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
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
Baccetti B, Afzelius BA (1976) The biology of the sperm cell. Monographs in developmental biology. Vol. 10. S. Karger, Basel
Bieler R, Hadfield MG (1990) Reproductive biology of the sessile gastropod Vermicularia spirata (Cerithioidea: Turritellidae) J mollusc Stud 56:205–219
Buckland-Nicks J, Chia F-S (1989) Spermiogenesis in Chaetoderma sp. (Aplacophora) J exp Zool 252:308–317
Buckland-Nicks J, Chia F-S, Koss R (1990) Spermiogenesis in Polyplacophora, with special reference to acrosome formation (Mollusca). Zoomorphology 109:179–188
Buckland-Nicks JA, Koss R, Chia F-S (1988) The elusive acrosome of chiton sperm. Int J Invert Reprod Dev 13:193–198
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
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
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
Daddow LYM (1986) An abbreviated method of double lead stain technique. J submicrosc Cytol 18:221–224
Dietrich HF, Fontaine AR (1975) A decalcification method for ultrastructure of echinoderm tissue. Stain Technol 50:351–354
Dorange G, Le Pennec M (1989) Ultrastructural characteristics of spermatogenesis in Pecten maximus (Mollusca, Bivalvia). Invert Reprod Develop 15:109–117
Drozdov AL, Reunov AA (1986) Spermatogenesis and the sperm ultrastructure in the mussel Modiolus difficilis. Tsitologiya 28:1069–1074 [In Russ., Engl summary]
Dufresne-Dube L, Picheral B, Guerrier P (1983) An ultrastructural analysis of Dentalium vulgare (Mollusca, Scaphopoda) gametes. J Ultrastruct Res 83:242–257
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
Franzén Å (1955a) Comparative morphological investigations into the spermiogenesis among Mollusca. Zool Bidr Upps 30:399–456
Franzén Å (1955b) On the spermiogenesis in solenogastres. Zool Bidr Upps 30:485–491
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
Giusti F (1971) L'ultrastruttura dello spermatozoo nella filogenesi e nella sistematica dei mollusci gasteropodi. Atti Soc ital Sci nat 112:381–402
Gonor JJ (1975) Monoplacophora. In: Pearse J (ed) Reproduction in marine invertebrates. Academic Press, New York and London, pp 87–93
Haszprunar G (1988) On the origin and evolution of major gastropod groups with special reference to the Streptoneura. J mollusc Stud 54:367–441
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
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
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)
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
Healy JM (1988) Sperm morphology and its systematic importance in the Gastropoda. Malac Rev(Suppl) 4:251–266
Healy JM (1989 a) Spermiogenesis and spermatozoa in the relict bivalve genus Neotrigonia: relevance to trigonioid relationships, particularly Unionoidea. Mar Biol 103:75–85
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
Healy JM (1990) Sperm structure in the scissurellid gastropod Sinezona sp. (Prosobranchia, Pleurotomarioidea). Zoologica Scr 19:189–193
Healy JM (1993a) Comparative sperm ultrastructure and spermiogenesis in basal heterobranch gastropods (Valvatoidea, Architectonicoidea, Rissoelloidea, Omalogyroidea, Pyramidelloidea) (Mollusca). Zoologica Scr 22:263–276
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
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
Healy JM, Willan RC (1984) Ultrastructural and phylogenetic significance of notaspidean spermatozoa (Mollusca, Gastropoda, Opisthobranchia). Zoologica Scr. 13:107–120
Healy JM, Willan RC (1991) Nudibranch spermatozoa: comparative ultrastructure and systematic importance. Veliger 34:134–165
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
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
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
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
Hou ST, Maxwell WL (1991) Ultrastructural studies of spermatogenesis in Antalis entalis (Scaphopoda, Mollusca). Phil Trans R Soc (Ser B) 333:101–110
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
Jamieson BGM (1991) Fish evolution and systematics: evidence from spermatozoa. Cambridge University Press, Cambridge, England
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
Klepal W (1993) Spermatogenesis and spermatozoa of Aspidosiphon muelleri (Sipunculida) An ultrastructural study. J submicrosc Cytol Path, 25:203–212
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
Kohnert R, Storch V (1983) Ultrastrukturelle Untersuchungen zur Morphologie und Genese der Spermien der Archaeogastropoda. Helgoländer Meeresunters 36:77–84
Kohnert R, Storch V (1984a) Vergleichend-ultrastrukturelle Untersuchungen zur Morphologie eupyrener Spermien der Monotocardia (Prosobranchia). Zool Jb 111:51–93
Kohnert R, Storch V (1984b) Elektronenmikroskopische Untersuchungen zur Spermiogenese der eupyrenen Spermien der Monotocardia (Prosobranchia). Zool Jb 112:1–32
Koike K (1985) Comparative ultrastructural studies on the spermatozoa of the Prosobranchia (Mollusca: Gastropoda). Sci Rep Fac Educ, Gunma Univ 34:33–153
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
Lemche H, Wingstrand K (1959) The anatomy of Neopilina galatheae Lemche, 1957 (Mollusca, Tryblidiacea). Galathea Rep 3:9–72
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
Longo FJ, Dornfeld EG (1967) The fine structure of spermatid differentiation in the mussel, Mytilus edulis. J Ultrastruct Res 20:462–480
Marshall BA (1990) Micropilina tangaroa, a new monoplacophoran (Mollusca) from northern New Zealand. Nautilus 104:105–107
McLean JH (1979) A new monoplacophoran limpet from the continental shelf off southern California. Contr Sci 307:1–19
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
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
Popham JD (1979) Comparative spermatozoon morphology and bivalve phylogeny. Malacol Rev 12:1–20
Popham JD, Marshall B (1977) The fine structure of the spermatozoon of the protobranch bivalve, Nucula hartvigiana Pfeiffer. Veliger 19:431–433
Rocha E, Azevedo C (1990) Ultrastructural study of the spermatogenesis of Anodonta cygnea L. (Bivalvia, Unionidae). Invert Reprod Dev 18:169–176
Rokop FJ (1972) A new species of monoplacophoran from the abyssal North Pacific. Veliger 15:91–95
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
Salvini-Plawen L v (1981) On the origin and evolution of the Mollusca. Atti Conv Lincei (Accad naz Lincei) 49:235–293
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
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
Sousa M, Corral L, Azevedo C (1989) Ultrastructural and cytochemical study of spermatogenesis in Scrobicularia plana (Mollusca, Bivalvia). Gamete Res 24:393–401
Takaichi T (1979) Spermiogenesis in the pulmonate snail Euhadra hickonis. IV. Effect of X-rays on the spermiogenesis. Dev Growth Differentiation 21:87–98
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
Warén A, Bouchet P (1990) Laevipilina rolani, a new monoplacophoran from off southwestern Europe. J mollusc Stud 56:449–453
Warén A, Hain S (1992) Laevipilina antarctica and Micropilina arntzi, two new monoplacophorans from the Antarctic. Veliger 35:165–176
Wingstrand KG (1985) On the anatomy and relationships of recent Monoplacophora. Galathea Rep 16:1–94
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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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DOI: https://doi.org/10.1007/BF00349277