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Gill development, functional and evolutionary implications in the Pacific oyster Crassostrea gigas (Bivalvia: Ostreidae)

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Abstract

Development of the Crassostrea gigas gill was studied in order to better understand the feeding biology of early life stages, identify potentially critical developmental stages which may influence rearing success or recruitment to wild populations, and shed light on the evolution of the basic bivalve gill types. Larvae and juveniles were reared in an experimental hatchery, and larger specimens were obtained from a commercial hatchery. Specimens were relaxed, fixed, dried, and observed using scanning electron microscopy (SEM). The right and left gills developed symmetrically, via a “cavitation–extension” process from the gill buds. The inner demibranchs developed first (V-stage, 0.29–2.70 mm), in a sequential postero-anterior series of homorhabdic filaments. The outer demibranchs developed later (W-stage, from 2.70 mm), also as homorhabdic filaments, synchronously along the gill axis. The principal filaments (PF) developed from the progressive fusion of three ordinary filaments (OF), at a size of 7.50 mm, and the consequent plication was accentuated by the formation of extensive tissue junctions. Effective filament number (number of descending and ascending filaments) showed a marked discontinuity at the transition from the V- to the W- stage of the gill. Filament ciliation showed several important changes: establishment of OF ciliation in the homorhabdic condition (2.70 mm), ciliary de-differentiation of the PF in the heterorhabdic condition (7.50 mm), and establishment of a latero-frontal cirri length gradient from the plical crest to the PF base. Reversal of direction of ciliary beat is also necessary prior to adult functioning of the PF. Three major transitions were identified in C. gigas gill development, each potentially important in rearing success or wild population recruitment: (1) transition from velum to gill at settlement, (2) transition from a V- to a W-shaped gill (2.70 mm), and (3) transition from the homorhabdic to the heterorhabdic condition (7.50 mm). Complete gill development was much more prolonged than in species previously studied. The major ontogenetic differences between the C. gigas heterorhabdic pseudolamellibranch gill and the pectinid heterorhabdic filibranch gill suggest that the heterorhabdic condition evolved independently in these two bivalve families.

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Acknowledgements

We thank Jean-Claude Cochard, Stéphane Pouvreau, Christian Mingant, and the Ecloserie expérimentale d’Argenton (IFREMER) for facilities, and assistance in larval and juvenile rearings. We are grateful to Stéphane Angeri (Vendée Naissain) for providing the larger juvenile specimens, and Alain Barreau for assistance in scanning electron microscopy. Research funding was provided by the Région des Pays de Loire (PhD stipend to RC), and partial operational funding was provided by IFREMER (Contrat universitaire IFREMER/EMI N° 03-2-2521559).

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  1. Laboratoire de Biologie Marine, Faculté des Sciences et Techniques, Université de Nantes, 2, rue de la Houssinière, 44322, Nantes Cedex 3, France

    Rozenn Cannuel & Peter G. Beninger

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  1. Rozenn Cannuel
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  2. Peter G. Beninger
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Correspondence to Peter G. Beninger.

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Communicated by S.A. Poulet, Roscoff

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Cannuel, R., Beninger, P.G. Gill development, functional and evolutionary implications in the Pacific oyster Crassostrea gigas (Bivalvia: Ostreidae). Mar Biol 149, 547–563 (2006). https://doi.org/10.1007/s00227-005-0228-6

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