Skip to main content
Log in

Development of the pericalymma larva of Solemya reidi (Bivalvia: Cryptodonta: Solemyidae) as revealed by light and electron microscopy

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Solemya reidi Bernard 1980 is a gutless protobranch bivalve known to possess intracellular chemoautotrophic bacterial symbionts in its gill. A light and electron microscope study on the embryology and larval development of S. reidi provides data for the bivalve Subclass Cryptodonta. S. reidi spontaneously spawned large eggs (271 μm in diameter), which developed within individual gelatious egg capsules. The first several cleavages were equal and a distinct molluscan cross was formed at the animal pole of the embryo, features previously unreported in bivalve development. Lecithotrophic pericalymma larvae (similar to the larvae of paleotaxodont protobranch bivalves and aplacophoran molluscs) hatched at 18 to 24 h and remained in the water column for a further 5 d at 10°C. At hatching, larvae measured from 360 to 440 μm in length and from 225 to 265 μm in cross-sectional diameter. Definitive adult structures developed within an epithelial locomotory test entirely covered with compound cilia. The test histolysed at metamorphosis and was ingested throught the mouth into the perivisceral cavity. Length and height of the shell following metamorphosis was 433 μm (±42 μm, n=16) and 282 μm (± 29 μm, n=13), respectively. Primary data and data from the literature show that the type of larval development in both paleotaxodont and cryptodont bivalves cannot be reliably estimated from egg or prodissoconch sizes.

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

  • Allen, J. A.: The development of Pandora inaequivalvis (Linne). J. Embryol. exp. Morph. 9, 252–268 (1961)

    PubMed  Google Scholar 

  • Allen, J. A. and H. L. Sanders: Studies on deep-sea Protobranchia (Bivalvia); the families Siliculidae and Lametilidae. Bull. Mus. comp. Zool. Harv. 145, 263–309 (1973)

    Google Scholar 

  • Allen, J. A. and H. L. Sanders: Studies on the deep-sea Protobranchia; the subfamily Spinulinae (Family Nuculanidae). Bull. Mus. comp. Zool. Harv. 150, 1–30 (1982)

    Google Scholar 

  • Bayne, B. L.: The biology of mussel larvae, pp 81–120. In: Marine mussels: their ecology and physiology, pp 81–120. Ed. by B. L. Bayne. Cambridge: Cambridge Univ. Press 1976

    Google Scholar 

  • Bernard, F. R.: A new Solemya s. str. from the northeastern Pacific (Bivalvia: Cryptodonta). Venus, Kyoto 39, 17–23 (1980)

    Google Scholar 

  • Bickell, L. R. and S. C. Kempf: Larval and metamorphic morphogenesis in the nudibranch Melibe leonina (Mollusca: Opisthobranchia). Biol. Bull. mar. biol. Lab., Woods Hole 165, 119–138 (1983)

    Google Scholar 

  • Bonar, D. B. and M. G. Hadfield: Metamorphosis of the marine gastropod Phestilla sibogae Bergh (Nudibrachia: Aeolidacea). I. Light and electron microscopic analysis of larval and metamorphic stages. J. exp. mar. Biol. Ecol. 16, 227–255 (1974)

    Article  Google Scholar 

  • Cavanaugh, C. M.: Symbiosis of chemoautotrophic bacteria and marine invertebrates. Biol. Bull. mar. biol. Lab., Woods Hole 159, 457 (1980)

    Google Scholar 

  • Cavanaugh, C. M.: Symbiotic chemoautotrophic bacteria in marine invertebrates from sulfide-rich habitats. Nature, Lond. 302, 58–61 (1983)

    Google Scholar 

  • Cavanaugh, C. M., S. L. Gardiner, M. L. Jones, H. W. Jannasch and J. B. Waterbury: Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila: possible chemoautotrophic symbionts. Science, N. Y. 213, 340–342 (1981)

    Google Scholar 

  • Chia, Fu-Shiang, J. Buckland-Nicks and C. M. Young: Locomotion of marine invertebrate larvae: a review. Can. J. Zool. 62, 1205–1222 (1984)

    Google Scholar 

  • Cole, H. A.: The fate of larval organs in the metamorphosis of Ostrea edulis. J. mar. biol. Ass. U.K. 2, 469–484 (1938)

    Google Scholar 

  • Davis, J. P. and J. G. Wilson: The population structure and ecology of Nucula turgida (Leckenby and Marshall) in Dublin Bay. Prog. Underwat. Sci. 8, 53–60 (1983)

    Google Scholar 

  • Dietrich, H. F. and A. R. Fontaine: A decalcification method for ultrastructure of echinoderm tissues. Stain Technol. 50, 351–353 (1975)

    PubMed  Google Scholar 

  • Drew, G. A.: Notes on the embryology, anatomy, and habits of Yoldia limatula, Say. Johns Hopkins Univ. Circ. 17, 11–14 (1897)

    Google Scholar 

  • Drew, G. A.: The anatomy, habits, and embryology of Yoldia limatula, Say. Mem. biol. Lab. Johns Hopkins Univ. 4, 1–37 (1899a)

    Google Scholar 

  • Drew, G. A.: Some observations on the habits, anatomy and embryology of members of the Protobranchia. Anat. Anz. 15, 493–519 (1899b)

    Google Scholar 

  • Drew, G. A.: The life history of Nucula delphinodonta (Mighels). Q. J. microsc. Sci. 44, 313–391 (1901)

    Google Scholar 

  • Felbeck, H.: Sulfide oxidation and carbon fixation by the gutless clam Solemya reidi: an animal-bacteria symbiosis. J. comp. Physiol. B 152, 3–11 (1983)

    Google Scholar 

  • Felbeck, H., J. J. Childress and G. N. Somero: Calvin-Benson cycle and sulphide oxidation enzymes in animals from sulphide-rich habitats. Nature, Lond. 293, 291–293 (1981)

    Google Scholar 

  • Felbeck, H., J. J. Childress and G. N. Somero: Biochemical interactions between molluscs and their algal and bacterial symbionts. In: The mollusca, vol. 2, Environmental biochemistry and physiology, pp 331–358. Ed. by P. W. Hochachka. New York: Academic Press 1983

    Google Scholar 

  • Fisher, C. R. and J. J. Childress: Carbon fixation and translocation in Solemya reidi (Bivalvia: Protobranchia). Am. Zool. 24, 57A (1984)

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

    Google Scholar 

  • Fretter, V.: Metamorphic changes in the velar musculature, head and shell of some prosobranch veligers. J. mar. biol. Ass. U. K. 52, 161–177 (1972)

    Google Scholar 

  • Hadfield, H. G.: Aplacophora. In: Reproduction of marine invertebrates, vol. V., Pelecypods and lower classes, pp 1–25. Ed. by A. C. Giese and J. S. Pearse. New York: Academic Press 1979

    Google Scholar 

  • Hand, S. C. and G. N. Somero: Energy metabolism pathways of hydrothermal vent animals: adaptations to a food-rich and sulfide-rich deep-sea environment. Biol. Bull. mar. biol. Lab., Woods Hole 165, 167–181 (1983)

    Google Scholar 

  • Heath, H.: Solenogastres from the eastern coast of North America. Mem. Mus. comp. Zool. Harv. 45, 185–263 (1918)

    Google Scholar 

  • Jablonski, D. and R. A. Lutz. Molluscan larval shell morphology: ecological and paleontological applications. In: Skeletal growth of aquatic organisms, pp 323–377. Ed. by D. C. Rhoads and R. A. Lutz. New York: Plenum Publ. Corp. 1980

    Google Scholar 

  • Jablonski, D. and R. A. Lutz: Larval ecology of marine benthic invertebrates: paleobiological implications. Biol. Rev. 58, 21–89 (1983)

    Google Scholar 

  • Jørgensen, C. B.: Lamellibranchia: In: Reproduction and larval development of Danish bottom invertebrates. Meddr Kommn Havunders. Serie Plankton 4, 277–311 (1946)

  • Korschelt, E. and K. Heider: Text-book of the embryology of invertebrates, vol. IV. London: Swan Sonnenschein 1900

    Google Scholar 

  • Knudsen, J.: The deep-sea bivalvia. Scient. Rep. John Murray Exped 11 (3), 237–343 (1967)

    Google Scholar 

  • Kuznetsov, A. P. and A. A. Shileiko: Gutless Protobranchia (Bivalvia). Biol. Nauki (Moscow) 0 (2), 39–49 (1984)

  • LaBarbera, M.: Larval and post-larval development of five species of Miocene bivalves (Mollusca). J. Paleont. 48, 265–277 (1974)

    Google Scholar 

  • Lebour, M. V.: Notes on the breeding of some lamellibranchs from Plymouth, and their larvae. J. mar. biol. Ass. U. K. 23, 119–144 (1938)

    Google Scholar 

  • Lightfoot, R. H., P. A. Tyler and J. D. Gage: Seasonal reproduction in deep-sea bivalves and brittlestars. Deep Sea Res. 26A, 967–973 (1979)

    Article  Google Scholar 

  • Loosanoff, V. L. and H. C. Davis: Rearing of bivalve mollusks. Adv. mar. Biol. 1, 1–136 (1963)

    Google Scholar 

  • Lutz, R. A., R. Mann, J. G. Goodsell and M. Castagna: Larval and early post-larval development of Arctica islandica. J. mar. biol. Ass. U. K. 62, 745–769 (1982)

    Google Scholar 

  • McMahon, R. F. and R. G. B. Reid: Respiratory responses of the gutless bivalve, Solemya reidi, to temperature, hypoxia, H-S, and dissolved organic matter. Am. Zool. 24, 136A (1984)

  • Moore, D. R.: Small species of Nuculidae (Bivalvia) from the tropical western Atlantic. Nautilus 91, 119–128 (1977)

    Google Scholar 

  • Morse, E. S.: Observations on living Solenomya. Biol. Bull. mar. biol. Lab., Woods Hole 25, 261–281 (1913)

    Google Scholar 

  • Mortimer, J. E.: A comparative study of post-larval feeding mechanisms in the Bivalvia. Ph. D. thesis, Univ. of Glasgow 1962

  • Morton, B.: The hypobranchial gland in the Bivalvia. Can. J. Zool. 55, 1225–1234 (1977)

    Google Scholar 

  • Newell, N. D.: Classification of the Bivalvia, pp 205–218, Treatise on invertebrate paleontology, Part N, 1 (Moll. 6) 1969

  • Ockelmann, K. W.: The zoology of East Greenland Lamellibranchiata. Meddr Gronland 122 (6), 1–256 (1958)

    Google Scholar 

  • Ockelmann, K. W.: Developmental types in marine bivalves and their distribution along the Atlantic coast of Europe. In: Proc. First Eur. Malac. Congress (1962), pp 25–35. Ed. by L. R. Cox and J. F. Peake. London: Conchological Society of Great Britian and Ireland and the Malacological Society of London 1965

    Google Scholar 

  • Oldfield, E.: Observations on the anatomy and mode of life of Lasaea rubra (Montagu) and Turtonia minuta (Fabricius). Proc. malac. Soc. Lond. 31, 226–249 (1955)

    Google Scholar 

  • Oldfield, E.: The reproduction and development of some members of the Erycinidae and Montacutidae (Mollusca, Eulamellibranchia), Proc. malacol. Soc. Lond. 36, 79–120 (1964)

    Google Scholar 

  • Pearse, J. S.: Polyplacophora. In: Reproduction of marine invertebrates, vol. V., Pelecypods and lower classes, pp 27–85. Ed. by A. C. Giese and J. S. Pearse. New York: Academic Press 1979

    Google Scholar 

  • Pelseneer, P.: Contribution à l'étude des Lamellibranches. Archs Biol., Paris 11, 147–312 (1891)

    Google Scholar 

  • Powell, M. A. and G. N. Somero: Sulfide oxidation occurs in the animal tissue of the gutless clam, Solemya reidi. Biol. Bull. mar. biol. Lab., Woods Hole 169, 164–181 (1985)

    Google Scholar 

  • Pruvot, G.: Sur le développement d'un solenogastre. C. r. hebd. Seanc. Acad. Sci., Paris 111, 689–692 (1890)

    Google Scholar 

  • Pruvot, G.: Sur l'embryogénie d'une Proneomenia. C. r. hebd. Seanc. Acad. Sci., Paris 114, 1211–1214 (1892)

    Google Scholar 

  • Rachor, E.: Structure, dynamics and productivity of a population of Nucula nitidosa (Bivalvia: Protobranchia). Ber. dt. wiss. Kommn Meeresforsch 24, 296–331 (1976)

    Google Scholar 

  • Raven, C. P.: Morphogenesis. The analysis of molluscan development, 365 pp. Oxford: Pergamon Press 1966

    Google Scholar 

  • Reid, R. G. B.: Aspects of the biology of a gutless species of Solemya (Bivalvia: Protobranchia). Can. J. Zool. 58, 386–393 (1980)

    Google Scholar 

  • Reid, R. G. B. and F. R. Bernard: Gutless bivalves. Science, N.Y. 208, 609–610 (1980)

    Google Scholar 

  • Rice, M. E.: Morphological and behavioral changes at metamorphosis in the Sipuncula. In: Settlement and metamorphosis of marine invertebrate larvae, pp 83–102. Ed. by F. S. Chia and M. E. Rice. Amsterdam: Elsevier 1978

    Google Scholar 

  • Richardson, K. C., L. Jarrett and E. H. Finke: Embedding in epoxy resins for ultrathin sectioning in electron microscopy. Stain Technol. 35, 313–323 (1960)

    PubMed  Google Scholar 

  • Rokop, F. J.: Year-round reproduction in the deep-sea bivalve molluscs. In: Reproductive ecology of marine invertebrates, pp 189–198. Ed. by S. E. Stancyk. Columbia, S. Carolina: Univ. S. Carolina Press 1979

    Google Scholar 

  • Runnegar, B. and C. Bentley: Anatomy. ecology and affinities of the Australian Early Cambrian bivalve Pojetaia runnegariJell. J. Paleont. 57, 73–92 (1983)

    Google Scholar 

  • Saleuddin, A. S. M.: The gonads and reproductive cycle of Astarte sulcata (Da Costa) and sexuality in A. elliptica (Brown). Proc. malac. Soc. Lond. 36, 141–148 (1964)

    Google Scholar 

  • Salvini-Plawen, L. v.: Zur Morphologie und Phylogenie der Mollusken. Die Bezeichnungen der Caudofoveata und der Solenogastre als Aculifera, als Mollusca und als Spiralia. Z. wiss. Zool. 184, 205–394 (1972)

    Google Scholar 

  • Salvini-Plawen, L. v.: Zur Klärung des “Trochophora”-Begriffes. Experientia 29, 1434–1436 (1973)

    Google Scholar 

  • Salvini-Plawen, L. v.: Was ist eine Trochophora? Eine Analyse der Larventypen mariner Prostomier. Zool. Jb. Anat. Ont. Tierre 103, 389–423 (1980)

    Google Scholar 

  • Sanders, H. L. and J. A. Allen: Studies on deep-sea Protobranchia (Bivalvia); prologue and the Pristiglomidae. Bull. Mus. comp. Zool. Harv. 145, 237–262 (1973)

    Google Scholar 

  • Sanders, H. L. and J. A. Allen: Studies on the deep-sea Protobranchia (Bivalvia); the family Tindariidae and the genus Pseudotindaria. Bull. Mus. comp. Zool. Harv. 148, 23–59 (1977)

    Google Scholar 

  • Sastry, A. N.: Pelecypoda (excluding Ostreidae). In: Reproduction of marine invertebrates, vol. V. Pelecypods and lower classes, pp 113–292. Ed. by A. C. Giese and J. S. Pearse. New York: Academic Press 1979

    Google Scholar 

  • Scheltema, R. S.: Reproduction and dispersal of bottom dwelling deep-sea invertebrates: a speculative summary. In: Barobiology and the experimental biology of the deep-sea, pp 58–66. Ed. by R. W. Brauer. Chapel Hill: Univ. N. Carolina Press 1972

    Google Scholar 

  • Sigerfoos, C. P.: Natural history, organization and late development of the Teredinidae, or shipworms. Bull. Bur. Fish., Wash. 27, 191–231 (1907)

    Google Scholar 

  • Sullivan, C. M.: Bivalve larvae of Malpeque Bay, P. E. I. Bull. Fish. Res. Bd Can. 77, 1–36 (1948)

    Google Scholar 

  • Switzer-Dunlap, M. and M. G. Hadfield: Observations on development, larval growth and metamorphosis of four species of Aplysiidae (Gastropoda: Opisthobranchia) in laboratory culture. J. exp. mar. Biol. Ecol. 29, 245–261 (1977)

    Article  Google Scholar 

  • Thompson, T. E.: Development of the aplacophorous mollusc Neomenia carinata Tullberg. Nature, Lond. 184, 122–123 (1959)

    Google Scholar 

  • Thompson, T. E.: The development of Neomenia carinata Tullberg (Mollusca Aplacophora). Proc. R. Soc. B 153, 263–278 (1960)

    Google Scholar 

  • Thorson, G.: The larval development, growth, and metabolism of Arctic marine bottom invertebrates, compared with those of other seas. Meddr Gronland 100 (6), 1–155 (1936)

    Google Scholar 

  • Trevallion, C.: A study of detritus-feeding bivalve molluscs, and an investigation on detritus, 211 pp. Ph. D. Thesis, Univ. Southampton 1965

  • Verdonk, N. H. and J. A. M. van den Biggelaar: Early development and the formation of the germ layers. In: The mollusca, vol. 3, Development, pp 91–121. Ed. by N. H. Verdonk, J. A. M. van den Biggelaar and A. S. Tompa. New York: Academic Press 1983

    Google Scholar 

  • Wada, S. K.: Amphineura, Gastropoda, Scaphopoda, Pelecypoda. In: Invertebrate embryology (transl. from Japanese by J. C. Dan), pp 485–525. Ed. by M. Kume and K. Dan. Belgrade: NOLIT Publ. House 1968

    Google Scholar 

  • Yonge, C. M.: The status of the Protobranchia in the bivalve Mollusca. Proc. malac. Soc. Lond. 33, 210–214 (1959)

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by J. M. Shick, Orono

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gustafson, R.G., Reid, R.G.B. Development of the pericalymma larva of Solemya reidi (Bivalvia: Cryptodonta: Solemyidae) as revealed by light and electron microscopy. Marine Biology 93, 411–427 (1986). https://doi.org/10.1007/BF00401109

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00401109

Keywords

Navigation