Marine Biology

, Volume 149, Issue 3, pp 547–563 | Cite as

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

  • Rozenn Cannuel
  • Peter G. BeningerEmail author
Research Article


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.


Cavitation Gill Filament Gill Lamella Lateral Cilium Ventral Extremity 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



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).


  1. Baker SM, Mann R (1994a) Description of metamorphic phases in the oyster Crassostrea virginica and effects of hypoxia on metamorphosis. Mar Ecol Prog Ser 104:91–99CrossRefGoogle Scholar
  2. Baker SM, Mann R (1994b) Feeding ability during settlement and metamorphosis in the oyster Crassostrea virginica (Gmelin, 1791) and the effects of hypoxia on post-settlement ingestion rates. J Exp Mar Biol Ecol 181:239–253CrossRefGoogle Scholar
  3. Bayne BL (1971) Some morphological changes that occur at the metamorphosis of the larvae of Mytilus edulis. In: Crisp DJ (ed) Proceedings of 4th European marine biology symposium. European marine biology symposia, vol 4. pp 259–280Google Scholar
  4. Beninger PG, Dufour SC (1996) Mucocyte distribution and relationship to particle transport on the pseudolamellibranch gill of Crassostrea virginica (Bivalvia: Ostreidae). Mar Ecol Prog Ser 137:133–138CrossRefGoogle Scholar
  5. Beninger PG, Dufour SC (2000) Evolutionary trajectories of a redundant feature: lessons from bivalve gill abfrontal cilia and mucocyte distributions. In: Harper EM, Taylor JD, Crame JA (eds) The evolutionary biology of the Bivalvia. vol 177.Geological Society, London (special publications), pp 273–278Google Scholar
  6. Beninger PG, Dwiono SAP, Le Pennec M (1994) Early development of the gill and implications for feeding in Pecten maximus (Bivalvia: Pectinidae). Mar Biol 119:405–412CrossRefGoogle Scholar
  7. Beninger PG, Potter TM, St-Jean SD (1995) Paddle cilia fixation artefacts in pallial organs of adult Mytilus edulis and Placopecten magellanicus (Mollusca, Bivalvia). Can J Zool 73:610–614CrossRefGoogle Scholar
  8. Beninger PG, Veniot A, Poussart Y (1999) Principles of pseudofeces rejection on the bivalve mantle: integration in particle processing. Mar Ecol Prog Ser 178:259–269CrossRefGoogle Scholar
  9. Beninger PG, Dufour SC, Decottignies P, Le Pennec M (2003) Particle processing mechanisms in the archaic, peri-hydrothermal vent bivalve Bathypecten vulcani, inferred from cilia and mucocyte distributions on the gill. Mar Ecol Prog Ser 246:183–195CrossRefGoogle Scholar
  10. Beninger PG, Decottignies P, Rincé Y (2004) Localization of qualitative particle selection sites in the heterorhabdic filibranch Pecten maximus (Bivalvia: Pectinidae). Mar Ecol Prog Ser 275:163–173CrossRefGoogle Scholar
  11. Beninger PG, Cannuel R, Jaunet S (2005) Particle processing on the gill plicae of the oyster Crassostrea gigas: fine-scale mucocyte distribution and functional correlates. Mar Ecol Prog Ser 295:191–199CrossRefGoogle Scholar
  12. Braet F, De Zanger R, Wisse E (1997) Drying cells for SEM, AFM and TEM by hexamethyldisilazane: a study on hepatic endothelial cells. J Microsci 186:84–87CrossRefGoogle Scholar
  13. Bricelj VM, Ford SE, Borrero FJ, Perkins FO, Rivara G, Hillman RE, Elston RA, Chang J (1992) Unexplained mortalities of hatchery-reared, juvenile oysters, Crassostrea virginica Gmelin. J Shellfish Res 11:331–347Google Scholar
  14. Cannuel R, Beninger PG (2005) Is oyster broodstock feeding always necessary? A study using oocyte quality predictors and validators in Crassostrea gigas. Aquat Living Resour 18:35–43CrossRefGoogle Scholar
  15. Chaparro OR, Videla JA, Thompson RJ (2001) Gill morphogenesis in the oyster Ostrea chilensis. Mar Biol 138:199–207CrossRefGoogle Scholar
  16. Cognie B, Barillé L, Massé G, Beninger PG (2003) Selection and processing of large suspended algae in the oyster Crassostrea gigas. Mar Ecol Prog Ser 250:145–152CrossRefGoogle Scholar
  17. Cole HA (1937) Metamorphosis of the oyster Ostrea edulis. Nature 139:413–414CrossRefGoogle Scholar
  18. Cole HA (1938) The fate of the larval organs in the metamorphosis of the oyster Ostrea edulis. J Mar Biol Assoc UK 22:469–484CrossRefGoogle Scholar
  19. Dubois S, Barillé L, Cognie B Beninger PG (2005) Particle capture and processing mechanisms in Sabellaria alveolata (Polychaeta: Sabellariidae). Mar Ecol Prog Ser 301: 159–171CrossRefGoogle Scholar
  20. Dufour SC, Beninger PG (2001) A functional interpretation of cilia and mucocyte distributions on the abfrontal surface of bivalve gills. Mar Biol 138:295–309CrossRefGoogle Scholar
  21. Dufour SC, Steiner G, Beninger PG (2005) Phylogenetic analysis of the peri-hydrothermal vent bivalve Bathypecten vulcani based on 18S rRNA. Malacologia (in press)Google Scholar
  22. Eble AF, Scro R (1996) General anatomy. In: Kennedy VS, Newell RIE, Eble AF (eds) The Eastern oyster Crassostrea virginica. Maryland Sea Grant, Maryland, pp 19–73Google Scholar
  23. Forbes TL, Lopez GR (1989) Determination of critical periods in ontogenetic trajectories. Funct Ecol 3:625–632CrossRefGoogle Scholar
  24. Galstoff PS (1964) The American oyster, Crassostrea virginica Gmelin. US Fish Wildl Ser Fish Bull 64:1–480Google Scholar
  25. Giribet G, Wheeler WC (2002) On bivalve phylogeny: a high-level analysis of the Bivalvia (Mollusca) based on combined morphology and DNA sequence data. Invertebr Biol 121:271–324CrossRefGoogle Scholar
  26. Gosling E (2003a) Reproduction, settlement and recruitment. In: Gosling E (ed) Bivalve molluscs: biology, ecology and culture. Fishing news books, Blackwell, Oxford, pp 131–168CrossRefGoogle Scholar
  27. Gosling E (2003b) Diseases and parasites. In: Gosling E (ed) Bivalve molluscs: biology, ecology and culture. Fishing news books, Blackwell, Oxford, pp 370–411CrossRefGoogle Scholar
  28. Gosling E (2003c) Bivalve culture. In: Gosling E (ed) Bivalve molluscs: biology, ecology and culture. Fishing news books, Blackwell, Oxford, pp 284–332CrossRefGoogle Scholar
  29. Gosselin LA, Qian PY (1996) Early post-settlement mortality of an intertidal barnacle: a critical period for survival. Mar Ecol Prog Ser 135:69–75CrossRefGoogle Scholar
  30. Gosselin LA, Qian PY (1997) Juvenile mortality in benthic marine invertebrates. Mar Ecol Prog Ser 146:265–282CrossRefGoogle Scholar
  31. Gusnard D, Kirshner RH (1977) Cell and organelle shrinkage during preparation for scanning electron microscopy: effects of fixation, dehydration and critical point drying. J Microscopy 110:51–57CrossRefGoogle Scholar
  32. Heraty J, Hawks D (1998) Hexamethyldisilazane—a chemical alternative for drying insects. Entomol News 109:369–374Google Scholar
  33. Hochberg R, Litvaitis MK (2000) Hexamethyldisilazane for scanning electron microscopy of Gastrotricha. Biotech Histochem 75:41–44CrossRefPubMedCentralGoogle Scholar
  34. Hunt HL, Scheibling RE (1997) Role of early post-settlement mortality in recruitement of benthic marine invertebrates. Mar Ecol Prog Ser 155:269–301CrossRefGoogle Scholar
  35. Jackson RT (1888) The development of oyster with remarks on allied genera. Proc Boston Soc Nat Hist 23:531–556Google Scholar
  36. Jackson RT (1890) Phylogeny of the pelecypoda. The aviculidae and their allies. Mem Read Boston Soc Nat Hist 4:277–400, 23–30Google Scholar
  37. Jones HD, Richards OG, Hutchinson S (1990) The role of ctenidial abfrontal cilia in water pumping in Mytilus edulis L. J Exp Mar Biol Ecol 143:15–26CrossRefGoogle Scholar
  38. Jones HD, Richards OG, Southern TA. (1992) Gill dimensions, water pumping rate, and body size in the mussel Mytilus edulis L.. J Exp Mar Biol Ecol 155:213–237CrossRefGoogle Scholar
  39. Kingzett BC (1993) Ontogeny of suspension feeding in post-metamorphic Japanese scallops, Patinopecten yessoensis (Jay). MS Thesis, Simon Fraser UniversityGoogle Scholar
  40. Korniushin AV (1996) Growth and development of the outer demibranch in freshwater clams (Mollusca: Bivalvia): a comparative study. Ann Zool 46:111–124Google Scholar
  41. Korniushin AV (1997) Patterns of gill structure and development as taxonomic characters in bivalve Molluscs (Mollusca, Bivalvia). Ann Zool 46:245–254CrossRefGoogle Scholar
  42. Krantz GE, Chamberlin JV (1978) Blue crab predation on cultchless oyster spat. Proc Natl Shellfish Assoc 68:38–41Google Scholar
  43. Lacaze-Duthiers H (1856) Mémoire sur le développement des branchies des mollusques acéphales lamellibranches. Ann Sci Nat B 5:5–47Google Scholar
  44. Leibson NL, Movchan OT (1975) Cambial zones in gills of Bivalvia. Mar Biol 31:175–180CrossRefGoogle Scholar
  45. Masski H, Guillou J (1999) The role of biotic interactions in juvenile mortality of the cockle (Cerastoderma edule L.): field observations and experiment. J Shellfish Res 18:575–578Google Scholar
  46. Moor B (1983) Organogenesis. In: Verdonk NH, van den Biggelaar JAM, Tompa AS (eds) The mollusca development. vol 3. Academic Press, New York, pp 123–177Google Scholar
  47. Nation JL (1983) A new method using hexamethyldisilazane for preparation of s oft insect tissues for scanning electron microscopy. Stain Technol 58:347–351CrossRefPubMedCentralGoogle Scholar
  48. Neumann D, Kappes H (2003) On the growth of bivalve gills initiated from a lobule-producing budding zone. Biol Bull 205:73–82CrossRefPubMedCentralGoogle Scholar
  49. Newell RIE, Alspach GS Jr, Kennedy VS, Jacobs D (2000) Mortality of newly metamorphosed eastern oysters (Crassostrea virginica) in mesohaline Chesapeake Bay. Mar Biol 136:665–676CrossRefGoogle Scholar
  50. Ó Foighil D, Kingzett B, Ó Foighil G, Bourne N (1990) Growth and survival of juvenile Japanese scallops, Patinopecten yessoensis, in nursery culture. J Shellfish Res 9:135–144Google Scholar
  51. Osman RW, Whitlatch RB, Zajac RN (1989) Effects of resident species on recruitment into a community: larval settlement versus post-settlement mortality in the oyster Crassostrea virginica. Mar Ecol Prog Ser 54:61–73CrossRefGoogle Scholar
  52. Pechenik JA (1999) On the advantages and disadvantages of larval stages in benthic marine invertebrates life cycles. Mar Ecol Prog Ser 177:269–297CrossRefGoogle Scholar
  53. Quayle DB (1952) Structure and biology of the larva and spat of Venerupis pullastra (Montagu). Trans R Soc Edinb 62(1):255–297CrossRefGoogle Scholar
  54. Raven CP (1958) Morphogenesis: the analysis of molluscan development. Pergamon, New YorkGoogle Scholar
  55. Rice EL (1908) Gill development in Mytilus. Biol Bull 14:61–77CrossRefGoogle Scholar
  56. Ridewood WG (1903) On the structure of the gills of the Lamellibranchia. Philos Trans R Soc Lond B 1905:147–284CrossRefGoogle Scholar
  57. Robert R, Gérard A (1999) Bivalve hatchery technology: the current situation for the Pacific oyster Crassostrea gigas and the scallop Pecten maximus in France. Aquat Living Resour 12:121–130CrossRefGoogle Scholar
  58. Robert R, Parisi G, Rodolfi L, Poli BM, Tredici MR (2001) Use of fresh and preserved Tetraselmis suecica for feeding Crassostrea gigas larvae. Aquaculture 192:333–346CrossRefGoogle Scholar
  59. Roegner GC (1991) Temporal analysis of the relationship between settlers and early recruits of the oyster Crassostrea virginica (Gmelin). J Exp Mar Biol Ecol 151:57–69CrossRefGoogle Scholar
  60. Roegner GC, Mann R (1995) Early recruitment and growth of the American oyster Crassostrea virginica (Bivalvia: Ostreidae) with respect to tidal zonation and season. Mar Ecol Prog Ser 117:91–101CrossRefGoogle Scholar
  61. Rumrill SS (1990) Natural mortality of marine invertebrate larvae. Ophelia 32:163–198CrossRefGoogle Scholar
  62. Silverman H, Lynn JW, Beninger PG, Dietz TH (1999) The role of latero-frontal cirri in particle capture by the gills of Mytilus edulis. Biol Bull 197:368–376CrossRefPubMedCentralGoogle Scholar
  63. Silverman H, Lynn JW, Dietz TH (1996) Particle capture by the gills of Dreissena polymorpha: structure and function of latero-frontal cirri. Biol Bull 191:42–54CrossRefPubMedCentralGoogle Scholar
  64. Stasek CR (1962) Aspects of ctenidial feeding in immature bivalves. Veliger 5:78–79Google Scholar
  65. Tamm SL, Terasaki M (1994) Visualization of calcium transients controlling orientation of ciliary beat. J Cell Biol 125:1127–1135CrossRefPubMedCentralGoogle Scholar
  66. Veniot A, Bricelj VM, Beninger PG (2003) Ontogenic changes in gill morphology and potential significance for food acquisition in the scallop Placopecten magellanicus. Mar Biol 142:123–131CrossRefGoogle Scholar
  67. Ventilla RF (1984) Recent developments in the Japanese oyster culture industry. Adv Mar Biol 21:1–57CrossRefGoogle Scholar
  68. Waller T (1981) Functional morphology and development of veliger larvae of the European oyster, Ostrea edulis Linné. Smithson Contrib Zool 328:1–70CrossRefGoogle Scholar
  69. Walne PR (1974) Culture of bivalve molluscs: 50 years’ experience at Conwy. Fishing news books, OxfordGoogle Scholar
  70. Ward JE, Levinton JS, Shumway SE, Succi T (1998) Particle sorting in bivalves: in vivo determination of the pallial organs of selection. Mar Biol 131:283–292CrossRefGoogle Scholar
  71. Whyte JNC, Bourne N, Ginther NG, Hodgson CA (1992) Compositional changes in the larva to juvenile development of the scallop Crassadoma gigantea (Gray). J Exp Mar Biol Ecol 163:13–29CrossRefGoogle Scholar
  72. Wilson JH (1980) Particle retention and selection by larvae and spat of Ostrea edulis in algal suspensions. Mar Biol 57:135–145CrossRefGoogle Scholar
  73. Yonge CM (1926) Structure and physiology of the organs of feeding and digestion in Ostrea edulis. J Mar Biol Assoc UK 14:295–386, 92CrossRefGoogle Scholar
  74. Zajac RM, Whitlatch RB, Osman RW (1989) Effects of inter-specific density and food supply on survivorship and growth of newly settled benthos. Mar Ecol Prog Ser 56:127–132CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Laboratoire de Biologie Marine, Faculté des Sciences et TechniquesUniversité de NantesNantes Cedex 3France

Personalised recommendations