Interior Remodeling of the Shell by a Gastropod Mollusc (Biomineralization/Conus/Shell Dissolution) ALAN J

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Interior Remodeling of the Shell by a Gastropod Mollusc (Biomineralization/Conus/Shell Dissolution) ALAN J Proc. Natl. Acad. Sci. USA Vol. 76, No. 7, pp. 3406-3410, July 1979 Evolution Interior remodeling of the shell by a gastropod mollusc (biomineralization/Conus/shell dissolution) ALAN J. KOHN, ELIZABETH R. MYERS, AND V. R. MEENAKSHI Department of Zoology, University of Washington, Seattle, Washington 98195 Communicated by W. T. Edmondson, April 26, 1979 ABSTRACT As the Conus shell grows by spiraling of the outer lip around the axis, profound internal shell dissolution thins the walls of the protected penultimate whorl from several millimeters to <50&m. Shell material is added to the inside of the spire and the anterior part of the columella. The resulting shell has a uniformly thick last whorl and thickened spire that enhance defense against crushing predators and a greatly ex- panded interior living space for the animal. The molluscan shell has gained prominence in recent years as an especially favorable system for the analysis of biominerali- zation processes (1-4). Much less attention has been paid to shell dissolution, a continuing, permanent, and profound process that alters exterior and interior surfaces of the shell in certain pro- sobranch gastropods (5-7). In the genus Conus, dissolution of the internal walls of the shell is particularly striking while shell material is added from within to thicken regions of the shell some distance from its growing edge. Although these renova- tions have not been studied previously, the resulting very thin inner wall structure has long been known (8) and was used as the primary character separating subfamilies of the Conidae in an early classification (9). In this study we addressed the following questions: (i) What regions and layers of the shell are involved in dissolution and FIG. 1. Axial section of shell of C. lividus Hwass in Bruguiere, thickening? (ii) Of the shell material deposited by the animal illustrating terms used. The outer lip is at right (also the animal's right during its life, how much is later dissolved? (iii) How much of side); the anterior end is at the bottom. Outermost calcified layer 1 the animal's living space within the shell does dissolution pro- appears white but contains a yellow pigment in C. lividus. Layer 2 duce? (iv) What is the adaptive significance of interior shell contains dark purple to brown pigment visible in the photograph. Inner layers 3 and 4 appear white and indistinguishable from each remodeling? other. Lines mark percentages of total aperture height and correspond to cross sections in Figs. 2 and 3. i, Posterior region of whorl where MATERIALS AND METHODS dissolution does not occur; ii, depositional region at adhesion zone on previous whorl; iii, depositional region on abapical surface ofdis- We selected Conus lividus Hwass in Bruguiere, an inhabitant solved previous whorl; col, anterior thickening of columella; ridge, of tropical Indo-West Pacific coral reefs, as representative of spiral ridge in last whorl. the genus. Shells collected in Hawaii were filled with resin to preserve the integrity of the inner whorls and then were sec- tioned axially or transversely to permit measurements of shell the several layers comprising the gastropod shell (11). The thickness. Etched, polished, gold-coated sections were used to mantle on the animal's right side secretes the growing edge or aid visualization of boundaries between shell layers. For scan- outer lip of the dextrally coiled shell. The outermost shell layer ning electron microscopy, pieces of fractured shell were cleaned is the uncalcified proteinaceous periostracum. Inward of this in dilute sodium hypochlorite and coated with gold or gold/ are several layers of crystalline CaCO3 with a glycoprotein palladium. matrix of 2% or less by weight (1, 12). Primitive prosobranch gastropods (order Archaeogastropoda) vary widely in crystal RESULTS form and architecture (13). Shells of the most derived order Neogastropoda are structurally more uniform, consisting pri- In C. lividus as well as most species in the genus, both spire and marily of three or four aragonitic layers of linear or branching last whorl are conic; thus, the whole shell appears biconic, with This consists of a long, narrow aperture (Fig. 1). As the shell grows, its shape crossed lamellar crystal architecture (14, 15). remains constant (10). series of elongate, curved, branching and interdigitating pri- To appreciate dissolution, one must understand how the shell mary lamels, each comprised of secondary lamels oriented as is produced. Histochemically differentiated regions of outer parallel laths. Each secondary lamel consists of tertiary lamels; and calcium cells secrete these are parallel needle- or rod-like crystals (Fig. 2E) (13-17). mantle epithelium underlying gland The secondary lamels in adjacent primary lamels are oriented at a characteristic angle [commonly, 82° (14); mean d SD, 82.90 The publication costs of this article were defrayed in part by page L charge payment. This article must therefore be hereby marked "ad- 5.50 in layers 1 and 3 of a specimen of C. lividus]. This is a vertisement" in accordance with 18 U. S. C. §1734 solely to indicate strong, interwoven or interlocking structure analogous to ply- this fact. wood (16, 17). Although the pattern is not rigidly maintained 3406 Downloaded by guest on September 30, 2021 Evolution: Kohn et al. Proc. Natl. Acad. Sci. USA 76 (1979) 3407 Thickness of the shell, and of each component layer, is rather uniform proximal to the growth region of the outer lip in the posterior region of the last whorl (Figs. 2B, 3 A, B, E, and F). ! Layer 2 is the thickest (Fig. 2E) and strongest; it determines the I path of shell breakage, particularly near the outer lip where the growing shell is thin and most susceptible to damage from ac- cident or attempted predation (18). The shell is thickened in two ways anterior to the midregion I of the last whorl, primarily by layer 3: (i) between about 2250 and the columella (Fig. 1, col; Fig. 2 C and D; major peaks in Fig. 3C; high end points of curves in Fig. 3D), and (i) a spiral ridge characteristic of C. lividus and certain other species of Conus but not of general occurrence in the genus (Figs. 1 and .i. 2C; peaks in Fig. 3D and at left in Fig. 3C). Figs. 2B and 4 show that the shell does not merely gradually t1 thicken as it grows. The walls of the penultimate and earlier whorls are extremely thin, due to dissolution that begins slightly I I4 more than one revolution in from the outer lip (range 3720- 4560; mean, 413°; n = 13) and is mostly completed within an arc of 85°-160° (mean, 1120; n = 8). If thinning of the penul- timate whorl did not keep pace with thickening of the last whorl, the narrow aperture of the shell would be nearly oc- cluded (Fig. 2B). Etched, polished sections and scanning electron micrographs of fractured shells in the region of dissolution show that shell material is dissolved smoothly and without regard to crystal architecture (Fig. 4C). We assume that the mantle on the ani- mal's left side is applied to the shell and causes its dissolution in this region, but we base this on anatomy of the animal re- moved from its shell rather than on direct observation. Layer 1 is dissolved first, at about 390°-400° at the 80% level (Figs. 2B and 3E) and further inward (420°-470°) anteriorly (Figs. 3 and 4A). Thinning of layer 2 begins immediately at the point of its exposure to the mantle; it completely disappears at FIG. 2. C. lividus. (A) Cross section of outer lip, showing 450°-495° (Figs. 3 and 4 B and C). Layer 3 then immediately crossed-lamellar crystal microstructure oflayer 1 at growing edge (left) begins to thin (Fig. 4C). Generally it does not completely dis- and layer 2 beginning on inner depositional surface (arrow). (Light appear, but some regions of inner whorls in the posterior third micrograph of etched, polished, gold-coated specimen; scale bar = consist of 4 The innermost 0.5 mm.) (B) Cross section at 80% level (Fig. 1), showing system of only layer (Fig. 3E). walls, consisting indicating position by degrees from outer lip and regions of thickening of layer 3 or 4 or both, remain patent throughout (Fig. 4D; gaps (0°-90°) and dissolution (380o°480'). (C) Cross section at 32%o level, in Fig. 2B are artifacts of preparation), but they are extremely showing spiral ridge and thickening of central columellar region, thin, often 35-50 Am (Figs. 1 and 2B). They presumably primarily by layer 3. (D) Cross section at 20%o level, showing columellar function to support the digestive gland, which fills all early thickening. (B-D, etched, polished, uncoated specimens; scale bars whorl space within the spire. = 5 mm.) (E) Cross section at 50% level, about 900 from outer lip, showing lamel structure and orientation in layers 1, 2, and 3. Outer As the Conus shell grows by helical progression of the outer shell surface is at top; inner or depositional surface is at bottom right. lip around the axis of coiling, the new growth covers all but the 1', width of primary lamel; 2', arrow indicates secondary lamels within most posterior part of the previous whorl. This results in a spire primary lamel; 3', arrows indicate edges oftertiary lamels on surface that, unlike the last whorl, is not covered by subsequent external of primary lamel. (Scanning electron micrograph of fractured, gold- deposition of shell, but remains exposed to attack by predators, coated specimen; scale bar = 0.05 mm.) boring organisms, and physical environmental stresses for the animal's entire life. because the primary lamels curve, the long axes of primary The thick shell in the spire (Fig.
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