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Spermatozoa and spermatogenesis in a monoplacophoran mollusc, Laevipilina antarctica: ultrastructure and comparison with other Mollusca

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Abstract

Ultrastructural features of spermatozoa and spermatogenesis are described for the first time in a monoplacophoran and compared with data for other conchiferan molluses. Spermatozoa of Laevipilina antarctica Warén and Hain, 1992, are of the structurally simple, aquasperm type, featuring a conical acrosome, a compact nucleus with lacunae, a short midpiece and a single flagellum. The acrosomal vesicle shows an electron-dense inner zone, and a basal invagination (subacrosomal space) contains granular material but no axial rod. The nucleus exhibits a shallow indentation apically which contains subacrosomal material, and five (sometimes four) indentations posteriorly which partially accommodate the five (rarely four) midpiece mitochondria. Two centrioles are present, the distal connected to the annulus by satellite fibres and acting as a basal body for the flagellum (axoneme probably 9+2 structure). Spermatogonia, characterized by an oblong nucleus and one or two nucleoli, line the basal membrane of the testis wall; spermatids of varying stages of maturity occupy the remainder of the testis. Acrosome and flagellum production is already well advanced in spermatids and probably commences at the spermatocyte stage. Cytoplasmic bridges occur in all developmental stages, most visibly in spermatids. The spermatid chromatin condenses in large tracts, leaving electron-lucent lacunae. Mitochondria collect posteriorly and form, presumably by fusion, the five (or four) larger, spherical mitochondria which gather around the centrioles.

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References

  • Azevedo C (1981) The fine structure of the spermatozoon of Patella lusitanica (Gastropoda: Prosobranchia), with special reference to acrosome formation. J submicrosc Cytol 13:47–56

    Google Scholar 

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

    Google Scholar 

  • Baccetti B, Afzelius BA (1976) The biology of the sperm cell. Monographs in developmental biology. Vol. 10. S. Karger, Basel

    Google Scholar 

  • Bieler R, Hadfield MG (1990) Reproductive biology of the sessile gastropod Vermicularia spirata (Cerithioidea: Turritellidae) J mollusc Stud 56:205–219

    Google Scholar 

  • Buckland-Nicks J, Chia F-S (1989) Spermiogenesis in Chaetoderma sp. (Aplacophora) J exp Zool 252:308–317

    Google Scholar 

  • Buckland-Nicks J, Chia F-S, Koss R (1990) Spermiogenesis in Polyplacophora, with special reference to acrosome formation (Mollusca). Zoomorphology 109:179–188

    Google Scholar 

  • Buckland-Nicks JA, Koss R, Chia F-S (1988) The elusive acrosome of chiton sperm. Int J Invert Reprod Dev 13:193–198

    Google Scholar 

  • Buckland-Nicks JA, Scheltema AH (1993) Comparative spermatology of Aculifera has important implications for the early evolution of Mollusca. In: Origin and evolutionary radiation of the Mollusca (Malacological Society of London, Centenary Symposium) 14–16 September, 1993 (Abstract). Malacological Society, London p. 42

    Google Scholar 

  • Cesari P, Giusti F, Minelli A (1987) Recent monoplacophorans in the Mediterranean Sea: findings of Neopilina zografi (Dautzenberg & Fischer, 1896) off the Isles of Capraia, Gorgona, Corsica and Sardinia (Mollusca, Monoplacophora). Boll Malacol (Milano) 23:107–118

    Google Scholar 

  • Daddow LYM (1983) A double lead stain method for enhancing contrast of thin sections in electron microscopy: a modified multiple staining method. J Microscopy 129:147–153

    Google Scholar 

  • Daddow LYM (1986) An abbreviated method of double lead stain technique. J submicrosc Cytol 18:221–224

    Google Scholar 

  • Dietrich HF, Fontaine AR (1975) A decalcification method for ultrastructure of echinoderm tissue. Stain Technol 50:351–354

    Google Scholar 

  • Dorange G, Le Pennec M (1989) Ultrastructural characteristics of spermatogenesis in Pecten maximus (Mollusca, Bivalvia). Invert Reprod Develop 15:109–117

    Google Scholar 

  • Drozdov AL, Reunov AA (1986) Spermatogenesis and the sperm ultrastructure in the mussel Modiolus difficilis. Tsitologiya 28:1069–1074 [In Russ., Engl summary]

    Google Scholar 

  • Dufresne-Dube L, Picheral B, Guerrier P (1983) An ultrastructural analysis of Dentalium vulgare (Mollusca, Scaphopoda) gametes. J Ultrastruct Res 83:242–257

    Google Scholar 

  • Eckelbarger KJ, Bieler R, Mikkelsen PM (1990) Ultrastructure of sperm development and mature sperm in three species of commensal bivalves (Mollusca: Galeommatoidea). J Morp 205: 63–75

    Google Scholar 

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

    Google Scholar 

  • Franzén Å (1955b) On the spermiogenesis in solenogastres. Zool Bidr Upps 30:485–491

    Google Scholar 

  • Franzén Å (1983) Ultrastructural studies of spermatozoa in three bivalve species with notes on the evolution of elongated sperm nucleus in primitive spermatozoa. Gamete Res. 7:199–214

    Google Scholar 

  • Giusti F (1971) L'ultrastruttura dello spermatozoo nella filogenesi e nella sistematica dei mollusci gasteropodi. Atti Soc ital Sci nat 112:381–402

    Google Scholar 

  • Gonor JJ (1975) Monoplacophora. In: Pearse J (ed) Reproduction in marine invertebrates. Academic Press, New York and London, pp 87–93

    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 

  • Haszprunar G (1992) Preliminary anatomical data on a new neopilinid (Monoplacophora) from Antarctic waters. In: Giusti F, Manganelli G (eds) Abstracts of the Eleventh International Malacological Congress. University of Siena, Siena, pp 307–308

    Google Scholar 

  • Haszprunar G (1993) Anatomische Untersuchungen an Micropilina arntzi Warén & Hain, 1992 (Mollusca, Monoplacophora) aus der Weddell See (Antarctis). Verh dt Zool Ges 86.1: p. 137

    Google Scholar 

  • Haszprunar G, Schaefer K (1995 a) Monoplacophora. In: Harrison FW, Kohn AJ (eds) Microscopic anatomy of invertebrates. Vol. 6. Mollusca. II, John Wiley & Sons, New York (in press)

    Google Scholar 

  • Haszprunar G, Schaefer K (1995 b) Anatomy and affinities of two neopilinid limpets (Mollusca, Monoplacophora) from the Antarctic. Acta zool Stockh (in press)

  • Healy JM (1982) An ultrastructural examination of developing and mature euspermatozoa in Pyrazus ebeninus (Mollusca, Gastropoda, Potamididae). Zoomorphology 100:157–175

    Google Scholar 

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

    Google Scholar 

  • Healy JM (1989 a) Spermiogenesis and spermatozoa in the relict bivalve genus Neotrigonia: relevance to trigonioid relationships, particularly Unionoidea. Mar Biol 103:75–85

    Google Scholar 

  • Healy JM (1989b) Ultrastructure and spermiogenesis in the gastropod Calliotropis glyptus Watson (Prosobranchia: Trochidae), with special reference to the embedded acrosome. Gamete Res 24:9–20

    Google Scholar 

  • Healy JM (1990) Sperm structure in the scissurellid gastropod Sinezona sp. (Prosobranchia, Pleurotomarioidea). Zoologica Scr 19:189–193

    Google Scholar 

  • Healy JM (1993a) Comparative sperm ultrastructure and spermiogenesis in basal heterobranch gastropods (Valvatoidea, Architectonicoidea, Rissoelloidea, Omalogyroidea, Pyramidelloidea) (Mollusca). Zoologica Scr 22:263–276

    Google Scholar 

  • Healy JM (1993b) Sperm and spermiogenesis in Opisthoteuthis persephone (Octopoda: Cirrata): ultrastructure, comparison with other cephalopods and evolutionary significance. J mollusc Stud 59:105–115

    Google Scholar 

  • Healy JM (1995) Molluscan sperm ultrastructure: correlation with taxonomic units within the Gastropoda, Cephalopoda and Bivalvia. J mollusc Stud (in press)

  • Healy JM, Harasewych MG (1992) Spermatogenesis in Perotrochus quoyanus (Fischer & Bernardi) (Gastropoda: Pleurotomariidae). Nautilus 106:1–14

    Google Scholar 

  • Healy JM, Willan RC (1984) Ultrastructural and phylogenetic significance of notaspidean spermatozoa (Mollusca, Gastropoda, Opisthobranchia). Zoologica Scr. 13:107–120

    Google Scholar 

  • Healy JM, Willan RC (1991) Nudibranch spermatozoa: comparative ultrastructure and systematic importance. Veliger 34:134–165

    Google Scholar 

  • Hodgson AN, Baxter JM, Sturrock MG, Bernard RTF (1988) Comparative spermatology of 11 species of Polyplacophora (Mollusca) from the suborders Lepidopleurina, Chitonina and Acanthochitonina. Proc R Soc (Ser B) 235:161–177

    Google Scholar 

  • Hodgson AN, Bernard RTF (1988) A comparison of the structure of the spermatozoa and spermatogenesis of 16 species of patellid limpet (Mollusca: Gastropoda: Archaeogastropoda). J Morph 195:205–223

    Google Scholar 

  • Hodgson AN, Bernard RTF, Van Der Horst G (1990) Comparative spermatology of three species of Donax (Bivalvia) from South Africa. J mollusc Stud 56:257–265

    Google Scholar 

  • Hodgson AN, Foster GG (1992) Structure of the sperm of some South African archaeogastropods (Mollusca) from the superfamilies Haliotoidea, Fissurelloidea and Trochoidea. Mar Biol 113:89–97

    Google Scholar 

  • Hou ST, Maxwell WL (1991) Ultrastructural studies of spermatogenesis in Antalis entalis (Scaphopoda, Mollusca). Phil Trans R Soc (Ser B) 333:101–110

    Google Scholar 

  • Jamieson BGM (1987) A biological classification of sperm types, with special reference to annelids and molluscs, and an example of spermiocladistics. In. Mohri H (ed) New horizons of sperm cell research. Japan Scientific Societies Press, Tokyo, Gordon & Breach Science Publications, New York, pp 311–332

    Google Scholar 

  • Jamieson BGM (1991) Fish evolution and systematics: evidence from spermatozoa. Cambridge University Press, Cambridge, England

    Google Scholar 

  • Jamieson BGM, Hodgson AN, Bernard RTF (1991) Phylogenetic trends and variation in the ultrastructure of the spermatozoa of sympatric species of South African patellid limpets (Archaeogastropoda, Mollusca). Invert Reprod Dev 20:137–146

    Google Scholar 

  • Klepal W (1993) Spermatogenesis and spermatozoa of Aspidosiphon muelleri (Sipunculida) An ultrastructural study. J submicrosc Cytol Path, 25:203–212

    Google Scholar 

  • Knight JB, Yochelson EL (1960) Monoplacophora. In: Moore RC (ed) Treatise on invertebrate paleontology. Part I. Mollusca. 1. Geological Society of America and University of Kansas Press, Lawrence, pp 177–183

    Google Scholar 

  • Kohnert R, Storch V (1983) Ultrastrukturelle Untersuchungen zur Morphologie und Genese der Spermien der 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 

  • Kotrla MB (1989) Evidence suggestive of ameiotic spermatogenesis in unionoid bivalves. Am Zool 29:p. 148A (Abstract)

  • Lemche H (1957) A new living deep-sea mollusk from the Cambro-Devonian class Monoplacophora. Nature, Lond 179:413–416

    Google Scholar 

  • Lemche H, Wingstrand K (1959) The anatomy of Neopilina galatheae Lemche, 1957 (Mollusca, Tryblidiacea). Galathea Rep 3:9–72

    Google Scholar 

  • Longo FJ, Anderson E (1969) Spermiogenesis in the surf clam Spisula solidissima with special reference to the formation of the acrosomal vesicle. J Ultrastruct Res 27:435–443

    Google Scholar 

  • Longo FJ, Dornfeld EG (1967) The fine structure of spermatid differentiation in the mussel, Mytilus edulis. J Ultrastruct Res 20:462–480

    Google Scholar 

  • Marshall BA (1990) Micropilina tangaroa, a new monoplacophoran (Mollusca) from northern New Zealand. Nautilus 104:105–107

    Google Scholar 

  • McLean JH (1979) A new monoplacophoran limpet from the continental shelf off southern California. Contr Sci 307:1–19

    Google Scholar 

  • Menzies RJ (1968) New species of Neopilina of the Cambro-Devonian class Monoplacophora from the Milne-Edwards Deep of the Peru-Chile Trench, R/V Anton Bruun. Proc Symp Mollusca (Mar Biol Ass India) 1:1–9

    Google Scholar 

  • Popham JD (1974) Comparative morphometrics of the acrosomes of the sperms of “externally” and “internally” fertilizing sperms of the shipworms (Teredinidae, Bivalvia, Mollusca). Cell Tissue Res 150:291–297

    Google Scholar 

  • Popham JD (1979) Comparative spermatozoon morphology and bivalve phylogeny. Malacol Rev 12:1–20

    Google Scholar 

  • Popham JD, Marshall B (1977) The fine structure of the spermatozoon of the protobranch bivalve, Nucula hartvigiana Pfeiffer. Veliger 19:431–433

    Google Scholar 

  • Rocha E, Azevedo C (1990) Ultrastructural study of the spermatogenesis of Anodonta cygnea L. (Bivalvia, Unionidae). Invert Reprod Dev 18:169–176

    Google Scholar 

  • Rokop FJ (1972) A new species of monoplacophoran from the abyssal North Pacific. Veliger 15:91–95

    Google Scholar 

  • Rouse GW, Jamieson BGM (1987) An ultrastructural study of the spermatozoa of the polychaetes Eurythoe complanata (Amphinomidae), Clymenella sp. and Micromaldane sp. (Maldanidae), with a definition of sperm types in relation to reproductive biology. J submicrosc Cytol 19:573–584

    Google Scholar 

  • Salvini-Plawen L v (1981) On the origin and evolution of the Mollusca. Atti Conv Lincei (Accad naz Lincei) 49:235–293

    Google Scholar 

  • Salvini-Plawen L v (1985) Early evolution and the primitive groups. In: Trueman E, Clarke MR (eds) The Mollusca. Vol. 10. Evolution. Academic Press, London and New York, pp 59–150

    Google Scholar 

  • Scheltema AH, Tscherkassky M, Kuririan AM (1994) Aplacophora. In: Harrison FW and Kohn AJ (eds) Microscopic anatomy of invertebrates. Vol. 5. Mollusca I. John Wiley & Sons, New York, 13–54

    Google Scholar 

  • Sousa M, Corral L, Azevedo C (1989) Ultrastructural and cytochemical study of spermatogenesis in Scrobicularia plana (Mollusca, Bivalvia). Gamete Res 24:393–401

    Google Scholar 

  • Takaichi T (1979) Spermiogenesis in the pulmonate snail Euhadra hickonis. IV. Effect of X-rays on the spermiogenesis. Dev Growth Differentiation 21:87–98

    Google Scholar 

  • Tscherkassky M (1993) Zur Ultrastruktur der Caudofoveata (Mollusca, Aculifera) unter spezieller Berücksichtigung des Gonopericards und des Pallialraumes. Dissertation. Doctorat Universität Wien

  • Warén A (1988) Neopilina goesi, a new Caribbean monoplacophoran dredged in 1869. Proc biol Soc Wash 101:676–681

    Google Scholar 

  • Warén A, Bouchet P (1990) Laevipilina rolani, a new monoplacophoran from off southwestern Europe. J mollusc Stud 56:449–453

    Google Scholar 

  • Warén A, Hain S (1992) Laevipilina antarctica and Micropilina arntzi, two new monoplacophorans from the Antarctic. Veliger 35:165–176

    Google Scholar 

  • Wingstrand KG (1985) On the anatomy and relationships of recent Monoplacophora. Galathea Rep 16:1–94

    Google Scholar 

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Communicated by G. F. Humphrey, Sydney

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Healy, J.M., Schaefer, K. & Haszprunar, G. Spermatozoa and spermatogenesis in a monoplacophoran mollusc, Laevipilina antarctica: ultrastructure and comparison with other Mollusca. Marine Biology 122, 53–65 (1995). https://doi.org/10.1007/BF00349277

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