Abstract
Despite the importance of understanding feeding in the early stages of bivalve development, little information is available concerning the organogenesis of the bivalve gill. The present study used histological and scanning electron microscopical techniques to present a detailed account of gill development in the early stages of the scallop Pecten maximus L. (Bivalvia: Pectinidae). Live specimens from larval cultures were observed daily using light microscopy, while five scallops were sampled for electron and light microscopy every 2 to 3 d from Day 18 to 35, then weekly to Day 56, with a final sampling on Day 58. Although development was continuous, four distinct stages were identified (1-primordia, 2-homorhabdic unreflected, 3-homorhabdic reflected, 4-heterorhabdic), partially recapitulating the presumed phylogenetic evolution of this character in the Pectinidae. The absence of a ventral grcove in all stages suggests that the particle transport mechanism of pectinids evolved independently of such a structure, which is found in other bivalve families. Similarly, the absence of latero-frontal cilia in all specimens up to the largest observed (4 mm) indicates that the single row found in adults is a later development, rather than a vestige of a more abundant ciliation in ancestral forms. The anatomical data, together with in vivo observations of feeding in postlarvae, suggest that the developmental stages of the P. maximus gill correspond to critical changes in gill function. The early life of P. maximus may thus be characterized by distinct functional changes in feeding.
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References
Allen JA (1985) The recent Bivalvia: their form and evolution. In: Trueman ER, Clarke MR (eds) The Mollusca, Vol 10. Evolution. Academic Press, Orlando, pp 337–397
Ansell AD (1962) The functional morphology of the larva, and the post-larval development of Venus striatula (da Costa). J mar Biol Ass UK 42:419–443
Beninger PG, Le Pennec M, Salaün M (1988) New observations of the gills of Placopecten magellanicus (Mollusca: Bivalvia), and implications for nutrition. I. General anatomy and surface microanatomy. Mar Biol 98:61–70
Beninger PG, Ward JE, MacDonald BA, Thompson RJ (1992) Gill function and particle transport in Placopecten magellanicus (Mollusca: Bivalvia) as revealed using video endoscopy. Mar Biol 112:281–288
Bower SM, Meyer GR (1990) Atlas of anatomy and histology of larvae and early juvenile stages of the japanese scallop Patinopecten yessoensis. Can Spec Publ Fish aquat Sciences 111:1–51
Caddy JF (1969) Development of mantle organs, feeding, and locomotion in postlarval Macoma balthica (L.) (Lamellibranchia). Can J Zool 47:609–617
Cole HA (1937) Metamorphosis of the larva of Ostrea edulis. Nature, Lond 139:413–414
Creek GA (1960) The development of the lamellibranch Cardium edule L. Proc Zool Soc Lond 135:243–260
Dwiono SAP (1992) La métamorphose chez Pecten maximus L. (Mollusque, Bivalve). Doctoral thesis, Université de Bretagne Occidentale, Brest, France
Elston R (1980) Functional anatomy, histology, and ultrastructure of the soft tissues of the larval American oyster, Crassostrea virginica. Proc natn Shellfish Ass 70:65–93
Gabbott PA (1975) Energy metabolism. In: Bayne BL (ed) Marine mussels: their ecology and physiology. Cambridge, University Press, Cambridge, pp 293–355
Gérard A, Salaün M, Tritar S (1989) Critères de compétences des larves à la métamorphose chez Pecten maximus. Haliotis 19: 373–380
Gruffydd LID, Beaumont AR (1970) Determination of the optimum concentration of eggs and spermatozoa for the production of normal larvae in Pecten maximus (Mollusca, Lamellibranchia). Helgoländer wiss Meeresunters 20:486–497
Hickman RW, Gruffydd LID (1971) The histology of the larva of Ostrea edulis during metamorphosis. In: Crisp DJ (ed) Proc 4th Eur mar Biol Symp. Cambridge University Press, Cambridge, pp 281–293
Hodgson CA, Burke RD (1988) Development and larval morphology of the spiny scallop, Chlamys hastata. Biol Bull mar biol Lab, Woods Hole 174:303–318
Holland DL, Spencer BE (1973) Biochemical changes in fed and starved oysters, Ostrea edulis L. during larval development, metamorphosis and early spat growth. J mar biol Ass UK 53:287–298
Jackson RT (1890) Phylogeny of the Pelecypoda. The Aviculidae and their allies. Mem Boston Soc nat Hist 4:277–400, pl 23–30
Jørgensen CB (1990) Bivalve filter feeding: hydrodynamics, bioenergetics, physiology and ecology. Olsen and Olsen Press, Fredensborg, Denmark
Lacaze-Duthiers H (1856) Mémoire sur le développement des branchies des Mollusques Acéphales lamellibranches. Annls Sci nat (sér Zool) 5:5–47
Le Pennec M, Beninger PG, Herry A (1988a) New observations of the gills of Placopecten magellanicus (Mollusca: Bivalvia), and implications for nutrition. II. Internal anatomy and microanatomy. Mar Biol 98:229–237
Le Pennec M, Herry A, Lutz R, Fiala-Médioni A (1988b) Premières observations ultrastructurales de la branchie d'un Bivalve Pectinidae hydrothermal profound. C r hebd Acad Séanc Sci, Paris 307 (sér III):627–633
Manahan DT, Crisp DJ (1982) The role of dissolved organic matter in the nutrition of pelagic larvae: amino acid uptake by bivalve veligers. Am Zool 22:635–646
Manahan DT Crisp DJ (1983) Autoradiographic studies on the uptake of dissolved amino acids from sea water by bivalve larvae. J mar Biol Ass UK 63:673–682
Marshall CT, Lee K (1991) Uptake of dissolved glycine by sea scallop (Placopecten magellanicus (Gmelin, 1791)) larvae. In: Shumway SE, Sandifer PA (eds) Scallop biology and culture. World aquaculture workshops 1. The World Aquaculture Society, Baton Rouge pp 60–66
ÓFoighil D, Kingzett B, ÓFoighil G, Bourne N (1990) Growth and survival of Japanese scallops, Patinopecten yessoensis, in nursery culture. J Shellfish Res 9:135–144
Quayle DB (1952) Structure and biology of the larva and spat of Venerupis pullastra (Montagu). Trans R Soc Edinb 62 (Part I): 255–297
Reid RGB, McMahon RF, ÓFoighil D, Finnigan R (1992) Anterior inhalent currents and pedal feeding in bivalves. Veliger 35:93–104
Rice EL (1908) Gill development in Mytilus. Biol Bull mar biol Lab, Woods Hole 14:61–77
Ridewood WG (1903) On the structure of the gills of the lamellibranchia. Phil Trans R Soc Lond (Ser B) 195:147–284
Sastry AN (1965) The development and external morphology of pelagic larval and post-larval stages of the bay scallop, Aequipecten irradians concentricus Say, reared in the laboratory. Bull mar Sci 15:417–435
Waller TR (1981) Functional morphology and development of veliger larvae of the European oyster, Ostrea edulis Linné. Smithson Contr Zool 328:1–70
Ward JE, MacDonald BA, Thompson RJ, Beninger PG (1993) Mechanisms of suspension-feeding in bivalves: resolution of current controversies using endoscopy. Limnol Oceanogr 38:265–272
Whyte JNC, Bourne N, Ginther NG, Hodgson CA (1992) Compositional changes in the larva to juvenile development of the scallop Crassosdoma gigantea (Gray). J exp mar Biol Ecol 163: 13–29
Yonge CM (1926) Structure and physiology of the organs of feeding and digestion in Ostrea edulis. J mar biol Ass UK 14:295–386
Yonge CM (1947) The pallial organs in the aspidobranch Gastropoda and their evolution throughout the Mollusca. Phil Trans R Soc Lond (Ser B) 232:443–518
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Communicated by R. J. Thompson, St. John's
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Beninger, P.G., Dwiono, S.A.P. & Le Pennec, M. Early development of the gill and implications for feeding in Pecten maximus (Bivalvia: Pectinidae). Marine Bioliogy 119, 405–412 (1994). https://doi.org/10.1007/BF00347537
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DOI: https://doi.org/10.1007/BF00347537