Skip to main content
Log in

Euspermatozoa and paraspermatozoa in the trochoid gastropodZalipais laseroni (Trochoidea: Skeneidae)

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Pronounced sperm dimorphism is reported for the first time in the prosobranch order Vetigastropoda. Using transmission electron microscopy, it is demonstrated thatZalipais laseroni Kershaw (Trochoidea: Skeneidae) produces uniflagellate euspermatozoa (eupyrene, fertile sperm) and multiflagellate paraspermatozoa (oligopyrene, infertile sperm). Euspermatozoa show the following features: (1) a conical acrosomal vesicle; (2) a long tubular, helically coiled nucleus; (3) a short midpiece (mitochondrial sleeve surrounding a 3µm-long electron-dense rod); (4) a chambered body (? fused centrioles) continuous with the dense rod of the midpiece; (5) a flagellum (characterized by an electron-dense sheath surrounding and partly obscuring the central pair of tubules). Paraspermatozoa are composed of an elongate head (lacking an acrosomal complex), a short midpiece (centriolar rods interspersed with mitochondria), and a posterior tuft of flagella. The head consists of a rodshaped anterior body and a condensed nuclear remnant — the latter lodged in a shallow invagination of the anterior body. Multiple flagella are attached via centriolar rods to a layer of dense material lining the nuclear remnant membrane. During paraspermatozoan development, the nucleus partially degenerates, then condenses, while the endoplasmic reticulum (ER), apparently assisted by the Golgi complex, is responsible for production of numerous, electron-dense secretory vesicles. These vesicles subsequently fuse to form the elongate, anterior body of the head region. The ability of at least one line of trochoid gastropods to produce an oligopyrene, multiaxonemal paraspermatozoon, suggests that the Caenogastropoda (with this feature) might have been derived from the Vetigastropoda rather than from any other archaeogastropod source.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Literature cited

  • Azevedo, C., Lobo-Da-Cunha, A., Oliveira, E. (1985). Ultrastructure of the spermatozoon inGibbula umbilicalis (Gastropoda, Prosobranchia), with special reference to acrosomal formation. J. submicrosc. Cytol. 17: 609–614

    Google Scholar 

  • Azevedo, C., Oliveria, E. (1984). Two types of spermatozoa inGibbula umbilicalis. Cienc. biol. (Ser. C) 9: 25–26

    Google Scholar 

  • Cox, L. R. (1960). Thoughts on the classification of the Gastropoda. Proc. malac. Soc. Lond. 33: 239–261

    Google Scholar 

  • Daddow, L. Y. M. (1983). A double lead stain method for enhancing contrast of ultrathin sections in electron microscopy: a modified multiple staining technique. J. Microscopy 129: 147–153

    Google Scholar 

  • Franzén, A. (1955). Comparative morphological investigations into the spermiogenesis among Mollusca. Zool. Bidr. Upps. 30: 399–456

    Google Scholar 

  • Franzén, A. (1956). On spermiogenesis, morphology of the spermatozoon and biology of fertilization among invertebrates. Zool. Bidr. Upps. 31: 356–482

    Google Scholar 

  • Gall, J. G. (1961). Centriole replication. A study of spermatogenesis in the snailViviparus. J. biophys. biochem. Cytol. 10: 163–193

    Google Scholar 

  • Garreau de Loubresse, N. (1971). Spermiogenèse d'un gastéropode prosobranche:Nerita senegalensis: evolution du canal intranucleaire. J. Microscopie 12: 425–440

    Google Scholar 

  • Giusti, F., Selmi, M. G. (1982a). The morphological peculiarities of the typical spermatozoa ofTheodoxus fluviatilis (L.) (Neritoidea) and their implications for motility. J. Ultrastruct. Res. 78: 166–177

    Google Scholar 

  • Giusti, F., Selmi, M. G. (1982b). The atypical sperm in the prosobranch molluscs. Malacologia 22: 171–181

    Google Scholar 

  • Griffond, B. (1980). Etude ultrastructurale de la spermatogenèse typique deViviparus viviparus (L.), mollusque gastéropode. Archs Biol., Bruxelles 91: 445–462

    Google Scholar 

  • Griffond, B. (1981). Etude ultrastructurale de la spermatogenèse atypique deViviparus viviparus (L.), mollusque gastéropode. Archs Biol., Bruxelles 92: 275–286

    Google Scholar 

  • Hachiri, S., Higashi, S. (1972). Spermiogenesis in the melanian snailsSemisulcospira decipiens andSemisulcospira niponica. Mem. Fac. Educ. Shiga Univ. nat. Sciences 21: 43–51

    Google Scholar 

  • Haszprunar, G. (1988). On the origin and evolution of major gastropod groups, with special reference to the Streptoneura. J. mollusc. Stud. 54: 367–441

    Google Scholar 

  • Healy, J. M: (1982). Ultrastructure of paraspermatozoa, euspermatozoa and eusperm-like spermatozoa ofObtortio cf.fulva (Prosobranchia Cerithiacea). Helgoländer Meeresunters. 35: 489–500

    Google Scholar 

  • Healy, J. M. (1983). Ultrastructure of euspermatozoa of cerithiacean gastropods (Prosobranchia: Mesogastropoda). J. Morph. 178: 57–75

    Google Scholar 

  • Healy, J. M. (1984). The ultrastructure of gastropod spermatozoa and spermiogenesis. Ph. D. thesis. University of Queensland

  • Healy, J. M. (1986a). Ultrastructure of paraspermatozoa of cerithiacean gastropods (Prosobranchia: Mesogastropoda). Helgoländer Meeresunters. 40: 177–199

    Google Scholar 

  • Healy, J. M. (1986b). Euspermatozoa and paraspermatozoa of the relict cerithiacean gastropod,Campanile symbolicum (Prosobranchia, Mesogastropoda). Helgoländer Meeresunters. 40: 201–218

    Google Scholar 

  • Healy, J. M. (1987). Spermatozoan ultrastructure and its bearing on gastropod classification and evolution. Aust. Zool. 24: 108–113

    Google Scholar 

  • Healy, J. M. (1988). Sperm morphology and its systematic importance in the Gastropoda. Malac. Rev. (Suppl.) 4: 251–266

    Google Scholar 

  • Healy, J. M. (1989). Ultrastructure of spermiogenesis in the gastropodCalliotropis glyptus Watson (Prosobranchia: Trochidae), with special reference to the embedded acrosome. Gamete Res. 24: 9–20

    Google Scholar 

  • Healy, J. M., Jamieson, B. G. M. (1981). An ultrastructural examination of developing and mature paraspermatozoa inPyrazus ebeninus (Mollusca, Gastropoda, Potamididae). Zoomorphology 98: 101–119

    Google Scholar 

  • Houbrick, R. S. (1981). Anatomy, biology and systematics ofCampanile symbolicum with reference to adaptive radiation in the Cerithiacea. Malacologia 21: 263–289

    Google Scholar 

  • Ishizaki, T., Kato, K. (1958). The fine structure of atypical spermatozoa of the pond snailViviparus malleatus. Zool. Mag., Tokyo 67: 286–295

    Google Scholar 

  • Kohnert, R., Storch, V. (1983). Ultrastrukturelle Untersuchungen zur Morphologie und Genese der Spermien von Archaeogastropoda. Helgoländer Meeresunters. 36: 77–84

    Google Scholar 

  • Kohnert, R., Storch, V. (1984a). Vergleichend-ultrastrukturelle Untersuchungen zur Morphologie eupyrener Spermien der Monotocardia (Prosobranchia). Zool. Jb. 111: 51–93

    Google Scholar 

  • Kohnert, R., Storch, V. (1984b). Elektronenmikroskopische Untersuchungen zur Spermiogenese der eupyrenen Spermien der Monotocardia (Prosobranchia). Zool. Jb. 112: 1–32

    Google Scholar 

  • Koike, K. (1985). Comparative ultrastructural studies on the spermatozoa of the Prosobranchia (Mollusca: Gastropoda). Sci. Rep. Fac. Educ., Gunma Univ. 34: 33–153

    Google Scholar 

  • Melone, G., Lora Lamia Donin, D., Cotelli, F. (1980). The paraspermatic cell (atypical spermatozoon) of the Prosobranchia: a comparative ultrastructural study. Acta zool., Stockh. 61: 191–201

    Google Scholar 

  • Nishiwaki, S. (1964). Phylogenetical study on the type of the dimorphic spermatozoa in Prosobranchia. Sci. Rep. Tokyo Kyoiku Daig. (Sect. B) 11: 237–275

    Google Scholar 

  • Rouse, G. W., Jamieson, B. G. M. (1987). An ultrastructural study of the spermatozoa of the polychaetesEurythoe complanata (Amphinomidae),Clymenella laseroni andMicromaldane laseroni (Maldanidae) with definition of sperm types in relation to reproductive biology. J. submicrosc. Cytol. 19: 573–584

    Google Scholar 

  • Salvini-Plawen, L., Haszprunar, G. (1987). The Vetigastropoda and the systematics of streptoneurous Gastropoda (Mollusca). J. Zool., Lond. 211: 747–770

    Google Scholar 

  • Selmi, M. G., Giusti, F. (1980). Structure and function in typical and atypical spermatozoa of Prosobranchia (Mollusca). 1.Cochlostoma montanum (Issel) (Mesogastropoda). Atti Accad. Fisiocr. Siena 1980: 115–167

    Google Scholar 

  • Yasuzumi, G., Tanaka, H. (1958). Spermatogenesis in animals as revealed by electron microscopy. VI. Researches on the spermatozoon dimorphism in a pond snailCipangopaludina malleata. J. biophys. biochem. Cytol. 4: 621–632

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by G. F. Humphrey, Sydney

Rights and permissions

Reprints and permissions

About this article

Cite this article

Healy, J.M. Euspermatozoa and paraspermatozoa in the trochoid gastropodZalipais laseroni (Trochoidea: Skeneidae). Mar. Biol. 105, 497–507 (1990). https://doi.org/10.1007/BF01316321

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01316321

Keywords

Navigation