemoglobin and chlorocruorin synthesis in polychaete annelids. Z. Zellforsch. mikrosk. Anat. 109 20–32 (1970)CrossRefGoogle Scholar
  14. Defretin, R.: Recherches sur la musculature des néréidiens au cours de l'épitoquie. Annls Inst. océanogr., Monaco 24, 117–257 (1949)Google Scholar
  15. Dhainaut, A.: Étude ultrastructurale de l'évolution des éléocytes chez Nereis pelagica L. (annélide polychète) a l'approche de la maturité sexuelle. C.r. hebd. Séanc. Acad. Sci., Paris 262, 2740–2743 (1966)Google Scholar
  16. —: Étude cytochimique et ultrastructurale de l'évolution ovocytaire de Nereis pelagica L. (annélide polychète). I. Ovogenese naturelle. Z. Zellforsch. mikrosk. Anat. 104, 375–390 (1970)CrossRefGoogle Scholar
  17. Durchon, M. et M. Lafon: Quelques données biochimiques sur les annélides. Annls Sci. nat. (Zool.) 13, 427–452 (1951)Google Scholar
  18. Eckelbarger, K.J.: Population biology and larval development of the terebellid polychaete Nicolea zostericola. Mar. Biol. 27, 101–113 (1974)Google Scholar
  19. —: A light and electron microscope investigation of gametogenesis in Nicolea zostericola (Polychaeta: Terebellidae). Mar. Biol. 30, 353–370 (1975)CrossRefGoogle Scholar
  20. Fáure-Fremiet, E.: Constitution et proprietes physicochimiques des éléocytes d'Amphitrite johnstoni Malmgren. Protoplasma 5, 321–337 (1929)CrossRefGoogle Scholar
  21. Fauvel, P.: Classes des annélides polychètes. Traité Zool. 5, 132–196 (1959)Google Scholar
  22. Freudweiler, H.: Studien über das Gefäßsystem niederer Oligochäten. Jena. Z. Naturw. 40, 383–422 (1905)Google Scholar
  23. Gabe, M.: Techniques histologiques, 1113 pp. Paris: Masson et Cie 1968Google Scholar
  24. Herpin, R.: Sur l'origine et le rôle des cellules à réserves de la cavité générale chez Perinereis cultrifera et Perinereis marioni (Aud. et Edw.) et sur la differenciation precoce de leurs oeufs. C.r. hebd. Séanc. Acad. Sci., Paris 173, 249–252 (1921)Google Scholar
  25. Hess, R.T.: The fine structure of coelomocytes in the annelid Enchytraeus fragmentosus J. Morph. 132, 335–352 (1970)CrossRefGoogle Scholar
  26. Issel, R.: Intorno agli escreti dei linfociti. Arch. zool. ital. 2, 125–135 (1905)Google Scholar
  27. Jordan, H.E.: The evolution of blood-forming tissues. Q. Rev. Biol. 8, 58–76 (1933)CrossRefGoogle Scholar
  28. Kollman, M.: Notes sur les réserves albuminoides des insectes et des annélides. Bull. Soc. zool. Fr. 34, 149–155 (1908)Google Scholar
  29. Marsden, J.R.: The coelomocytes of Hermodice carunculata (Polychaeta: Amphinomidae) in relation to digestion and excretion. Can. J. Zool. 44, 377–389 (1966)CrossRefGoogle Scholar
  30. —: The digestion and storage of fat by the amphinomid polychaete, Hermodice carunculata. Can. J. Zool. 46, 615–618 (1968)CrossRefGoogle Scholar
  31. Millonig, G.: Advantages of a phosphate buffer for OsO4 solutions in fixation. J. appl. Physiol. 32, p. 1637 (1961)Google Scholar
  32. Nørrevang, A.: Oogenesis in Priapulus caudatus Lamarck. An electron microscopical study correlated with light microscopical and histochemical findings. Vidensk. Meddr. dansk. naturh. Foren 123, 1–76 (1965)Google Scholar
  33. Ochi, O.: Blood pigments and erythrocytes found in some marine annelida. Mem. Ehime Univ. (Sect. 2; Ser. B, Biol.) 6, 23–91 (1969)Google Scholar
  34. Picton, L.J.: On the heart-body and coelomic fluid of certain polychaetes. Q. Jl microsc. Sci. 41, 263–302 (1898)Google Scholar
  35. Reynolds, E.S.: The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J. Cell Biol. 17, 208–212 (1963)CrossRefGoogle Scholar
  36. Richardson, K.C., L. Jarett and E.H. Finke: Embedding in epoxy resins for ultra-thin sectioning in electron microscopy. Stain Technol. 35, 313–323 (1960)CrossRefGoogle Scholar
  37. Romieu, M.: Les inclusions cristallines des éléocytes de Nereis et leurs relations avec la granulation éosinophile. C.r. hebd. Séanc. Acad. Sci., Paris 168, 367–369 (1921)Google Scholar
  38. —: Recherches histophysiologiques sur le sang et sur le corps cardiaque des annélides polychètes. Archs Morph. gén. exp. 15, 1–339 (1923)Google Scholar
  39. Ruddell, C.L.: The fine structure of oyster agranular amoebocytes from regenerating mantle would in the Pacific oyster, Crassostrea gigas. J. Invertebr. Path. 18, 260–268 (1971a)CrossRefGoogle Scholar
  40. —: The fine structure of the granular amoebocytes of the Pacific oyster, Crassostrea gigas. J. Invertebr. Path. 18, 269–275 (1971b)CrossRefGoogle Scholar
  41. Schaeppi, T.: Das Chloragogen von Ophelia radiata. Jena Z. Naturw. 28, 249–293 (1894)Google Scholar
  42. Schneider, G.: Über die Segmentalorgane und den Herzkörper einiger Polychaeten. Arb. K. NatForschGes. St. Petersburg 27, 135–137 (1897) [German translation]Google Scholar
  43. —: Über Phagocytose und Excretion bei den Anneliden. Z. wiss. Zool. 66, 497–520 (1899)Google Scholar
  44. Schroeder, P.C.: Studies on oogenesis in the polychaete annelid Nereis grubei (Kinberg). II. Oocyte growth rates in intact and hormone-deficient animals. Gen. Comp. Endocr. 16, 312–322 (1971)CrossRefGoogle Scholar
  45. Sichel, G.: Ricerche sui celomocite dei polichete: nota I.: osservaziani istologiche ed istochemiche sue celomocite di Perinereis macropus Clap. Boll. Zool. 28, 573–578 (1961)CrossRefGoogle Scholar
  46. —: Ricerche sui celomocite dei Polichete: nota II.: attivita fogocitaria et atracitoria dei celomocite di Perinereis macropus Clap. Boll. Sed. Accad. gioenia Sci. nat. (Ser. IV) 6, 321–323 (1962a)Google Scholar
  47. —: Ricerche sui celomocite dei Polichete: nota III.: coelomocite id Perinereis macropus in relozione all' occresimenta sometica e alla soiluppa sessuale. Bool. Sed. Accad. gioenia Sci. nat. (Ser. IV) 6, 325–328 (1962b)Google Scholar
  48. —: Ricerche sui celomocite dei Polichete: nota IV.: osservazione sull' ultrastruttura dei celomocite di Perinereis cultrifera (Grube). Atti Accad. gioenia Sci. nat. 8, 86–93 (1964)Google Scholar
  49. Spek, J.: Zustandsänderungen der Plasmakolloide bei Befruchtung und Entwicklung des Nereis Eies. Protoplasma 9, 370–427 (1930)CrossRefGoogle Scholar
  50. Stang-Voss, C.: Zur Ultrastruktur der Blutzellen wirbelloser Tiere. IV. Die Hämocyten von Eisenia foetida L. (Sav.) (Annelidae). Z. Zellforsch. mikrosk. Anat. 117, 451–462 (1971)CrossRefGoogle Scholar
  51. Thomas, J.G.: Pomatoceros, Sabella and Amphitrite. L.M.B.C. Mem. typ. Br. mar. Pl. Anim. 33, 1–88 (1940)Google Scholar
  52. Valembois, P.: Étude ultrastructurale des coelomocytes du lombricien Eisenia foetida Sav. Bull. Soc. zool. Fr. 96, 59–72 (1971)Google Scholar
  53. Watson, M.L.: Staining of tissue sections for electron microscopy with heavy metals. J. biophys. biochem. Cytol. 4, 475–478 (1958)CrossRefGoogle Scholar
  54. Williams, T.: On the blood proper and chylaqueous fluid of invertebrate animals. Phil. Trans. R. Soc. 142, 595–653 (1852)CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 1976

Authors and Affiliations

  • K. J. Eckelbarger
    • 1
  1. 1.Harbor Branch Foundation, IncFort PierceUSA

Personalised recommendations