Summary
The development of the egg envelope and its incorporation into the larval cuticle of the polychaete Phragmatopoma lapidosa, was studied by correlative scanning and transmission electron microscopy. The mature egg possesses an envelope composed of five zones including an outer granular zone formed by the tips of the egg microvilli. The formation of the granules is described and their functions are discussed. The entire egg envelope is retained as the larval cuticle up to the 16 h trochophore stage. From this stage to about the 60 h larval stage, the envelope is gradually lost and replaced by a cuticle consisting of branching microvilli. The cuticle of the 20 day larva is composed of highly branching microvilli penetrating a homogeneous electron opaque cuticle. The possible functions of the cuticle among the Annelida are discussed.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Ahern, G.A., Gomme, J.: Transport of exogenous D-glucose by the integument of a polychaete worm (Nereis diversicolor Muller). J. exp. Biol. 62, 243–264 (1975)
Allen, M.J.: Embryological development of the polychaetous annelid Diopatra cuprea (Bosc). Biol. Bull. 116, 339–361 (1959)
Allen, M.J.: Embryological development of a syllid, Autolytus fosciatus (Bosc) (Class Polychaeta). Biol. Bull. 127, 187–205 (1964)
Chia, F.S.: Adaptive significance of marine invertebrates in assimilation of dissolved organic molecules from seawater. Chinese Bioscience 1, 41–48 (1972)
Chien, P.K., Stephens, G.C., Healey, P.L.: The role of ultrastructure and physiological differentiation of epithelia in amino acid uptake by the bloodworm, Glycera. Biol. Bull. 142, 219–235 (1972)
Coggeshall, R.E.: A fine structural analysis of the epidermis of the earthworm, Lumbricus terrestris. L. J. Cell Biol. 28, 95–108 (1966)
Colwin, L.H., Colwin, A.L.: Changes in the spermatozoon during fertilization in Hydroides hexagonus (Annelida). I. Passage of the acrosomal region through the vitelline membrane. J. biophys. biochem. Cytol. 10, 231–254 (1961)
Dales, R.P.: The reproduction and larval development of Nereis diversicolor O.F. Muller. J. Mar. Biol. Ass. U.K. 29, 321–360 (1950)
Day, J.H.: The development of Capitellides giardi Mesnil. Rep. Dove Mar. Lab. 4, 31–37 (1937)
Desser, S.S., Weller, I.: Ultrastructural observations on the body wall of the leech, Batrocobdella picta. Tissue and Cell 9, 35–42 (1977)
Eckelbarger, K.J.: Developmental studies of the postsettling stages of Sabellaria vulgaris (Polychaeta: Sabellariidae). Mar. Biol. 30, 137–149 (1975)
Eckelbarger, K.J.: Larval development and population aspects of the reef-building polychaete Phragmatopoma lapidosa from the east coast of Florida. Bull. Mar. Sci. 26, 117–132 (1976)
Eckelbarger, K.J., Chia, F.S.: Scanning electron microscope observations of the larval development of the reef-building polychaete Phragmatopoma lapidosa. Canad. J. Zool. 54, 2082–2088 (1976)
Eisig, H: Zur Entwicklungsgeschichte der Capitelliden. Mitt. Zool. Stat. Neapel. 13. 1–292 (1898)
Franklin, L.E.: An egg cell-membrane derivative on the vitelline membrane of annelid eggs. Exp. Cell Res. 43, 673–675 (1966)
Gwynn, I., Jones, P.C.T.: On the egg investments and fertilization reaction in Pomatoceros triqueter L. Z. Zellforsch. 113, 388–395 (1971)
Herpin, R.: Recherches biologiques sur la reproduction et le développement de quelques Annélides Polychètes. Bull. Soc. Sci. Mat. Quest. Fr. 5, 1–250 (1926)
Hess, R.T., Menzel, D.B.: The fine structure of the epicuticular particles of Enchytraeus fragmentosus. J. Ultrastruct. Res. 19, 487–498 (1967)
Holborow, P.L., Laverack, M.S., Barber, V.C.: Cilia and other surface structures of the trochophore of Harmothoë imbricata (Polychaeta). Z. Zellforsch. 98, 246–261 (1969)
Humphreys, S., Porter, K.R.: Collagenous and other organizations in mature annelid cuticle and epidermis. J. Morph. 149, 33–52 (1976)
Krall, J.F.: The cuticle and epidermal cells of Dero obtusa (Family Naididae). J. Ultrastruct. Res. 25, 84–93 (1968)
Lane, N.J.: Microvilli on the external surfaces of gastropod tentacles and body-walls. Quart. J. micr. Sci. 104, 495–504 (1963)
Lawry, J.V.: Structure and function of the parapodial cirri of the polynoid polychaete, Harmothoë Z. Zellforsch. 82, 345–361 (1967)
Luft, J.H.: Improvements in epoxy resin embedding methods. J. biophys. biochem. Cytol. 9, 409–414(1961)
Millonig, G.: Advantages of a phosphate buffer for OsO4 solutions in fixation. J. appl. Physiol. 32, 1637 (1961)
Misuraca, G., Zs.-Nagy, I.: Some new structural data concerning the cuticle of Eunicidae (Polychaeta, Annelida). Pubbl. Staz. Zool. Napoli 38, 249–261 (1970)
Novikoff, A.B.: Embryonic determination in the annelid Sabellaria vulgaris. I. The differentiation of the ectoderm and endoderm when separated through induced exogastrulation. Biol. Bull. 74, 198–210 (1938)
Okada, K.: The gametogenesis, the breeding habits, and the early development of Arenicola cristata, a tubicolous polychaeta. Sci. Rep. Tohoku Imp. Univ. 16, 99–146 (1941)
Pasteels, J.J.: Etude au microscope électronique de la réaction corticale. II. La réaction corticale de l'oeuf vierge de Sabellaria alveolata. J. Embryol. exp. Morph. 13, 327–339 (1965a)
Pasteels, J.J.: Aspects structuraux de la fécondation vus au microscope électronique. Arch. Biol. (Liège) 76, 463–509 (1965b)
Potswald, H.E.: Reproductive biology and development of Spirorbis (Polychaeta, Serpulidae). Doctoral thesis, University of Washington, Dissertation Abstracts No. 65-8528 (1965)
Potswald, H.E.: A fine structural analysis of the epidermis and cuticle of the oligochaete Aeolosoma bengalense Stephenson. J. Morph. 135, 185–212 (1971)
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)
Rice, M.E.: A comparative study of the development of Phascolosoma agassizii, Golfingia pugettensis and Themiste pyroides with a discussion of developmental patterns in the sipuncula. Ophelia 4, 143–171 (1967)
Rice, M.E.: Observations on the development of six species of Caribbean Sipuncula with a review of development in the phylum. Proceedings of the International Symposium on the Biology of the Sipuncula and Echiura, Kotor, June 18–25 (1970)
Rice, M.E.: Morphology, behavior, and histogenesis of the pelagosphera larva of Phascolosoma agassizii (Sipuncula). Smithson. Contr. Zool. 132, 1–51 (1973)
Rice, M.E.: Larval development and metamorphosis in Sipuncula. Amer. Zool. 16, 563–571 (1976)
Richards, K.S.: The ultrastructure of the cuticle of some British lumbricids (Annelida). J. Zool. (Lond.) 172, 303–316 (1974)
Rieger, R.M., Rieger, G.E.: Fine structure of the archiannelid cuticle and remarks on the evolution of the cuticle within the Spiralia. Acta zool. (Stockh.) 56, 53–68 (1976)
Schulte, E., Riehl, R.: Elektronenmikroskopische Untersuchungen an den Tentakeln von Lanice conchilega (Polychaeta, Sedentaria) Helgoländer wiss. Meeresunters. 28, 191–205 (1976)
Segrove, F.: The development of the serpulid Pomatoceros triqiteter L. Quart. J. micr. Sci. 82, 467–540 (1941)
Smith, R.I: On the early development of Nereis diversicolor in different salinities. J. Morph. 114, 436–464 (1964)
Stephens, G.C.: Dissolved organic matter as a potential source of nutrition for marine organisms. Amer. Zool. 8, 95–106 (1968)
Storch, V., Welsch, U.: Über die Feinstruktur der Polychaeten-Epidermis (Annelida). Z. Morph. Tiere 66, 310–311 (1970)
Tyler, A.: The biology and chemistry of fertilization. Amer. Naturalist 99, 309–334 (1965)
Watson, M.L.: Staining of tissue sections for electron microscopy with heavy metals. J. biophys. biochem. Cytol. 4, 475–478 (1958)
Wilson, D.P.: The larvae of the British sabellarians. J. Mar. Biol. Ass. U.K. 16, 221–268 (1929)
Wilson, D. P.: Notes on the early stages of two polychaetes, Nepthys hombergi Lamarck and Pectinaria koreni Malmgren. J. Mar. Biol. Ass. U.K. 21, 305–310 (1936)
Wilson, E.B.: Early stages of some polychaetous annelids. Stud. Biol. Lab. Johns Hopkins Univ. 2, 271–299 (1883)
Author information
Authors and Affiliations
Additional information
We thank Mrs. P.A. Linley, Mr. R. Koss, and Mr. G.D. Braybrook for technical assistance. Special appreciation is extended to Dr. Edward Ruppert for his contributions to many stimulating discussions during the course of this investigation. This study was partially supported by a National Research Council of Canada grant to F.S. Chia
Contribution No. 76, Harbor Branch Foundation, Inc.
Rights and permissions
About this article
Cite this article
Eckelbarger, K.J., Chia, FS. Morphogenesis of larval cuticle in the polychaete Phragmatopoma lapidosa . Cell Tissue Res. 186, 187–201 (1978). https://doi.org/10.1007/BF00225530
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00225530