Marine Biology

, Volume 151, Issue 3, pp 897–905 | Cite as

Acquisition of particle processing capability in juvenile oyster Crassostrea gigas: ontogeny of gill mucocytes

  • Rozenn Cannuel
  • Peter G. BeningerEmail author
Research Article


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.


Frontal Surface Shell Length Gill Filament Labial Palp Particle Processing 
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 S ANGERI (Vendée Naissain) for providing the juvenile specimens and O Aumaille for technical assistance in histology. Research funding was provided by the Région des Pays de Loire (PhD grant to RC), and partial operational funding was provided by IFREMER (Contrat IFREMER/EMI n 05-2-20723210).


  1. Atkins D (1937a) On the ciliary mechanisms and interrelationships of lamellibranchs. Part II. Sorting devices on the gills. Q J Microsc Sci 79:339–373Google Scholar
  2. 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 79:375–421Google Scholar
  3. Atkins D (1938) On the ciliary mechanisms and interrelationships of lamellibranchs. Part VII. Latero-frontal cilia of the gill filaments and their phylogenic value. Q J Microsc Sci 80:346–430Google Scholar
  4. Baker SM, Mann R (1994a) 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
  5. Baker SM, Mann R (1994b) Description of metamorphic phases in the oyster Crassostrea virginica and effects of hypoxia on metamorphosis. Mar Ecol Prog Ser 104:91–99CrossRefGoogle Scholar
  6. Barillé L (1994) Observations des éléments structuraux intervenant dans les mécanismes de nutrition préingestifs chez l’huître japonaise Crassostrea gigas. Haliotis 23:125–137Google Scholar
  7. Barillé L, Prou J, Héral M, Razet D (1997) Effects of high natural seston concentrations on the feeding, selection, and absorption of the oyster Crassostrea gigas (Thunberg). J Exp Mar Biol Ecol 212:149–172CrossRefGoogle Scholar
  8. Barillé L, Haure J, Cognie B, Leroy A (2000) Variations in pallial organs and eulatero-frontal cirri in response to high particulate matter concentrations in the oyster Crassostrea gigas. Can J Fish Aquat Sci 57:837–843CrossRefGoogle Scholar
  9. Beninger PG, Cannuel R (2006) Acquisition of particle processing capability in the oyster Crassostrea gigas: ontogeny of the mantle pseudofeces rejection tracts. Mar Ecol Prog Ser 325:153–163CrossRefGoogle Scholar
  10. 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
  11. Beninger PG, St-Jean SD (1997a) The role of mucus in particle processing by suspension-feeding marine bivalves: unifying principles. Mar Biol 129:389–397CrossRefGoogle Scholar
  12. Beninger PG, St-Jean SD (1997b) Particle processing on the labial palps of Mytilus edulis and Placopecten magellanicus (Mollusca: Bivalvia). Mar Ecol Prog Ser 147:117–127CrossRefGoogle Scholar
  13. Beninger PG, Veniot A (1999) The oyster proves the rule: mechanisms of pseudofeces transport and rejection on the mantle of Crassostrea virginica and C. gigas. Mar Ecol Prog Ser 190:179–188CrossRefGoogle Scholar
  14. 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 114:281–288CrossRefGoogle Scholar
  15. Beninger PG, St-Jean SD, Poussart Y, Ward JE (1993) Gill function and mucocyte distribution in Placopecten magellanicus and Mytilus edulis (Mollusca: Bivalvia): the role of mucus in particle transport. Mar Ecol Prog Ser 98:275–282CrossRefGoogle Scholar
  16. Beninger PG, Dufour SC, Bourque J (1997) Particle processing mechanisms of the eulamellibranch bivalves Spisula solidissima and Mya arenaria. Mar Ecol Prog Ser 150:157–169CrossRefGoogle Scholar
  17. 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
  18. 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
  19. Beninger PG, Decottignies P, Guiheneuf F, Barillé L, Rincé Y (2006) Comparison of particle processing in two introduced suspension-feeders: selection in Crepidula fornicata (Gastropoda) and Crassostrea gigas (Bivalvia). Mar Ecol Prog Ser (in press)Google Scholar
  20. Cannuel R, Beninger PG (2006) Gill development, functional and evolutionary implications in the Pacific oyster Crassostrea gigas (Bivalvia: Ostreidae). Mar Biol 149:547–563CrossRefGoogle Scholar
  21. Chaparro OR, Videla JA, Thompson RJ (2001) Gill morphogenesis in the oyster Ostrea chilensis. Mar Biol 138:199–207CrossRefGoogle Scholar
  22. Cognie B (2001) Alimentation de l’huître Crassostrea gigas (Thunberg): étude des mécanismes de sélection des particules et des processus rétroactifs entre le bivalve et les microalgues. PhD thesis, University of NantesGoogle Scholar
  23. 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
  24. Dégremont L, Bédier E, Soletchnik P, Ropert M, Huvet A, Moal J, Samain J-F, Boudry P (2005) Relative importance of family, site, and field placement timing on survival, growth, and yield of hatchery-produced Pacific oyster spat (Crassostrea gigas). Aquaculture 249:213–229CrossRefGoogle Scholar
  25. 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
  26. 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
  27. Eble AF, Scro R (1996) General anatomy. In: Kennedy VS, Newell RIE, Eble AF (eds) The Eastern oyster Crassostrea virginica. Maryland Sea Grant Book, College Park, pp 19–73Google Scholar
  28. FAO (2005) Total production 1950–2003. Aquaculture production: values 1984–2003. Fishstat Plus 2.30. Food and Agricultural Organisation, United Nations, RomeGoogle Scholar
  29. Galtsoff PS (1964) The American oyster, Crassostrea virginica (Gmelin). US Fish Wildl Ser Fish Bull 64:1–480Google Scholar
  30. Huvet A, Herpin A, Dégremont L, Labreuche Y, Samain J-F, Cunningham C (2004) The identification of genes from the oyster Crassostrea gigas that are differentially expressed in progeny exhibiting opposed susceptibility to summer mortality. Gene 343:211–220CrossRefGoogle Scholar
  31. Lacoste A, Jalabert F, Malham S, Cueff A, Gélébart F, Cordevant C, Lange M, Poulet SA (2001) A Vibrio splendidus strain is associated with summer mortality of juvenile oysters Crassostrea gigas in the Bay of Morlaix (North Brittany, France). Dis Aquat Org 46:139–145CrossRefGoogle Scholar
  32. Nelson TC (1960) The feeding mechanism of the oyster. II. On the gills and palps of Ostrea edulis, Crassostrea virginica and C. angulata. J Morphol 107:163–191CrossRefGoogle Scholar
  33. Newell RIE, Jordan SJ (1983) Preferential ingestion of organic material by the American oyster Crassostrea virginica. Mar Ecol Prog Ser 13:47–53CrossRefGoogle Scholar
  34. Ribelin BW, Collier A (1977) Studies on the gill ciliation of the American oyster Crassostrea virginica (Gmelin). J Morphol 151:439–450CrossRefGoogle Scholar
  35. Ridewood WG (1903) On the structure of the gills of the Lamellibranchia. Philos Trans R Soc Lond B 195:147–284CrossRefGoogle Scholar
  36. Riera P, Richard P (1996) Isotopic determination of food sources of Crassostrea gigas along a trophic gradient in the estuarine bay of Marennes-Oléron. Estuar Coast Shelf Sci 42:347–360CrossRefGoogle Scholar
  37. Ruesink JL, Lenihan HS, Trimble AC, Heiman KW, Micheli F, Byers JE, Kay MC (2005) Introduction of non-native oysters: ecosystem effects and restoration implications. Annu Rev Ecol Evol Syst 36:643–689CrossRefGoogle Scholar
  38. Samain J-F, Boudry P, Dégremont L, Soletchnik P, Ropert M, Moal J, Mathieu M, Pouvreau S, Lambert C, Escoubas JM, Nicolas JL, Le Roux F, Renault T, Burgeot T, Bacher C (2004) Summer mortality in the Pacific oyster Crassostrea gigas, overview of three year results of the cooperative “MOREST” project. J Shellfish Res 23:309–310Google Scholar
  39. 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
  40. Ward JE, MacDonald BA, Thompson RJ, Beninger PG (1993) Mechanisms of suspension feeding in bivalves: resolution of current controversies by means of endoscopy. Limnol Oceanogr 38:265–272CrossRefGoogle Scholar
  41. Ward JE, Newell RIE, Thompson RJ, MacDonald BA (1994) In vivo studies of suspension-feeding processes in the Eastern oyster, Crassostrea virginica (Gmelin). Biol Bull 186:221–240CrossRefGoogle Scholar
  42. Ward JE, Levinton JS, Shumway SE, Cucci T (1998) Particle sorting in bivalves: in vivo determination of the pallial organs of selection. Mar Biol 131:283–292CrossRefGoogle Scholar
  43. Wilson JH (1980) Particle retention and selection by larvae and spat of Ostrea edulis in algal suspensions. Mar Biol 57:135–145CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Ecophysiologie Marine Intégrée, EA 2663, ISOMer-UFR SciencesUniversité de Nantes, Nantes Atlantique UniversitésNantes Cedex 3France

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