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

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.     

Acquisition of particle processing capability in juvenile oyster <Emphasis Type="Italic">Crassostrea gigas</Emphasis>: ontogeny of gill mucocytes

Acquisition of particle processing capability in postlarval oysters depends upon the structural development of the pallial organs, as well as the development of cilia and mucocytes used (either directly or indirectly) in particle capture and transport. Mucocyte mapping was therefore used to identify mucocyte types and distributions throughout gill development in juvenile oyster Crassostrea gigas (Thunberg 1793) specimens from 2.9 mm to 2.4 cm in shell length. Three categories of gill filaments were identified: apical, lateral and principal filaments, corresponding to filament location or future location in gill plicae. Mucocyte densities were recorded per linear μm (l μm) of frontal surface, and converted to potential total volumes, using the mean volumes of each of the two major mucocyte types: acid mucopolysaccharide (AMPS)-mucocytes and mixed mucopolysaccharide (MMPS)-mucocytes. While AMPS secretions were dominant up to 1.0 cm (flat homorhabdic gill, to semi-heterorhabdic differentiation and plication), MMPS secretions increased progressively, dominating in 2.4 cm and adult specimens (fully heterorhabdic and plicated). Mucus composition, and hence mucus viscosity, thus appears to evolve in relation to the degree of enclosure of the gill frontal surfaces. Total (AMPS + MMPS) potential mucus secretion increased allometrically with juvenile growth, characterized by a sharp increase between 10 and 24 mm shell length, suggesting a marked improvement in particle processing capability. Mucocyte distributions on the gill were heterogeneous from the onset of heterorhabdic differentiation (7.5 mm): the apical filaments of the plicae contained much greater mucocyte total volumes, compared to the lateral and principal filaments. In addition to mucus composition, total potential mucus volume thus also evolved in relation to the degree of enclosure of the gill frontal surfaces. These results show that functional specialization in mucocyte distribution precedes the complete anatomical heterorhabdic differentiation. The completely functional adult gill system is thus attained in 2.4 cm juveniles. This information should be of use in understanding the dynamics of juvenile feeding, growth, and mortality, both in natural systems and in rearing operations.