Skip to main content

Advertisement

Log in

New observations of the gills of Placopecten magellanicus (Mollusca: Bivalvia), and implications for nutrition

I. General anatomy and surface microanatomy

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

The organization, general anatomy, and surface microanatomy of all regions of the gills of a representive bivalve mollusc, Placopecten magellanicus Gmelin, were studied using stereo-microscopic, histological, and scanning electron microscopic techniques. Individuals were collected in May and November 1985 from Chamcook Bay, New Brunswick, Canada. In addition to correcting earlier accounts of this structure, a number of new observations are reported. The orientation of the ciliated spurs appears to be responsible for the sinusoidal arrangement of the gill filaments. Micrographs showing the structure of the dorsal respiratory expansion are presented. The entire abfrontal surface of the principal filament, including the dorsal respiratory expansion, is densely ciliated and mucosecretory. These characteristics may aid in the establishment of a respiratory current and in the prevention of gill damage during escape responses. All nonciliated regions of the gill filaments are covered with microvilli, thus greatly increasing the surface area of the gill. The feeding mechanism is discussed in relation to the dorsal and ventral ciliated tracts. Symbiotic ciliate protozoans are constantly dislodged from the gill filaments and transported via the ventral mucus string to the buccal region. The nutritional implications of these observations are discussed.

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

  • Atkins, D. (1936). On the ciliary mechanisms and interrelationships of lamellibranchs. Part I: New observations on sorting mechanisms. Q. J. microsc. Sci. 79: 181–308

    Google Scholar 

  • Atkins, D. (1937a): On the ciliary mechanisms and interrelationships of lamellibranchs. Part II: Sorting devices on the gills. Q. J. microsc. Sci. 79: 339–373

    Google Scholar 

  • Atkins, D. (1937b). On the ciliary mechanisms and interrelationships of lamellibranchs. Part III: Types of lamellibranch gills and their food currents. Q. J. microsc. Sci. 79: 375–421

    Google Scholar 

  • Atkins, D. (1937c). On the ciliary mechanisms and interrelationships of lamellibranchs. Part IV: Cuticular fusion. Q. J. microsc. Sci. 79: 423–445

    Google Scholar 

  • Atkins, D. (1938a). On the ciliary mechanisms and interrelationships of lamellibranchs. Part V. Note on gills of Amussium pleuronectes L. Q. J. microsc. Sci. 80: 321–329

    Google Scholar 

  • Atkins, D. (1938b). On the ciliary mechanisms and interrelationships of lamellibranchs. Part VI. Patterns of the lateral ciliated cells of gill filaments. Q. J. microsc. Sci. 80: 331–344

    Google Scholar 

  • Atkins, D. (1938c). On the ciliary mechanisms and interrlationships of lamellibranchs. Part VII: Latero-frontal cilia of the gill filaments and their phylogenic value. Q. J. microsc. Sci. 80: 345–436

    Google Scholar 

  • Atkins, D. (1943). On the ciliary mechanisms and interrelationships of lamellibranchs. Part VIII. Notes on gill musculature in the Microciliobranchia. Q. J. microsc. Sci. 84: 187–256

    Google Scholar 

  • Barnes, R. D. (1987). Invertebrate Zoology. CBS College Publishing, New York

    Google Scholar 

  • Baur, P. S., Brinkley, B. R., Bowman, B. H. (1976). Effects of cystic fibrosis serum ciliary inhibitor on oyster gill ultrastructure: analysis by scanning and transmission electron microscopy. Tex. Rep. Biol. Med. 34: 155–174

    Google Scholar 

  • Ciocco, N. F. (1985). Biologia y ecologia de Chlamys tehuelchus d'Orbigny en el Golfo san José (Provincia del Chubut, Republica Argentina) Pelecypoda, Pectinidae. Ph. D. thesis, Universidad Nacional de La Plata, Argentina

    Google Scholar 

  • Dando, P. R., Southward, A. J., Southward, E. C., Terwilliger, N. B., Terwilliger, R. C. (1985). Sulphur-oxidizing bacteria and haemoglobin in gills of the bivalve mollusc Myrtea spinifera. Mar. Ecol. Prog. Ser. 23: 85–98

    Google Scholar 

  • Dando, P. R., Southward, A. J., Southward, E. C. (1986). Chemoautotrophic symbionts in the gills of the bivalve mollusc Lucinoma borealis and the sediment chemistry of its habitat. Proc. R. Soc. London, Ser. B. 227: 227–247

    Google Scholar 

  • Drew, G. A. (1906). The habits, anatomy, and embryology of the giant scallop (Pecten tenuicostatus, Mighels). Univ. Maine Studies 6: 1–71

    Google Scholar 

  • Dupouy, H. (1983). La pectiniculture à St.-Pierre et Miquelon. Sci. Pêche 337: 17–29

    Google Scholar 

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

    Google Scholar 

  • Fenchel, T. (1965). Ciliates from Scandinavian molluscs. Ophelia 2: 71–174

    Google Scholar 

  • Fiala-Médioni, A., Métivier, C. (1986). Ultrastructure of the gill of the hydrothermal vent bivalve Calyptogena magnifica with a discussion of its nutrition. Mar. Biol. 90: 215–222

    Google Scholar 

  • Fiala-Médioni, A., Métivier, C., Herry, A., Le Pennec, M. (1986). Ultrastructure of the gill of the hydrothermal-vent mytilid Bathymodiolus sp. Mar. Biol. 92: 65–72

    Google Scholar 

  • Fisher, C. R., Hand, S. C. (1984). Chemoautotrophic symbionts in the bivalve Lucina floridana from seagrass beds. Biol. Bull. mar. biol. Lab., Woods Hole 167: 445–459

    Google Scholar 

  • Gabe, M. (1968). Techniques histologiques. Masson et Cie, Paris

    Google Scholar 

  • Hausman, K. (1978). Parasitische Wimpertiere in Seemuscheln. Mikrokosmos 8: 240–242

    Google Scholar 

  • Henry, M., Vicente, N., Cornet, C. (1981). Analyse ultrastructurale du filament branchiale d'un mollusque bivalve Carastoderma glaucum Poiret 1789. Association particulière avec des microorganismes. Haliotis 11: 101–114

    Google Scholar 

  • Janssens, R. T. (1893). Les branchies des acéphales. La cellule 9

  • Jørgensen, C. B. (1966). The biology of suspension feeding. Pergamon Press, Oxford

    Google Scholar 

  • Kellogg, J. L. (1892). A contribution to our knowledge of the morphology of the lamellibranchiate mollusks. Bull. U.S. Fish. Commis. 10: 389–434

    Google Scholar 

  • Kellogg, J. L. (1915). Ciliary mechanisms of lamellibranchs with descriptions of anatomy. J. Morphol. 26: 625–701

    Google Scholar 

  • Knight, J. H. (1984). Studies on the biology and biochemistry of Pholas dactylus. L. Ph.D. thesis, University of London

  • Knight, J. H., Knight, R. (1986). The blood vascular system of the gills of Pholas dactylus L. (Mollusca, Bivalvia, Eulamellibranchia). Phil. Trans. R. Soc. London, Ser. B 313: 509–523

    Google Scholar 

  • Le Pennec, M., Hily, A. (1984). Anatomie, structure et ultrastructure de la branchie d'un Mytilidae des sites hydrothermaux du Pacifique Oriental. Oceanol. Acta 7: 517–523

    Google Scholar 

  • Le Pennec, M., Beninger, P. G.. Herry, A. (1988). New observations of the gill of Placopecten magellanicus (Mollusca: Bivalvia), and implications for nutrition II. Internal anatomy and microanatomy. Mar. Biol. (In press)

  • Manahan, D. T., Wright, S. H., Stephens, G. C., Rice, M. A. (1982). Transport of dissolved amino acids by the mussel, Mytilus edulis: demonstration of net uptake from natural seawater. Science, N.Y. 215, 1253–1255

    Google Scholar 

  • Mikulich, L. V., Tsikhon-Lukanina, Ye. A. (1981). Food of the scallop. Oceanology 21: 633–635

    Google Scholar 

  • Moore, H. J. (1971). The structure of the latero-frontal cirri on the gills of certain lamellibranch molluscs and their role in suspension feeding. Mar. Biol. 11: 23–27

    Google Scholar 

  • Morse, M. P., Robinson, W. E., Wehling, W. E. (1982). Effects of sublethal concentrations of the drilling mud components attapulgite and Q-broxin on the structure and function of the gill of the scallop, Placopecten magellanicus (Gmelin). In: Vernberg, W. B., Calabrese, A., Thurberg, F. P., Vernberg, F. J. (eds.) Physiological mechanisms of marine pollutant toxicity. Academic Press, New York, p. 235–259

    Google Scholar 

  • Morton, J. E. (1979). Molluscs. Hutchinson and Company Ltd, London

    Google Scholar 

  • Nelson, T. C. (1960). The feeding mechanism of the oyster. II. On the gills and palps of Ostrea edulis, Crassostrea virginica and C. angulata. J. Morph. 107: 163–191

    Google Scholar 

  • Owen, G. (1974). Studies on the gill of Mytilus edulis: The eulatero-frontal cirri. Proc. R. Soc. London, Ser. B. 187: 83–91

    Google Scholar 

  • Owen, G. (1987). Classification and the bivalve gill. Phil. Trans. R. Soc. London, Ser. B. 284: 377–385

    Google Scholar 

  • Owen, G., McCrae, J. M. (1976). Further studies on the laterofrontal tracts of bivalves. Proc. R. Soc. London, Ser. B. 194: 527–544

    Google Scholar 

  • Reed-Miller, C., Greenberg, M. J. (1984). The ciliary junctions of scallop gills: the effects of cytochalasins and concanvalin A. Biol. Bull. mar. biol. Lab., Woods Hole 163: 225–239

    Google Scholar 

  • Ridewood, W. G. (1903). On the structure of the gills of the lamellibranchia. Phil. trans. R. Soc. London Ser. B. 195: 147–284

    Google Scholar 

  • Schweimanns, M., Felbeck, H. (1985). Significance of the occurrence of chemoautotrophic bacterial endosymbionts in lucinid clams from Bermuda. Mar. Ecol. Prog. Ser. 24: 113–120

    Google Scholar 

  • Setna, S. B. (1930). Neuromusculature mechanism of the gill of Pecten. Q. J. microsc. Sci. 73: 365–391

    Google Scholar 

  • Shumway, S. E. (in press). Food resources related to habitat in the scallop, Placopecten megallanicus (Gmelin, 1791): a qualitative study. J. Shellfish Res. 62: 89–95

  • Shumway, S. E., Cucci, T. L., Newell, R. C., Yentsch, C. M. (1985). Particle selection, ingestion, and absorption in filter-feeding bivalves. J. exp. mar. Biol. Ecol. 91: 77–92

    Google Scholar 

  • Southward, E. C. (1986). Gill symbionts in thyasirids and other bivalve molluscs. J. mar. biol. Ass. U.K. 66: 889–914

    Google Scholar 

  • Spiro, B., Greenwood, P. B., Southward, A. J., Dando, P. R. (1986). 13C/12C ratios in marine invertebrates from reducing sediments: confirmation of nutritional importance of chemoautotrophic endosymbiotic bacteria. Mar. Ecol. Prog. Ser. 28: 233–240

    Google Scholar 

  • Uzman, J. R., Stickney, A. P. (1954). Trichodina myicola n. sp., a peritrichous ciliate from the marine bivalve Mya arenaria L. J. Protozool. 1: 149–155

    Google Scholar 

  • Wright, S. H., Southwell, K. M., Stephens, G. C. (1984). Autoradiographic analysis of amino acid uptake by the gill of Mytilus. J. comp. Physiol. 154 (B): 249–256

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by R. W. Doyle, Halifax

Rights and permissions

Reprints and permissions

About this article

Cite this article

Beninger, P.G., Le Pennec, M. & Salaün, M. New observations of the gills of Placopecten magellanicus (Mollusca: Bivalvia), and implications for nutrition. Marine Biology 98, 61–70 (1988). https://doi.org/10.1007/BF00392659

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00392659

Keywords

Navigation