Initiation, calcification, and form of larval “archaeogastropod” shells

Abstract

The coiled shell of gastropods begins as a cap-shaped lens of organic and calcined material that covers the posterior dorsal side of the larva. During development the cap enlarges to cover the larval visceral mass. Marginal growth then produces the characteristic coiled shell. One model of the initiation of shell coiling in "archaeogastropods" requires that the shell remains flexible and uncalcined until after torsion, and that muscle contraction during torsion deforms the shell. We describe early shell calcification and tested this requirement of the model for the patellogastropod limpets Tectura scutum and Lottia digitalis, the trochids Calliostoma ligatum and Margarites pupillus and the abalone Haliotis kamtschatkana. We determined the stage of initial calcification by staining larvae with the fluorescent calcium marker calcein and observing them with bright field, crossed polarizing filter, and fluorescence microscopy. In T. scutum the earliest observable shell was calcified and calcium was sometimes detected even before the initial shell was visible. Larvae of the other species deposited a noncalcified matrix that was subsequently calcified, and in C. ligatum and M. pupillus this initial calcification was distinctly spotty. Shells of both patellogastropods and the abalone were demonstrably rigid prior to torsion while the shells of the trochids were not. These results suggest that shell coiling in patellogastropods and abalone is not initiated by contraction of the larval retractor muscle during torsion; in trochids this mechanism is possible. However, analysis of camera lucida drawings of pre-and post-torsional shells of T. scutum and C. ligatum did not detect shell shape changes during torsion.

Light and electron microscopy study of late embryonic development in the land snail Limicolaria flammea (Müller) (Pulmonata, Achatinidae)

“…In addition to mechanical support, the function of the calcified egg shell is to supply the developing embryo with calcium to form the embryonic shell by the time of hatching (TOMPA 1979a(TOMPA , b, 1980(TOMPA , 1984. Coiling was observed in late post torsional shell in L. flammea similar to that reported in archaeogastropods probably due to growth around the aperture and thickened lips (COLLIN & VOLTZOW 1998). Embryos need more calcium than can be provided in the egg albumen and many terrestrial snails are known to cover their terrestrial eggs with soil rich in calcium (TOMPA 1980).…”

“…The shell which develops partially during embryonic development of the snail is called a protoconch; before torsion the protoconch is composed of flexible organic material (COLLIN & VOLTZOW 1998) which can be easily deformed asymmetrically by the pressure from the foot and contraction of the larval retractile muscles resulting in coiling of the formerly symmetrical embryonic shell. An organic layer is deposited in the shell of gastropods before calcification begins (COLLIN & VOLTZOW 1998) and measurable calcium levels was reported in the protoconch of pulmonate embryos, which was obtained from the egg shell calcium (TOMPA 1975 ABSTRACT. The late stages of embryogenesis in the achatinid land snail Limicolaria flammea (Müller, 1774) were described using light and electron microscopy.…”

Possible functions of Dpp in gastropod shell formation and shell coiling

“…2d,h and 3d,e). Therefore, the onset of mineralization is a little later than that of other gastropod species (Eyster and Morse 1984;Eyster 1986;Bielefeld and Becker 1991;Collin and Voltzow 1998;Jardillier et al 2008). The initial mineralization is likely to be performed not by the shell gland but by the mantle in L. stagnalis.…”

“…It appears that the initial shell mineralization generally occurs at the pre-veliger stage in gastropods (Eyster and Morse 1984;Eyster 1986;Collin and Voltzow 1998;Jardillier et al 2008). …”

Technical Note: Towards resolving in situ, centimeter-scale location and timing of biomineralization in calcareous meiobenthos – the calcein–osmotic pump method

“…The method employs commercially available osmotic pumps to deliver calcein, which is a fluorescent compound that binds to calcium in biomineralized structures as it is precipitated (e.g., Medeiros-Bergen and Ebert, 1995;Monaghan, 1993;Moran, 2000;Collin and Voltzow, 1998;Hernaman et al, 2000). Using full immersion incubations, calcein has been used to mark bivalves (e.g., Kaehler and McQuaid, 1999;Moran and Marko, 2005;van der Geest et al, 2011) and in laboratory studies regarding foraminiferal calcification Denoyelle et al, 2012;Dissard et al, 2009;Filipsson et al, 2010;Kurtarkar et al, 2015;Nardelli et al, 2014).…”