Skip to main content
Log in

Morphological, gravimetric, and biochemical changes in Crepidula fecunda (Gastropoda: Calyptraeidae) egg capsule walls during embryonic development

  • Research Article
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Walls of egg capsules of the gastropod Crepidula fecunda Gallardo, 1979 were examined at different developmental stages during the period of intracapsular development of embryos. The weight, biochemical composition, and structural features (using scanning and transmission electron microscopy) of the capsule walls were examined at several intervals during development of the embryos to the hatching stage. Biochemical analyses were also carried out on the intracapsular fluid to identify the possible transfer of organic material from the capsule wall to the intracapsular fluid. The capsule wall is composed principally of organic matter, primarily protein (91%), plus minor lipid and carbohydrate components. The capsule wall consists of a thin, fibrous external layer, which overlies a thicker, spongy inner layer. The spongy layer has almost disappeared by the end of the developmental period, losing about 90% of its thickness. The 40% loss in weight of the capsule walls over the developmental period is due to loss of organic matter as protein. This suggests that the inner layer of the capsules dissolves and/or disintegrates as larval development advances. The levels of dissolved and/or particulate proteins in the intracapsular fluid are much higher than those typical of the seawater surrounding the capsules. This suggests that, as embryonic development proceeds, the inner capsule walls could potentially provide extra nutrients to the embryos.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4A–C.
Fig. 5.
Fig. 6.
Fig. 7.

Similar content being viewed by others

References

  • Barnes H, Heath J (1966) The extraction of glycogen from marine invertebrate tissues. Helgol Wiss Meeresunters 13:115–117

    Google Scholar 

  • Bayne CJ (1968) Histochemical studies on the egg capsules of eight gastropod molluscs. Proc Malacol Soc Lond 38:199

    Google Scholar 

  • Chaparro OR, Flores ML (2002) Reproductive output of Crepidula fecunda females: distribution of energy in the production of gametes and capsular walls. NZ J Mar Freshw Res 36:661–673

    Google Scholar 

  • Chaparro OR, Paschke KA (1990) Nurse egg feeding and energy balance in embryos of Crepidula dilatata (Gastropoda: Calyptraeidae) during intracapsular development. Mar Ecol Prog Ser 65:183–191

    Google Scholar 

  • Chaparro OR, Pereda SV, Bahamondes-Rojas I (2001) Effects of protandric sex change on radula, pedal morphology, and mobility in Crepidula fecunda (Gastropoda: Calyptraeidae). NZ J Mar Freshw Res 35:881–890

    Google Scholar 

  • Chaparro OR, Soto AE, Bertran CE (2002a) Velar characteristics and feeding capacity of encapsulated and pelagic larvae of Crepidula fecunda Gallardo, 1979 (Gastropoda, Calyptraeidae). J Shellfish Res 21:233–237

    Google Scholar 

  • Chaparro OR, Charpentier JL, Collin R (2002b) Embryonic velar structure and function of two sibling species of Crepidula with different modes of development. Biol Bull (Woods Hole) 203:80–86

    Google Scholar 

  • D’Asaro CN (1988) Micromorphology of neogastropod egg capsules. Nautilus 102:134–148

    Google Scholar 

  • De Mahieu GC, Penchaszadeh PE, Casal AB (1974) Algunos aspectos de las variaciones de proteínas y aminoácidos libres totales del líquido intracapsular en relación al desarrollo embrionario en Adelomelon brasiliana (Lamarck, 1811) (Gastropoda, Prosobranchia, Volutidae). Cah Biol Mar 15:215–227

    Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350–356

    CAS  Google Scholar 

  • Fioroni P, Scheidegger DP, Sundermann G (1985) Die Ultrastruktur der Larvalnieren bei intrakapsulären Larven von Nucella lapillus (Gastropoda, Prosobranchia, Stenoglossa). Zool Jahrb Abt Anat Ontolog Tiere 113:145–164

    Google Scholar 

  • Flower NE (1973) The storage and structure of proteins used in the production of egg capsules by the mollusc Cominella maculosa. J Ultrastruct Res 44:134–145

    CAS  PubMed  Google Scholar 

  • Flower NE, Geddes AJ, Rudall KM (1969) Ultrastructure of the fibrous protein from the egg capsules of the whelk Buccinum undatum. J Ultrastruct Res 26:262–273

    CAS  PubMed  Google Scholar 

  • Fretter V, Graham A (1994) British prosobranch molluscs. Their functional anatomy and ecology. Ray Society, London

  • Gallardo CS (1977) Two modes of development in the morphospecies Crepidula dilatata (Gastropoda: Calyptraeidae) from southern Chile. Mar Biol 39:241–251

    Google Scholar 

  • Gallardo CS (1979) Especies gemelas de género Crepidula (Gastropoda, Calyptraeidae) en la costa de Chile; una redescripción de C. dilatata Lamarck y descripción de C. fecunda n. sp. Stud Neotrop Fauna Environ 14:215–226

    Google Scholar 

  • Gallardo CS, Garrido O (1987) Nutritive egg formation in the marine snails Crepidula dilatata and Nucella crassilabrum. Int J Invertebr Reprod Dev 11:239–254

    Google Scholar 

  • Garrido O, Gallardo CS (1993) Ultraestructura de la cápsula ovífera de Concholepas concholepas (Bruguiere, 1789) (Gastropoda: Muricidae). Rev Biol Mar 28:191–201

    Google Scholar 

  • Gnaiger E (1983) Calculation of energetic and biochemical equivalents of respiratory oxygen consumption. In: Gnaiger E, Forstner H (eds) Polarographic oxygen sensors. Springer, Berlin Heidelberg New York

  • Gnaiger E, Bitterlich G (1984) Proximate biochemical composition and caloric content calculated from elemental CHN analysis: a stoichiometric concept. Oecologia 62:289–298

    Google Scholar 

  • Hawkins LE, Hutchinson S (1988) Egg capsule structure and hatching mechanism of Ocenebra erinacea (L.) (Prosobranchia: Muricidae). J Exp Mar Biol Ecol 119:269–283

    Article  Google Scholar 

  • Hoagland KE (1977) Systematic review of fossil and recent Crepidula and discussion of evolution of the Calyptraeidae. Malacologia 17:365–381

    Google Scholar 

  • Hoagland KE (1986) Patterns of encapsulation and brooding in the Calyptraeidae (Prosobranchia: Mesogastropoda). Am Malacol Bull 4:173–183

    Google Scholar 

  • Hunt S (1966) Carbohidrate and amino-acid composition of the egg capsule of the whelk Buccinum undatum L. Nature 210:436–437

    CAS  Google Scholar 

  • Jaeckle WB, Manahan DT (1989) Feeding by a “nonfeeding” larva: uptake of dissolved amino acids from seawater by lecithotrophic larvae of the gastropod Haliotis rufescens. Mar Biol 103:87–94

    CAS  Google Scholar 

  • Lord A (1986) Are the contents of egg capsules of the marine gastropod Nucella lapillus (L.) axenic? Am Malacol Bull 4:201–203

    Google Scholar 

  • Manahan DT, Crisp DJ (1983) Autoradiographic studies on the uptake of dissolved amino acids from sea water by bivalve larvae. J Mar Biol Assoc UK 63:673–682

    Google Scholar 

  • Marsh JB, Weinstein DB (1966) Simple charring method for determination of lipids. J Lipid Res 7:574–576

    CAS  PubMed  Google Scholar 

  • Miloslavich P (1999) Nutritional value of the intracapsular liquid of Engoniophos unicinctus Say, 1825 (Caenogastropoda: Buccinidae). J Moll Stud 65:502–503

    Article  Google Scholar 

  • Moran AL (1999) Intracapsular feeding by embryos of the gastropod genus Littorina. Biol Bull (Woods Hole) 196:229–244

    Google Scholar 

  • Paschke KA (1992) Fisiología, energética y composición bioquímica de Concholepas concholepas (Bruguiere, 1789) (Gastropoda: Muricidae) durante el desarrollo intracapsular. Tesis, Esc. de Biología Marina, Fac. de Ciencias, Univ. Austral de Chile

  • Pechenik JA (1975) The escape of veligers from the egg capsules of Nassarius obsoletus and Nassarius trivittatus (Gastropoda, Prosobranchia). Biol Bull (Woods Hole) 149:580–589

    Google Scholar 

  • Pechenik JA (1979) Role of encapsulation in invertebrate life histories. Am Nat 114:859–870

    Article  Google Scholar 

  • Pechenik JA (1982) Ability of some gastropod egg capsules to protect against low-salinity stress. J Exp Mar Biol Ecol 63:195–208

    Article  Google Scholar 

  • Pechenik JA (1983) Egg capsules of Nucella lapillus (L.) protect against low-salinity stress. J Exp Mar Biol Ecol 71:165–179

    Article  Google Scholar 

  • Pechenik JA, Chang SC, Lord A (1984) Encapsulated development of the marine prosobranch gastropod Nucella lapillus. Mar Biol 78:223–229

    Google Scholar 

  • Rawlings TA (1996) Shields against ultraviolet radiation: an additional protective role for the egg capsules of benthic marine gastropods. Mar Ecol Prog Ser 136:81–95

    Google Scholar 

  • Rivest BR (1980) Larval kidneys in marine prosobranch embryos: specialized structures for the uptake of egg capsule albumen. Am Zool 20:905

    Google Scholar 

  • Rivest BR (1986) Extra-embryonic nutrition in the prosobranch gastropod Urosalpinx cinerea (Say, 1822). Bull Mar Sci 39:498–505

    Google Scholar 

  • Rivest BR, Strathmann RR (1994) Uptake of protein by an independently evolved transitory cell complex in encapsulated embryos of neritoidean gastropods. In: Wilson WH, Stricker SA, Shinn GL (eds) Reproduction and development of marine invertebrates. Johns Hopkins University Press, Baltimore, pp 166–176

  • Saldivia CL (2000) Ovoposición y aspectos regulatorios de la capacidad de incubación en Crepidula fecunda Gallardo, 1979 (Gastropoda, Calyptraeidae). Tesis, Esc. de Biología Marina, Fac. de Ciencias, Univ. Austral de Chile

  • Stöckmann-Bosbach R, Althoff J (1989) A correlated morphological and biochemical study of capsular fluid of Nucella lapillus (Gastropoda: Prosobranchia: Muricidae). Mar Biol 102:283–289

    Google Scholar 

  • Sullivan ChH, Bonar DB (1984) Biochemical characterization of the hatching process of Ilyanassa obsoleta. J Exp Zool 229:223–234

    CAS  Google Scholar 

  • Sullivan Ch, Maugel T (1984) Formation, organization, and composition of the egg capsule of the marine gastropod, Ilyanassa obsoleta. Biol Bull (Woods Hole) 167:378–389

    Google Scholar 

  • Tamarin A, Carriker MR (1967) The egg capsule of the muricid gastropod Urosalpinx cinerea: an integrated study of the wall by ordinary light, polarized light, and electron microscopy. J Ultrastruct Res 21:26–40

    CAS  PubMed  Google Scholar 

  • Taylor HH (1973) The ionic properties of the capsular fluid bathing embryos of Lymnaea stagnalis and Biomphalaria sudanica (Mollusca: Pulmonata). J Exp Biol 59:543–564

    CAS  Google Scholar 

  • Vaughn CM (1953) Effects of temperature on hatching and growth of Lymnaea stagnalis appressa Say. Am Midl Nat 49:214–228

    Google Scholar 

  • Welborn JR, Manahan DT (1990) Direct measurements of sugar uptake from seawater into molluscan larvae. Mar Ecol Prog Ser 65:233–239

    CAS  Google Scholar 

Download references

Acknowledgements

We thank Mr. R. Silva for his help with the SEM samples and Dr. R.J. Thompson for commenting on this manuscript. This research was funded by Fondecyt–Chile (grants 1980984 and 1020171).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to O. R. Chaparro.

Additional information

Communicated by J.P. Grassle, New Brunswick

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ojeda, J.A., Chaparro, O.R. Morphological, gravimetric, and biochemical changes in Crepidula fecunda (Gastropoda: Calyptraeidae) egg capsule walls during embryonic development. Marine Biology 144, 263–269 (2004). https://doi.org/10.1007/s00227-003-1194-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-003-1194-5

Keywords

Navigation