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.
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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
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
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
Atkins, D. (1937c). On the ciliary mechanisms and interrelationships of lamellibranchs. Part IV: Cuticular fusion. Q. J. microsc. Sci. 79: 423–445
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
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
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
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
Barnes, R. D. (1987). Invertebrate Zoology. CBS College Publishing, New York
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
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
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
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
Drew, G. A. (1906). The habits, anatomy, and embryology of the giant scallop (Pecten tenuicostatus, Mighels). Univ. Maine Studies 6: 1–71
Dupouy, H. (1983). La pectiniculture à St.-Pierre et Miquelon. Sci. Pêche 337: 17–29
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
Fenchel, T. (1965). Ciliates from Scandinavian molluscs. Ophelia 2: 71–174
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
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
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
Gabe, M. (1968). Techniques histologiques. Masson et Cie, Paris
Hausman, K. (1978). Parasitische Wimpertiere in Seemuscheln. Mikrokosmos 8: 240–242
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
Janssens, R. T. (1893). Les branchies des acéphales. La cellule 9
Jørgensen, C. B. (1966). The biology of suspension feeding. Pergamon Press, Oxford
Kellogg, J. L. (1892). A contribution to our knowledge of the morphology of the lamellibranchiate mollusks. Bull. U.S. Fish. Commis. 10: 389–434
Kellogg, J. L. (1915). Ciliary mechanisms of lamellibranchs with descriptions of anatomy. J. Morphol. 26: 625–701
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
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
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
Mikulich, L. V., Tsikhon-Lukanina, Ye. A. (1981). Food of the scallop. Oceanology 21: 633–635
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
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
Morton, J. E. (1979). Molluscs. Hutchinson and Company Ltd, London
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
Owen, G. (1974). Studies on the gill of Mytilus edulis: The eulatero-frontal cirri. Proc. R. Soc. London, Ser. B. 187: 83–91
Owen, G. (1987). Classification and the bivalve gill. Phil. Trans. R. Soc. London, Ser. B. 284: 377–385
Owen, G., McCrae, J. M. (1976). Further studies on the laterofrontal tracts of bivalves. Proc. R. Soc. London, Ser. B. 194: 527–544
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
Ridewood, W. G. (1903). On the structure of the gills of the lamellibranchia. Phil. trans. R. Soc. London Ser. B. 195: 147–284
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
Setna, S. B. (1930). Neuromusculature mechanism of the gill of Pecten. Q. J. microsc. Sci. 73: 365–391
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
Southward, E. C. (1986). Gill symbionts in thyasirids and other bivalve molluscs. J. mar. biol. Ass. U.K. 66: 889–914
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
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
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
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Communicated by R. W. Doyle, Halifax
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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
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DOI: https://doi.org/10.1007/BF00392659