Skip to main content
SpringerLink
Log in

Locomotion of the filiform sperm of Littorina (Gastropoda, Prosobranchia)

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Summary

The filiform sperm of Littorina sitkana swims effectively in sea water and more viscous fluids, overcoming the problems of a non-uniform flagellar beat with an unusual mechanism, which involves three main events: (1) the sperm rotates anti-clockwise (looking from tail to head); then (2) stops rotating and stiffens itself to form a screw-shape, with the tail being held perpendicular to the middle piece, and finally; (3) reverses its rotation and propels itself forward in a clockwise spiral. The average velocity of sperm is approximately 185 μms with a rotational frequency of 24 revs. The mechanism of propulsion may involve two kinetic centers at opposite ends of the sperm, which coordinate their movements to produce anti-clockwise rotation, stationary twisting, or clockwise rotation, in a manner reminiscent of spirochaetes.

Littorina sperm also exhibit slower methods of propulsion including swimming backwards (tail first) at 18 μm, and “gliding” at about 30 μm.

The adaptive significance of the rapid propulsion is not obvious, because Littorina copulate and fertilize internally and at each stage in the transfer there are external aids to sperm transport, such as ciliary action (oviduct) and muscular expulsion (bursa and seminal receptacle). The filiform shape, however, is well-adapted for long-term storage in the female body. These points are discussed.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Anderson WA, Personne P (1967) The fine structure of the neck region of Helix aspersa. J Microsc 6:1033–1042

    Google Scholar 

  • Anderson WA, Personne P (1969) Structure and histochemistry of the basal body derivative of the neck and axoneme of spermatozoa of Helix aspersa. J Microsc 8:97–102

    Google Scholar 

  • Anderson WA, Personne P (1970) Recent cytochemical studies on the spermatozoa of some invertebrate and vertebrate species. In: Baccetti B (ed) Comparative spermatology. Academic Press, New York, p 29

    Google Scholar 

  • Ankel WE (1926) Spermiozeugmenbildung durch atypische und typische Spermien bei Scala und Janthina. Verh Dtsch Zool Suppl 2:193–202

    Article  CAS  Google Scholar 

  • Barnes H, Klepal W, Munn EA (1971) Observations on the form and changes in the accessory droplet and motility of the spermatozoa of some cirripedes. J Exp Mar Biol Ecol 7:173–196

    Google Scholar 

  • Bataillon C (1921) Spermies couplées et heterochromosome dans la lignée typique d'une Turritelle. C R Soc Biol Paris 84:219–222

    Google Scholar 

  • Berg HL (1974) Dynamic properties of bacterial flagellar motors. Nature 249:77

    Google Scholar 

  • Berg HL (1976) How spirochetes may swim. J Theor Biol 56:269–273

    Google Scholar 

  • Berg HL, Anderson RA (1973) Bacteria swim by rotating their flagellar filaments. Nature 245:380

    Google Scholar 

  • Bishop DW (1958) Motility of the sperm flagellum. Nature 182:228–237

    Google Scholar 

  • Blokhuis EWM (1961) Optical investigations on the movement of bull spermatozoa. In: Proc 4th Int Congress on Animal Reproduction, Vol 2. The Congress, The Hague, p 243

  • Brokaw CJ (1965) Non-sinusoidal bending waves of sperm flagella. J Exp Biol 43:155–169

    Google Scholar 

  • Brokaw CJ (1966) Effects of increased viscosity on the movements of some invertebrate spermatozoa. J Exp Biol 45:115–119

    Google Scholar 

  • Brokaw CJ (1972) Flagellar Movement: a sliding filament model. Science 178:455–462

    Google Scholar 

  • Brokaw CJ (1974) Movement of the flagellum in some marine invertebrate spermatozoa. In: Sleigh MA (ed) Cilia and Flagella. Academic Press, London New York, p 93

    Google Scholar 

  • Brokaw CJ (1976) Spermatozoan Motility: A biophysical survey. In: Duckett JG, Racey PA (eds) The biology of the male gamete. Linn Soc Lond, Academic Press, London, p 423

    Google Scholar 

  • Brokaw CJ (1979) Calcium-induced asymmetrical beating of triton-demembranated sea urchin sperm flagella. J Cell Biol 82:401–411

    Google Scholar 

  • Brokaw CJ, Gibbons IR (1973) Localized activation of bending in proximal medial and distal regions of sea urchin sperm flagella. J Cell Sci 13:1–10

    Google Scholar 

  • Buckland-Nicks JA (1973) The fine structure of the spermatozoan of Littorina (Gastropoda: Prosobranchia), with special reference to sperm motility. Z Zellforsch 144:11–29

    Google Scholar 

  • Buckland-Nicks JA (1974) Reproductive biology of Littorina PhD Thesis, Univ of Alberta, Edmonton, Canada

    Google Scholar 

  • Buckland-Nicks JA, Chia F-S (1976) Spermatogenesis of a marine snail Littorina sitkana. Cell Tissue Res 170:455–475

    Google Scholar 

  • Buckland-Nicks JA, Chia F-S (1977) On the nurse cell and the spermatozeugma in Littorina sitkana. Cell Tissue Res 179:347–356

    Google Scholar 

  • Chwang AT, Wu TY (1971) A note on the helical movement of micro-organisms. Proc Roy Soc Lond B 178:327–346

    Google Scholar 

  • Chwang AT, Winet H, Wu TY (1974) A theoretical mechanism of spirochaete locomotion. J Mechanochem Cell Motil 3:69–76

    Google Scholar 

  • Favard P, Andre J (1970) Mitochondria of Spermatozoa. In: Baccetti B (ed) Comparative spermatology. Academic Press, New York, p 415

    Google Scholar 

  • Fawcett DW (1958) The structure of the mammalian spermatozoon. Int Rev Cytol 7:195–235

    Google Scholar 

  • Fawcett DW (1962) Sperm tail structure in relation to the mechanism of movement. In: Bishop DW (ed) Spermatozoan motility. AAAS Press, Washington, p 147

    Google Scholar 

  • Franzen A (1955) Comparative morphological investigations into the spermiogenesis among Mollusca. Zool Bidrag Uppsala 30:399–456

    Google Scholar 

  • Fretter V (1941) The genital ducts of some British stenoglossan prosobranchs. J Mar Biol Ass UK 25:173–211

    Google Scholar 

  • Fretter V (1953) The transference of sperm from male to female prosobranch, with reference also to the pyramidellids. Proc Linn Soc Lond Sess 164:217–224

    Google Scholar 

  • Fretter V, Graham A (1962) British Prosobranch Molluscs, their functional anatomy and ecology. The Ray Soc, London

    Google Scholar 

  • Gaddum-Rosse P, Lee WI (1978) Sperm motility in cervical mucus — a comparative study. Anat Rec 190:593

    Google Scholar 

  • Gibbons BH (1980) Intermittent swimming in live sea urchin sperm. J Cell Biol 84:1–12

    Google Scholar 

  • Gibbons BH, Gibbons IR (1980) Calcium-induced quiescence in reactivated sea urchin sperm. J Cell Biol 84:13–27

    Google Scholar 

  • Gibbons IR (1965) Chemical dissection of cilia. Arch Biol 76:317–352

    Google Scholar 

  • Graham A (1954) Some observations on the reproductive tract of Janthina janthina L. Proc Malac Soc Lond 31:1–6

    Google Scholar 

  • Gray J (1953) Undulatory propulsion. Q J Microsc Sci 94:551–578

    Google Scholar 

  • Gray J (1955) The movement of sea urchin spermatozoa. J Exp Biol 32:775–801

    Google Scholar 

  • Gray J (1958) The movement of the spermatozoa of the bull. J Exp Biol 35:96–108

    Google Scholar 

  • Gray J, Hancock GJ (1955) The propulsion of sea urchin spermatozoa. J Exp Biol 32:802–814

    Google Scholar 

  • Hancock GJ (1953) The self-propulsion of micro-organisms through liquids. Proc Roy Soc Lond A 217:96–121

    Google Scholar 

  • Holwill MEJ, McGregor JL (1974) Micromanipulation of the flagellum of Crithidia oncopelti: 1. Mechanical effects. J Exp Biol 60:437–444

    Google Scholar 

  • Holwill MEJ, McGregor JL (1975) Control of flagellar waves in Crithidia oncopelti. Nature 255:157–158

    Google Scholar 

  • Idelman S (1961) Evolution de la spermatogenèse chez un Mollusque prosobranch: Turritella communis. In: Hormunk AL, Spit BJ (eds) Proc Reg Conf on EM. Delft, Netherlands, p 942

    Google Scholar 

  • Jahn TL, Bovee EC (1965) Movement and locomotion of microorganisms. Ann Rev Microb 19:21–58

    Google Scholar 

  • Jahn TL, Landemann MD (1965) Locomotion of spirochetes. Trans Am Micr Soc 84:395–406

    Google Scholar 

  • Jarosch (1967) Studien zur Bewegungsmechanik der Bacterien und Spirochaeten des Hochmoores. Österr Botan Z 114:255–306

    Google Scholar 

  • Lindemann CB, Rikmenspoel R (1972) Sperm Flagelly: autonomous oscillation of the contractile system. Science 175:331–338

    Google Scholar 

  • Lindemann CB, Fentie I, Rikmenspoel R (1980) A selective effect of Ni++ on wave initiation in bull sperm flagella. J Cell Biol 87:420–426

    Google Scholar 

  • Linke O (1933) Morphologie und Physiologie des Genital-Apparates der Nordsee Littorinin. Helgoländer wiss Meeresunter 19:1–60

    Google Scholar 

  • Longo FJ, Anderson E (1970) Structural and cytochemical features of the sperm of the cephalopod, Octopus bimaculatus. J Ultrastruct Res 32:94–106

    Google Scholar 

  • Mattei X (1970) Spermiogenèse comparée des poissons. In: Baccetti B (ed) Comparative spermatology. Academic Press, New York, p 57

    Google Scholar 

  • Phillips DM (1972) Comparative analysis of mammalian sperm motility. J Cell Biol 53:561–573

    Google Scholar 

  • Reger JF, Florendo NT (1969) Studies on motile, non-tubule containing filiform spermatozoa of the ostracod Cypridopsis: Mature spermatozoa. J Ultrastruct Res 28:250–258

    Google Scholar 

  • Reinke EE (1912) A preliminary account of the development of apyrene sperm in Strombus and of the nurse cells in Littorina. Biol Bull 22:319–327

    Google Scholar 

  • Rikmenspoel R (1978) Movement of sea urchin sperm flagella. J Cell Biol 76:310–322

    Google Scholar 

  • Sale WS, Gibbons IR (1979) Study of the mechanism of vanadate inhibition of the dynein cross-bridge cycle in sea urchin sperm flagella. J Cell Biol 82:291–298

    Google Scholar 

  • Satir P (1979) Basis of flagellar motility in spermatozoa, current status. In: Fawcett DW, Bedford JM (eds) The Spermatozoon: maturation, motility, surface properties and comparative aspects. Urban & Schwarzenberg Inc, Baltimore-Munich, p 81

    Google Scholar 

  • Silverman M, Simon M (1974) Flagellar rotation and the mechanism of bacterial motility. Nature 249:73

    Google Scholar 

  • Sleigh MA (1962) The biology of cilia and flagella. Pergamon Press, New York, p 57

    Google Scholar 

  • Sotelo JR, Trujillo-Cenoz O (1958) Electron microscope study of the kinetic apparatus in animal sperm cells. Z Zellforsch 48:565–601

    Google Scholar 

  • Taylor GI (1952) The action of waving cylindrical tails in propelling microscopic organisms. Proc Roy Soc Lond A 211:225–239

    Google Scholar 

  • Thompson TE (1966) Studies on the reproduction of Archidoris pseudoargus Rapp (Gastropoda: Prosobranchia). Phil Trans Roy Soc B 250:343–375

    Google Scholar 

  • Walker MH (1969) Coiling of the flagellar shaft in the head region of the mature sperm of Nucella lapillus. J Cell Sci 5:211–225

    Google Scholar 

  • Walker MH (1970) Some unusual features of the sperm of Nucella lapillus. In: Baccetti B (ed) Comparative spermatology. Academic Press, New York, p 383

    Google Scholar 

  • Walker MH, McGregor HC (1968) Spermatogenesis and the structure of the mature sperm in Nucella lapillus L. J Cell Sci 3:95–104

    Google Scholar 

  • Wang C-Y, Jahn TL (1972) A theory for the locomotion of spirochaetes. J Theor Biol 36:53–60

    Google Scholar 

  • Warner FD (1972) Macromolecular organization of eukaryotic cilia and flagella. In: Advances in cell and molecular biology Vol 2. Academic Press, New York, p 193

    Google Scholar 

  • Weibull C (1960) Movement. In: Gunsalus IC, Stanier RY (eds) The bacteria. Academic Press, New York London, p 153

    Google Scholar 

  • Woolley DM (1977) Evidence for “twisted-plane” undulations in golden hamster sperm tails. J Cell Biol 75:851–865

    Google Scholar 

  • Woolley DM (1979) Interpretations of the pattern of sperm tail movements. In: Fawcett DW, Bedford JM (eds) The spermatozoon; maturation, motility, surface properties and comparative aspects. Urban & Schwarzenberg Inc, Baltimore Munich, p 69

    Google Scholar 

  • Yasuzumi G, Yamaguchi S, Takahashi Y, Nishimura Y, Yamagishi N, Nakai Y, Naito N, Iwashita T (1975) The structural and cytological bases for vertebrate and invertebrate sperm motility. In: Afzelius B (ed) The functional anatomy of the spermatozoon. Pergamon Press, Oxford, p 151

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Zoology, University of Alberta, Edmonton, Alberta, Canada

    John A. Buckland-Nicks & Fu-Shiang Chia

Authors
  1. John A. Buckland-Nicks
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fu-Shiang Chia
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Buckland-Nicks, J.A., Chia, FS. Locomotion of the filiform sperm of Littorina (Gastropoda, Prosobranchia). Cell Tissue Res. 219, 27–39 (1981). https://doi.org/10.1007/BF00210016

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00210016

Key words

Search

Navigation