Microstructural details in shells of the gastropod genera ... · interfaces and fractured sections...

$: Microstructural details in shells of the gastropod genera ... · interfaces and fractured sections of the shells using the JEOL JSM-6610LV (Germany) scanning electron microscope (SEM)$
Microstructural details in shells of the gastropod generaCarychiella and Carychium of the Middle Miocene

ADRIENNE JOCHUM, THOMAS A. NEUBAUER AND MATHIAS HARZHAUSER

Jochum, A., Neubauer, T. A. & Harzhauser, M. 2015: Microstructural details in shellsof the gastropod genera Carychiella and Carychium of the Middle Miocene. Lethaia,DOI: 10.1111/let.12134.

Microstructural details are revealed via scanning electron microscopy (SEM) in twocarychiid species from the early Middle Miocene of Styria, SE Austria. The proto-conchs of the shells of Carychiella eumicrum (Bourguignat 1857) and Carychiumgibbum (Sandberger 1875) show different types of microstructure on the embryonicshell during ontogeny. Total, superficial punctate structure on the shell of Carychi-ella eumicrum contrasts with the protoconch–teleoconch demarcation (p/t bound-ary) observed on the protoconch of Carychium gibbum. Both species exhibitaragonitic microstructure. Diagenetic effects, prismatic, homogeneous and crossedlamellar microstructures are detectible in both species. Rheomorphic folding anddense pitting within the columella of Carychiella eumicrum suggest a structure–function relationship for tensile strength and bulk weight reduction in carychiidsnails. We hypothesize that total superficial pitting on the shell of C. eumicum, seenhere for the first time in the Carychiidae, suggests paedomorphosis as a life-historystrategy to palaeoecological conditions of the Rein Basin during the early MiddleMiocene. □ Carychiella, Carychium, middle Miocene, mollusc assemblage, Rein Basin(Styria Austria), shell structure.

Adrienne Jochum [[email protected]], Naturhistorisches Museum derBurgergemeinde Bern, Bernastr. 15, Bern CH-3005, Switzerland Institute of Ecologyand Evolution, University of Bern, Baltzerstrasse 6, Bern CH-3012, Switzerland; ThomasA. Neubauer [[email protected]], and Mathias Harzhauser[[email protected]], Department of Geology and Paleontology, Natu-ral History Museum Vienna, Burgring 7, Vienna A-1010, Austria; manuscript receivedon 29/04/2014; manuscript accepted on 11/03/2015.

The Carychiidae represent a fascinating taxon of die-hard, terrestrial gastropods. Although it is assumedthey have a sketchy 330- to 300-million-year-old fos-sil record (Tracy et al. 1993; Bandel 1994), they arewell represented in the rich mollusc assemblages ofthe Neogene of Europe (Boettger 1870; Wenz 1923;Strauch 1977; Meijer 1986; Prisyazhnyuk & Stworze-wicz 1995; Stworzewicz 1999; Harzhauser & Kowalke2002; Bernor et al. 2004; Binder 2004; Harzhauser &Binder 2004; Harzhauser & Piller 2004; Frank 2006;Salvador 2015; Harzhauser et al. 2014a). As theCarychiidae are amongst the earliest gastropodgroups to have completed the transition from a mar-ine/estuarine habitat to a terrestrial mode of life,they provide a model for studying the adaptationsand ecology characterizing the radiation of terrestrialpulmonates (Barker 2001). The purpose of this studywas to examine and report discernible microstruc-tures found in carychiid fossils of this well-docu-mented mollusc assemblage of the early MiddleMiocene. In this study using SEM, we describe shellmicrostructures preserved in the two known cary-chiid species of the Rein Basin, Styria, SE Austria(Harzhauser et al. 2014a). This investigation is partof an ongoing search for ecological information and

potential new characters for phylogenetic analysis incongruence with recent molecular analyses of extantspecies (Weigand & Jochum 2010; Weigand et al.2011, 2012a,b, 2013) and fossil Carychiidae.

Carychium M€uller 1773, frequently dominatesmollusc assemblages and often characterizes com-munities, such as the ‘Carychium beds’ of the ViennaBasin (Jir�ıcek & Sene�s 1974; Bernor et al. 2004).Carychiidae are considered facies indicators formoist lakeshore habitats during the warm temperateto marginally tropical early Middle Miocene Bade-nian stage (Lueger 1981; Harzhauser & Kowalke2002). Extant Carychium inhabit shady, moist, inter-stitial layers of leaf, grass and wood litter of mesicenvironments in riparian zones, damp meadows,mountain forests and tropical woodlands. The Cary-chiidae show a Holarctic distribution (Pilsbry 1948;Morton 1955) and today comprise two genera: Cary-chium (epigean) and Zospeum (troglobitic).

Understanding the Carychiidae has as much to dowith carychiid evolutionary history, ontogeny, bio-chemistry and palaeoecology as with their reciprocalinfluences in the constructional morphology of theremarkably thin and translucent carychiid shell.Luchtel et al. (1997) emphasized that gastropod shell

DOI 10.1111/let.12134 © 2015 Lethaia Foundation. Published by John Wiley & Sons Ltd

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structure varies from species to species, and withineach species, distinctive details are specifically con-figured for general shape, pigment, mineral organi-zation and other features. Kano et al. (2008)observed that the smaller the snail’s body size, themore simplified anatomical structures become andthat a more specialized ecology is required to sustainit. Within the Ellobioidea, the degree of inner shellresorption varies within the different sub-families,whereby shell sculpture is considered most informa-tive at lower taxonomic levels and varies betweengenera (Martins 2007). To comprehend the Cary-chiidae and their role as baseline taxa in molluscanassemblages, it is essential to recognize and comparethe peculiarities of shell structure in both extant andfossil taxa. Although advanced assessment tech-niques such as X-ray diffraction (XRD), scanningelectron microscopy (SEM), nanocomputer tomog-raphy (NanoCT), transmission electron microscopy(TEM) and atomic force microscopy (AFM) havegiven many authors insight into the complex struc-ture of calcareous mollusc shells (Berman et al.1993; Hedegaard & Wenk 1998; Chateigner et al.2000; Hess et al. 2008; De Paula & Silveira 2009;Fr�yda et al. 2009; Furuhashi et al. 2009; Guzm�anet al. 2009; Vendrasco et al. 2010; Rodr�ıguez-Navar-ro et al. 2012; Hickman 2013), very few studies (Jo-chum 2011; Medakovi�c & Popovi�c 2012; Jochumet al. 2013) have been conducted at the microstruc-tural level on terrestrial ellobioid taxa. It is wellknown that environmental influences play a pivotalrole in shell mineralization and thus, influence shellform, development and repair (McMahon &Whitehead 1987; De Paula & Silveira 2009; Medak-ovi�c & Popovi�c 2012; Hickman 2013). As the Cary-chiidae inhabit semi-subterranean, subterranean andextreme subterranean habitats, some existing 980 mbelow the surface (Weigand et al. 2013), their shellsharbour a potential reservoir of valuable informa-tion.

Mollusc shells are polycrystalline complexes ofcalcium carbonate, diverse proteins rich in acidicamino acids and glycoproteins (Lowenstam & Wei-ner 1989; Berman et al. 1993; Hedegaard & Wenk1998). Gastropod and bivalve shells demonstrate acomparable range of shell mineralogy and micro-structure (Carter et al. 1998), whereby gastropodshells comprise an outer organic periostracal sheetand an inner carbonate layer (Saleuddin & Petit1983; Slapnik & Medakovi�c 2007). Their rigidity anddurability (texture) are governed by hierarchicallyorganized layered carbonates (Hickman 2013) in theform of calcite, aragonite and vaterite (rarest form)such that the fractions of minerals, grain morphol-ogy and aggregation and crystal orientation

comprise a microstructure identifiable and charac-teristic for specific taxa at the genus to family levels(Hedegaard & Wenk 1998; Fuchigami & Sasaki2005; Medakovi�c & Popovi�c 2012). Although knowl-edge of the structure and composition of the organiccomponents constituting the biominerals within thecrystalline composites has grown considerably, thatof their fossilization process is still sparse (Guzm�anet al. 2009). Moreover, the specificity of structuralorganization reflects structure–function relation-ships, which have recently become increasingly use-ful in designing models for material sciences(Ehrlich et al. 2011).

Our knowledge of mineralogy in the Carychiidaeis limited to three studies (Medakovi�c et al. 1999;Slapnik & Medakovi�c 2007; Medakovi�c & Popovi�c2012), whereby X-ray powder diffraction (XRD) wasused on Zospeum shells to investigate mineral com-position and phase fractions. A high concentrationof aragonite and a small fraction of calcite in theshells were detected. As calcite is a better insulatorthan aragonite, these authors attributed the calcitefraction to adaptation to the fluctuating tempera-tures in certain cave habitats. As very little is knownabout ellobioid, let alone extant or fossil carychiidmicrostructure, our investigation presents newinformation about the microstructure of the Cary-chiidae.

Carychiid taxonomy and systematics

As fossil and extant carychiid gastropods are knownto be highly morphologically variable (Watson &Verdcourt 1953; Strauch 1977; Burch & Van Dev-ender 1980; Stworzewicz 1999; Weigand & Jochum2010; Weigand et al. 2012a,b; Weigand et al. 2013),they have been subject to frequent taxonomic re-evaluation. Consequently, the plethora of forms hassystematically been shuffled and reshuffled into gen-era and sub-genera, based on the degree of characterexpression in shell size, shape, form, dentition, whorlnumber, whorl height and, most specifically, thedegree of sinuosity of the columellar lamella(Strauch 1977; Lueger 1981; Prisyazhnyuk & Stwor-zewicz 1995; Salvador 2015). For the herein treatedcarychiids, we follow the latest taxonomic and sys-tematic revisions of Miocene freshwater deposits byHarzhauser et al. (2014a,b). Although recent molec-ular analyses focusing on phylogenetic and phylo-geographical studies of extant Carychiidae haveanswered some profound questions regarding cary-chiid phylogeny (Weigand & Jochum 2010; Weigandet al. 2011, 2012a,b, 2013), shell microstructuralinvestigations of extant and fossil material are stillrequisite to support these studies in an integrative,

2 A. Jochum et al. LETHAIA 10.1111/let.12134

contemporary taxonomic approach (Jochum 2011;Jochum et al. 2013).

Faunal composition and palaeoecologicalsetting

Recently, Harzhauser et al. (2014a) performed acomprehensive survey on all mollusc fauna of theLake Rein (Fig. 1), including an up-to-date system-atic concept, critical synonymy lists, revisions ofmany taxa and descriptions of several new species.Along with the two species of Carychiidae comprisingthis present study, this work revealed a moderatelydiverse assemblage including 47 gastropod species(12 freshwater, 35 terrestrial) and one bivalve.

During the early Middle Miocene, the basin har-boured a geologically short-lived wetland withephemeral ponds, altogether referred to as LakeRein. More precise information on the palaeoenvi-ronment was recently inferred from the molluscfauna (Harzhauser et al. 2014a). These authorsemphasize that the freshwater molluscs comprise alarge number of pulmonate gastropods, indicating ashallow and stagnant water body with densely vege-tated banks and limited riverine influx. Moist wood-land habitats fringing Lake Rein are indicated bymost of the terrestrial taxa. The herein discussedcarychiids, Carychiella eumicrum (Bourguignat1857) and Carychium gibbum (Sandberger 1875),most likely settled the permanently moist to inun-dated habitats near the lakeshore.

Material and methods

The shell dimensions of Carychiella eumicrum rangefrom a height of 0.95 to 1.1 mm and a width of0.45 to 0.5 mm. The larger Carychium gibbumshows a height ranging from 1.40 to 1.45 mm anda width of 0.75 to 0.85 mm (Harzhauser et al.2014a).

Two microscopically well-preserved specimens ofCarychiella eumicrum (Bourguignat 1857) and sixspecimens with the exposed columella of Carychiumgibbum (Sandberger 1875) were selected andmounted on 13-mm aluminium pin stubs andcoated with gold–palladium in a sputter coater. Shellmicrostructures were examined on the shell surfaces,interfaces and fractured sections of the shells usingthe JEOL JSM-6610LV (Germany) scanning electronmicroscope (SEM) at the Natural History MuseumVienna (NHMW, Austria). In this study, we describethe preserved microstructures according to thenomenclature established by Gr�egoire (1972), Carter& Clark (1985) and Carter (1990). These descrip-tions were recently modified by G�enio et al. (2012)(Table 1).

We interpret carychiid shell microstructures anddiscernible textures using SEM images collated fromthe vast pool of literature spanning geological time-scales. We use the following abbreviations to desig-nate structures: Hom, homogeneous structure; Lam,laminar (tablet) structure; Le, lamellar structure; Li,

A

B

C

D

Fig. 1. A, political units of Austria. B, province of Styria with indication of studied region (grey area corresponds to the extension of theAlps). C, distribution of Miocene freshwater deposits in the marginal Styrian Basin and nearby intramontane basins. D, geological unitsof the Rein Basin with indication of localities mentioned in the text (main coal-mining area at the Tallak hill shaded). Maps modifiedafter Ebner & Gr€af (1979), Ebner (1983), Weber & Weiss (1983), Fl€ugel & Neubauer (1984), Sachsenhofer et al. (2003) and Harzhauseret al. (2012, 2014a,b).

LETHAIA 10.1111/let.12134 Middle Miocene shell microstructures 3

laminated structure; Gr, granular structure; and SP,simple prismatic structure.

The studied material is housed at the Natural His-tory Museum Vienna, Austria, under the collectionnumber NHMW 2012/0154.

Results

Descriptions of shell microstructures

Carychiella eumicrum (Bourguignat 1857) (Figs 2A–F, 3A–C, 5A, B): the outer layer of the shell showshomogeneous structure (Fig. 2F) consisting of gran-ular and shoal-like formations. Shallow semi-ellipti-cal pits are regularly distributed over the entire shellsurface. These pits show a generally granular, homo-geneous structure embedded by larger, aragonitic,rhomboidal laminate (RLi) tablets described by Car-ter (1990, p. 611) as ‘rods, laths, blades or tablets’(Fig. 2E, F). Faint transverse rheomorphic striationsintersperse the cavities and follow the curvature ofthe shell.

The region of dense calcium carbonate (Fig. 3A,B), constituting the columella at the second abapicalcolumellar fold, demonstrates an inner and outerlayer. The outer layer (Fig. 3B) is composed of sim-ple prismatic laminar shell microstructure. At thehomogeneous, horizontal interface between the twolayers (Fig. 3B), individual crystals show prismaticrhomboidal and tabular form. The curvature of theinner layer shows strongly diagenetically alteredcrossed lamellar structure abutting a region of diage-netically altered simple prismatic microstructure.The surrounding structure (Fig. 3B, right side) isprismatic, but the exact underlying morphology isdifficult to ascertain.

The ventral surface (Fig. 3A) of the columellaencompassing the second abapical columellar fold is

densely punctate. A pattern of regular pits (Fig. 3C)is located on the planar surface emanating from theinterface of the outer, columellar shell layer.

By close inspection of the pitted rheomorphicfolds, still smaller equidistantly arranged, distinctpinprick-like pores symmetrically pock a series ofnon-joining segments of a lightly discernible track-like pattern of horizontal meshwork. These non-fibrillar (at least with SEM) ‘caterpillar feet-like’tracks are co-marginally concentrated on the mid-outermost section of the shell fracture. They demon-strate an irregular pattern. Although no reference tothese tracks in other molluscs is found in the litera-ture, they do not resemble growth lines or micro-structural details described by previous authors. Wespeculate this pattern is due to a Middle Miocenebacterium, fungus, parasite or commensal inter-loper. From a constructional perspective, the irregu-lar positioning of these peculiar microstructuressuggests no function–structure relationship.

The strongly diagenetic deteriorated outer layer ofthe ventral side of the columella is comprised ofhomogeneous structure, whereby a nacreous ‘arago-nitic laminar structure consisting of polygonal torounded tablets arranged in a regularly formed, par-allel sheet’ (Carter & Clark 1985, p. 55) can be dis-cerned. Laminate laths and tablets loosely flank theperimeters of this structure.

Carychium gibbum (Sandberger 1875) (Fig. 4A):The surface structure of C. gibbum reveals a differentmorphology than Carychiella eumicrum. The proto-conch and, in a few cases, the early teleoconch(Fig. 4B) are marked by the regular pattern of char-acteristic carychiid punctation (Jochum 2011; Jo-chum et al. 2013). In contrast to Carychiellaeumicrum, the second protoconch whorl bears theclear line indicating the demarcation zone of larvaltorsion and the reorganization of shell secretionbetween the protoconch and teleoconch (the p/t

Table 1. Modified definitions by G�enio et al. (2012) of shell microstructure from Carter (1990).

Microstructure Description

Simple prismatic (SP) First-order prisms that show low-to-moderate length–width ratios: individual first-order prisms lackfan-like arrangements of their second-order structural subunits; the boundaries between adjacentsimple prisms are generally well defined

Nacreous Polygonal to round aragonitic tablets arranged in broadly continuous, regular, mutually parallellaminae, by definition, this structure is always aragonitic

Homogeneous (Hom) More or less equidimensional, irregularly shaped crystallites or crystal morphotypes lacking clearfirst-order structural arrangement except for possible accretion banding

Crossed lamellar (CL) First-order lamellae of thin mutually parallel laths or rods, with two non-horizontal dip directions oftheir elongate sub-units in adjacent lamellae. The structure is co-marginal, if the first-order lamellaeare parallel to the shell margin, radial if perpendicular

Complex crossed lamellar (CCL) Crossed structure with three or more non-vertical dip directions of other elongate structural units.It differs from crossed lamellar in that the largest sub-units are not concentrically elongate first-orderlamellae but are much less regular and more variable in form

Intersected cross-platy A crossed structure with only two predominant dip directions in which the first-order lamellaeconsist of short, rhomboidal platy crystallites


boundary) (Hickman 2013). This significant featurewas observed only in one specimen of Carychiella e-umicrum from this assemblage.

The edge of the fractured teleoconch (Fig. 4A, C–F) shows discernible microstructure of Carychium

gibbum. Revealed is a plane of tabular aragoniteprism comprised of vertical crystalline sub-unitsconstituting the simple prismatic laminar shellmicrostructure on the inner marginal side of theshell (Fig. 4C, E, F). Below this layer is a stratum of

HomHom

Hom

RLi

RLi

RLiStr

A B

C D

E F

Fig. 2. SEM images of Carychiella eumicrum (Bourguignat 1857). A–F, shell with total superficial punctate structure. A, ventral view ofshell. B, punctate ultimate whorl. C, bulbous protoconch with punctate structure. D, regular pattern of semi-elliptical pits and diageneticrubble. E, contextual view of shell and pit morphology showing RLi, rhomboidal- and blade-shaped nacreous laminate tablets; Hom,shoal of granular homogeneous structure initiating depth of pit mixed with diagenetic rubble; and Str, rheomorphic transverse striations.F, close-up view of RLi, rhomboidal- and blade-shaped nacreous laminate tablet, concave to the shoal of Hom, homogeneous shell struc-ture; granular and diagenetic homogenous structure surrounds the pit.


homogeneous structure marked by a bifurcatedribbon of potential accretion banding (Fig. 4C). Asthis banding oddly bifurcates and is oblique to theshell growth surfaces, it could possibly be organicmaterial attached to the fossil shell surface. Slightlydiscernible, co-marginal crossed lamellar micro-structure of thin, mutually aligned laths or lamellaeare arranged parallel to the point of bifurcation ofthe aforementioned banding. At the endpoint of theaccretion banding ribbon is an isolated, superim-posed ropey structure of mineral sheets built up oflaths (Fig. 4C, D). These laths show a regularity ofcrystal thickness in an arrangement of successivesheets of obliquely aligned crossed lamellar structuresurrounded by homogeneous structure and diage-netic rubble (Fig. 4D).

A second fractured shell of C. gibbum provideda clearer and different perspective of microstruc-tures at approximately the same region along theedge of the shell (Fig. 4E–F). This specimen showssheets of simple prismatic structure merging intomicrostructure described by Hedegaard (1997, fig.6) as ‘first order lamellae perceived as irregularaggregates of intergrown pieces of simple crossedlamellar structure’. Cliffs of simple prismatic struc-ture border a zone of either crossed lamellar struc-ture or an interface of continuation of the simpleprismatic layer with variable diagenetic alterationbelow (Fig. 4E). The crossed lamellar structureshows different orientation of the cleavage planes(Fig. 4E).

Simple prismatic structure is indicated by a planeof tabular crystal aragonite (Fig. 4F). C. gibbum herepresents Hedegaard’s (1997) aforementioned com-plex of crossed lamellar structure at the inner shellmargin. Additionally, transverse jagged sheets ofcross-lamellar structure (Fig. 4F) superficiallyresemble those described by Chateigner et al. (ICP,fig. 7b, 2000) for intersected cross-platy structure. Astar-like complex of acicular bodies is embedded in amass of diagenetic rubble (Fig. 4F). It is not clearwhether this formation is due to intrinsic prismaticarrangement, whether the bodies are themselves ar-tefacts or whether these structures comprise a con-stellation of randomly assembled prisms amassed indiagenetic rubble.

A regular pattern of wedge-shaped planes of ara-gonitic structure (Fig. 5A–D) is present in differentdensities on the columellar lamellae of both species.This structure has been consistently observed on thecolumellar lamellae in extant Carychiidae and likelyaids in traction during mobility (Jochum 2011; Jo-chum et al. 2013).

A

B

C

SP

SP

CLLam

Lam

Lam Hom

CL

Hom

PStr

PpTr

Fig. 3. SEM images of columellar structure of Carychiella eumi-crum (Bourguignat 1857). A, contextual view of interior of colu-mella showing SP, simple prismatic structure at the inner shellmargin; CL, laths of crossed lamellar structure eroded by diage-netic alteration; Hom, homogeneous structure; PStr, punctatestructure on ventral interface. B, close-up view of SP, diageneti-cally altered simple prismatic structure; Lam, nacreous aragoniticlaminar structure; CL, underside of fracture showing laths ofcrossed lamellar structure eroded by diagenetic alteration; C,ventral interface of columellar fracture showing PpTr, fine pin-prick tracks on rheomorphic folds of planar surface of PStr,punctate structure (tensile function?) on ventral interface; Lam,nacreous laminate laths and tablets intersected by homogeneousstructure.


Discussion

Protoconch morphology and structure

Strauch (1977) reported that one of five known spe-cies of the genus Carychiella is usually found in

European fossil biotopes inhabited concurrently byone to three Carychium or Saraphia species. Ourinvestigation here agrees with this finding in thatCarychiella eumicrum was found inhabiting thesame biotope with the larger Carychium gibbum.Moreover, although no direct phylogenetic relation-ship was determined within the few fossil forms

edge

P/t

P/t

SP

SP

SP

SP

CLCL

ACC

CL

DR

DR

HomCL

CL CL

ACCB

pits

A B

C D

E F

Fig. 4. SEM images of Carychium gibbum (Sandberger 1870–1875). A, shell showing inspection zones. B, characteristic carychiid protoconchpitting and protoconch–teleoconch (p/t) boundary of larval reorganization C, shell fracture showing ACCB, accretion banding of homoge-neous structure; SP, simple prismatic structure at the inner shell margin and CL, superimposed mineral sheets of crossed lamellar structure.D, shell fracture (rightmost section of C) in context showing regularity of thickness of CL laths; Hom, homogeneous structure and DR, dia-genetic rubble. E, SP, simple prismatic structure at the inner shell margin; CL, crossed lamellar layer. F, tabular forms of Sp, simple prismaticstructure; CL, transverse sheets of intergrown, crossed lamellar structure; ACC, acicular crystal arrangement in diagenetic rubble.


representing Carychiella in his investigations,Strauch (1977) hypothesized that Carychiella mostplausibly originated from a common ancestor stem-ming from the Oligocene (33.9–23 Mya).

Although comparable morphological analyses ofCarychiella eumicrum (Bourguignat 1857) (Fig. 2A)are documented by Strauch (1977, pl. 14, fig. 13)and Prisyazhnyuk & Stworzewicz (1995) from Opole(Poland), Stworzewicz (1999, fig. 5–6) fromBełchat�ow (Poland) and Tucho�rice (Czech Repub-lic), and Salvador (2015, fig. 1) from Sandelzhausen,Mainburg (Germany) (2013, fig. 1), the specimensexamined here and presented by Harzhauser et al.(2014a, 2014b), pl. 6, fig. 5) differ significantly inthat the entire shell is densely punctate beyond theprotoconch (Fig. 2B, C). This total pitting of theshell is a structural feature new to both fossil andrecent Carychiidae.

Superficial semi-ellipsoidal pitting (Fig. 2D) hasbeen consistently observed in the protoconch ofextant Carychiidae (Jochum 2011; Jochum et al.2013) as well as in the protoconch of Carychium

gibbum here (Harzhauser et al. 2014a,b) (Fig. 3A).Stworzewicz (1999) observed pitting on the proto-conch of Carychium rhenanum (Strauch 1977)although Strauch (1977) did not describe this featurein this species nor in any other in his extensiveanalysis of Miocene carychiids. Moreover, Stworze-wicz (1999) equally did not report similar finds onthe shells of Carychiella eumicrum material sheexamined from Bełchat�ow, Opole or Tucho�rice. Onthe other hand, and contrary to these observations,it is notable that Harzhauser et al. (2014b) recentlyfound punctate microstructure on the protoconchand early teleoconch of shells of C. eumicrum fromTucho�rice.

The pronounced, globular protoconch (Fig. 2C)of Carychiella eumicrum (Harzhauser et al. 2014a,b;pl. 6, figs 5, 6), although not uncommon to lesserdegrees for extant Carychiidae, is indicative of onto-genetic development derived from a large egg con-taining a large yolk supply (Lima & Lutz 1990). Doll(1982) and Bulman (1990) confirm that the egg cap-sule of extant Carychium tridentatum (Risso 1826) is

Wss

Wss

Wss

A B

C D

Fig 5. SEM images of Wss, wedge-shaped aragonitic structure. A, B, columellar lamella of Carychiella eumicrum (Bourguignat 1857). C,D, columellar lamella of Carychium gibbum (Sandberger 1870–1875).


‘gigantic’ compared to the adult, encompassingabout one-fifth the maximal length of the adult shell(Doll 1982). This observation holds equally well forthe relationship of protoconch to adult shell lengthin Carychiella eumicrum here (Fig. 2A). Together,these two structural features are striking in that theyfail to consistently demonstrate the usual proto-conch–teleoconch boundary (the p/t boundary),indicating when hatching occurred during the het-erotectonic constructional processes of shell secre-tion (Hickman 2013). This line is associated withlarval reorientation and the accompanying ontoge-netic shift in shell morphology during metamorpho-sis. The p/t boundary, however, is well marked onthe shells of Carychium gibbum (Fig. 3A–B). A likelysimilar constructional transition was reported on theshells for Carychiella puisseguri (Truc 1972) of theEarly Pliocene from Celleneuve (H�erault), France(Strauch 1977). Our observations suggest a partialdevelopmental and/or transitory stage for the genusCarychiella of the Lake Rein.

Shell microstructure

Microstructure in molluscs is characterized by themorphology of crystal units and their mode of ori-entation and layering arrangement. The most com-mon extant shell microstructures (spheruliticprismatic, crossed lamellar, nacre and foliated cal-cite) are known since the Middle Cambrian (Runne-gar 1985; Vendrasco et al. 2010). Carter (1979)detected microstructural similarities in brachiopodsand mollusc shells, suggesting a similarity in biomin-eralization processes which may have derived froman early common ancestor (Vendrasco et al. 2010).

Five terms describe the different levels of crystalaggregation in molluscan shell microstructures:homogeneous, prismatic, spherulitic (grained),crossed lamellar and complex crossed lamellar(Gr�egoire 1972; Carter 1990; Chateigner et al. 2000).Carter (1990) referred to microstructural modes ofcrystal aggregations as ‘rods, tablets, laths andblades’. Simple crossed lamellar structures are com-monly found in gastropods and are always aragonitic(Bøggild 1930; Taylor et al. 1969; Carter 1990;Hedegaard 1990; G�enio et al. 2012). Crossed lamel-lar calcite is known in some patellogastropods(Fuchigami & Sasaki 2005).

The pits and the surrounding superficial surfaceof Carychiella eumicrum (Fig. 2E, F) present a rubblyhomogeneous structure (Fig. 2E, F). The tabular ele-ments of C. eumicrum here are morphologically sim-ilar to the laminate, rhombic type, aragoniticnacreous tablets (Taylor & Weeden 2000; Vendrascoet al. 2010) observed on imprints of internal moulds

of Mellopegma georginensis (Runnegar & Jell 1976)from the Middle Cambrian of Australia (Vendrascoet al. 2010; pl. 1, fig. 10). These tablets within thepits of C. eumicrum are rhomboidal- and bladeshaped (Fig. 2E, F), suggesting similarity with thenacre tablet forms known in extant bivalves (Tayloret al. 1969; fig. 10, Pinctada margaritifera; Wada1972; fig. 8, Pinna attenuata) and from fossilsdescribed by Vendrasco et al. (2010, text-fig. 4E–J)dating from the Middle Cambrian. Additionally, themoderately advancing homogeneous wave of struc-ture initiating the depth of each pit (Fig. 2E) sug-gests a merging of tabular structure as described byVendrasco et al. (2010, fig. 4H–J).

The microstructure comprising the outer surfaceof the columella (Fig. 3A, B) of Carychiella eumi-crum consists of simple prismatic structure. Theinterior, crossed lamellar structures show the ‘plate-like elongated aspect’ of lamellae described for Conusomaria by Rodr�ıguez-Navarro et al. (2012, fig. 1E,F).

The regular punctate microstructure observed atthe lower ventral face of the Carychiella eumicrumcolumella (3A, C), just below the second abapicalcolumellar fold, is reminiscent of similar superficialpock-like structures found on shells of brachiopodsand diverse molluscs. War�en & Gofas (1996, fig. 5a)reported external pitting in the monoplacophoranVeleropilina reticulata. Vendrasco et al. (2010)described a pattern of regular pitting structure onthe interior surface of the shell in Figurina specimens(pl. 4, fig. 8) and in specimens of Corystos thorntoni-ensis (Pl. 5, figs. 7–8) from the Middle Cambrian.These authors attributed this punctate morphologyto either an accelerated rate of organic matrix degra-dation in relation to the dissolution of shell structureor to shell diagenesis. For Carychiella here, wehypothesize with Jochum (2011) that a function–structure relationship, similar to that carried by tra-becular bone in vertebrate skeletons, is an intrinsicelement of design. The vast network of pores mostplausibly serves to underscore shell strength whilereducing shell weight during the unwieldy, semi-rotary manoeuvering of the carychiid snail in action.In addition, the densely pitted microstructure mostlikely enhanced tensile strength in the columella ofCarychiella eumicrum during the tractional exertionof the columellar muscle on the columella. More-over, it can be assumed that Carychiidae from theMiddle Miocene manoeuvered in the same charac-teristic, semi-rotational jerking movements observedin extant species when they circumvent obstacles orenter tight crevices in wood or rocks.

Our SEM analyses suggest that homogeneousmicrostructure is prevalent in both carychiid species.


Carter & Clark (1985, p. 63) defined this seeminglyamorphous structure as ‘aggregations of more or lessequidimensional, irregularly shaped crystallites lack-ing clear first-order structural arrangement exceptfor possible accretion banding’. Irregularly shapedcrystallites are present on the protoconch of Carychi-ella eumicrum, while a large ribbon of accretionbanding is clearly visible on the shell fracture ofCarychium gibbum. Although accretion banding hasoften been observed in extant Carychiidae (Jochumpersonal observation), it is not necessarily an ele-ment of repair but rather an ‘extra’ manifestation ofconchiolin fabric. The mechanisms responsible forwhy and where it appears are not yet clear.

The ‘intersected cross-platy’ variety of crossedlamellar microstructure may be demonstrated byC. gibbum here (Fig. 4F). This form, however, isperplexing in that a microstructural consensus is dif-ficult to reach with SEM here. For example, trans-verse jagged sheets of crossed lamellar structureresemble those described for ‘intersected cross-platy’reported by Chateigner et al. (2000, ICP, fig. 7b).Hedegaard (1990), on the other hand, observed thismicrostructure only in vetigastropods. Chateigneret al. (2000) found it to be identical to the ‘Type IIcrossed lamellar structure’ reported by Batten(1975). Methods such as TEM or the implementa-tion of a wider sample basis from the same facies ofLake Rein would shed more light on this type of CLmicrostructure.

Small shell size and paedomorphosis inCarychiella

The minute (max. 1.1 mm shell height), completelypunctate shell of Carychiella eumicrum, suggests apaedomorphic life strategy. To understand the sig-nificance and singular context of paedomorphismand small body size in C. eumicrum, a cursory dis-cussion of the literature is necessary.

Paedomorphosis involves the heterochronic pro-cess by which descendants resemble the juveniles oftheir ancestors (Bhullar et al. 2012). It is a frequentmechanism of phenotypic change (Gould 1977;McNamara 1997), whereby larvae do not completemetamorphosis and individuals reach sexual matu-rity while retaining a larval morphology. Paedo-morphosis is largely driven by ecological factors(Diz et al. 2012; Bonett et al. 2013). Moreover,paedomorphosis via progenesis promotes earlysomatic maturation and an abbreviated ontogeny(Bhullar et al. 2012). Although small size alonedoes not result in paedomorphic morphology, ithas factored in discussions about the evolution ofpaedomorphosis (Bhullar et al. 2012; Diz et al.

2012). For example, if tininess of C. eumicrum(and all Carychiella species) promoted increasedsurvival by wedging into tight crevices to avoidpredation or desiccation in extreme environmentalsituations, then an apparent trade-off may haveencompassed their avoidance in reaching the mini-mum possible size/age for sexual maturation. Thus,in this context, a selective pressure favouring a shifttowards paedomorphosis via progenesis is plausible(Diz et al. 2012). In a recent model, Edeline et al.(2013) observed that warming-induced body down-sizing (Bergmann’s rule and the temperature-sizerule) was a primary determinant of life-historytrends in river fish spanning decades and encom-passing 52 species. These authors determined thatinterspecific competition favoured small body sizeand that this played an advantageous role in highdiversity communities. In the light of Harzhauseret al. (2014a,b) survey depicting the diverse assem-blage of 47 gastropod species of the Lake Reinenvironment, Carychiella eumicrum factors specifi-cally, with the larger member of the genus Carychi-um, Carychium gibbum as a potential competitor inthis context.

Paedomorphosis, on the other hand, has beenfound to be reversible over relatively long time inter-vals (i.e. millions of years) in a recent phylogeneticstudy of spelerpine salamanders, suggesting thatmetamorphosis and adult traits can re-evolve afterbeing evolutionarily lost (Bonett et al. 2013).Hereby, genes were found to counteract time byassuming alternate functions.

Paedomorphosis also occurs in small-sized, vent-seep bathymodiolin mussels found at organic falls(G�enio et al. 2012). The bathymodiolin genus Idas isknown from wood and whale-falls dating from theEocene to Miocene (Amano & Little 2005). In thelight of their extreme habitat status, Idas favours atransitory, ephemeral lifestyle much like the extantterrestrial Carychiidae (i.e. Zospeum in caves, Cary-chium in semi-subterranean habitats). G�enio et al.(2012) hypothesize that the small size of Idas maywell reflect an adaptation to ephemeral habitats thatdisappear in a few months or a few years. Theseauthors attribute the evolution of paedomorphicforms to the distinct ecological selective pressures atorganic falls such as space limitation, communityproductivity and ephemeralism. Truncated lifespans,accommodated by a trade-off of resource allocationduring early development, would likely favourreproduction rather than growth. In agreement withOckelmann & Dinesen (2011) and G�enio et al.(2012), it is plausible that ‘a short generation timeand small population size are preconditions for thepossibility of an accelerated evolution’. Specifically,


Carychiella eumicrum likely represents this scenariofor Lake Rein.

As this study revealed the only known carychiid tomorphologically suggest paedomorphosis, furtherinvestigation of other fossil assemblages containingCarychiella species may reveal more occurrencesfrom the Neogene. The question remains openwhether the observed microstructural aspects andprotoconch form of C. eumicrum are indicatory of apotential transitory stage of C. eumicrum formsknown from Bełchat�ow, Opole, Tucho�rice and San-delzhausen. In this context, it is interesting thatStrauch (1977) observed C. eumicrum finds fre-quently associated with other, larger Carychiella spe-cies at different geological periods: Miocene(eumicrum, crossei) and Pliocene (marinae, puisseg-uri). Strauch (1977) also observed apparent construc-tional transitions on the shells of C. puisseguri (Truc1972) of the Early Pliocene from Celleneuve. A con-temporary investigation emphasizing morphologicaland anatomical studies of Carychiella’s proposedclosest extant relative, Carychium sibiricum (Westerl-und 1897) (Strauch 1977; Stworzewicz 1999), couldwell reveal valuable, ecologically contextual informa-tion in this smallest of extant epigean Carychiidae.

Shell morphology reflects ecology

Constructional shifts in shell morphology, such asthe p/t boundary observed in Carychium gibbum,often correlate with ecological transitions duringontogeny (Jackson et al. 2007; Hickman 2013). Inaddition, as similar shell ornamentation in the Cary-chiidae may reflect similar shifts in gene expressionprofiles (Gr�egoire 1972), shell structure may showsimilar gene regulatory transitions in response toecological and functional requirements (Jacksonet al. 2007; Hickman 2013).

Mechanisms influencing fossil and extant terres-trial gastropod shell structure are manifold. Lessapparent but none the less influential for shell struc-ture are those involving cross-ecosystem interactionssuch as species-specific coupling of plants with soilin extant and paleobiotic communities. Plant speciesinfluence the soil biota, including carychiid snails,via changes in the quality and quantity of organicmaterial entering the substrate (Bardgett & Wardle2010). Ions used for biomineralization are derivedfrom the diet or directly from the environment(Weiner 2008), whereby the onset of shell minerali-zation may be correlated to feeding requirements(Eyster & Morse 1984). As extant carychiid speciesdemonstrate a marked affinity towards specific plantcommunities (Morton 1955; Lo�zek 1957), and plantcommunities and species preferentially select for

decomposer communities that most effectively min-eralize their own litter (Wardle 2002; Ayres et al.2006, 2009; Vivanco & Austin 2008; Strickland et al.2009), it is fundamental to consider this relationshipin the light of direct biochemical influences exertedin the individual mineralization of shells as well as inthe subsequent taphonomic processes of both Cary-chiella eumicrum and Carychium gibbum facies.

Conclusions

The presented data provide additional evidence thatshell microstructures are similar (i.e. within similarmorphotypes) throughout diverse molluscan groupsthrough geological time (Runnegar 1985; Vendrascoet al. 2010). This study reveals instances of consis-tency with extant Carychiidae such as pitting on theprotoconch and wedge-shaped planes of aragoniticstructure on the columella in fossils of two carychiidgenera from the Middle Miocene. The Carychiidaeof the Lake Rein show similar microstructures andtextures in the same parts of the shell of differentgenera. Our SEM images show the most commoncrystallographical aragonitic microstructural unitsaccording to Carter (1990). These structures includehomogeneous, simple prismatic and crossed lamellarstructure. However, we conclude that although SEMis effective in detecting these structure types, it is notsufficient enough to reveal finer structural relation-ships such as crystallographical texture in fossil cary-chiid shells. Also, as mineralogical diageneticalteration is highly variable within a single layer offossil shell structure, mineralogy and chemical com-position (Barskov et al. 1997; Guzm�an et al. 2009),more carychiid shells would need to be investigatedfor palaeoecological reconstructions based on thesestructures for the Lake Rein. As the organic matrixof the periostracum provides a key source of ontoge-netic and ecological information setting Carychiellaeumicrum of Lake Rein apart, future research usingX-ray diffraction of shell tissue and TEM investiga-tions of the periostracal layer would greatly augmentthese studies. Carychiella eumicrum specifically rep-resents a highly context-dependent dynamic forwhich ontological, biochemical, genetic and ecologi-cal interactions at many different levels contributedto producing either: (1) an ecophenotype capable ofexploiting a potentially novel and extreme habitat;or (2) it represents an autapomorphic condition (i.e.character state derived via natural selection) inancient carychiid phylogeny.

As protoconch pitting has been consistentlyobserved in microstructural investigations of recentCarychiidae, including the troglobitic genus Zospe-


um (Jochum 2011; Jochum et al. 2013), it can beassumed that this frequent ellobioid microstructuralcharacteristic (Martins 2007) appears more fre-quently in the fossil record than reported thus far.More importantly, this consistency within the Cary-chiidae suggests that pitting is a microstructuralcharacter demonstrating low phenotypic plasticityand thus reflects evidence of strong genetic controlin both extant and fossil species. In addition, as pre-vious investigations (Strauch 1977; Prisyazhnyuk &Stworzewicz 1995; Stworzewicz 1999) predate con-temporary technological refinements, the degrees oftechnological advancement (SEM in this case) aswell as the preservation potential of the shell havemuch, if not all, to do with this discrepancy. Up tonow, five records show pitting on the protoconchand early teleoconch of the shells of fossil Carychii-dae dating from the Miocene. These include Carych-ium rhenanum (Strauch 1977) (from Bełchat�ow)and Harzhauser et al.’s (2014b) observations inspecimens of Carychiopsis schwageri (Reuss 1868),Carychiopsis prisyazhnyuki (Stworzewicz 1999),Carychiella eumicrum (Bourguignat 1857) (fromTucho�rice) and Carychium gibbum (Sandberger1875) (from Lake Rein). Only one carychiid, Cary-chiella eumicrum (Bourguignat 1857) (from LakeRein) is known to possess total shell punctation.Two of these records document two genera from theLake Rein.

Lastly, in a second line of consideration, as recentCarychiidae demonstrate a wide spectrum of mor-phological and intraspecific variability (Winslow1922; Zimmermann 1925; Bulman 1990; Nekola &Barthel 2002; Weigand et al. 2012a,b), reflectingconditions such as phenotypic plasticity, that is thephenotypic response of an organism to fluctuatingenvironmental conditions (Trussell 1996; Hollander& Butlin 2010; Weigand et al. 2013), it can beassumed that fossil Carychiidae, comprising theseNeogene assemblages, responded phenotypically inthe same manner to paleoenvironmental circum-stances. Hence, the multitude of carychiid fossil sub-genera and the diversity of fossil species assigned tothem most likely well reflect the same skeweddynamic. Subsequently, a falsely sufficient and mis-leading understanding of species comprising theseNeogene assemblages is likely. Work discussing thebroad spectrum of morphological and intraspecificvariability in extant Carychiidae is currently in pro-gress.

Acknowledgements. – We thank Dan Topa for his expertise withthe SEM at the NHMW. We also thank Angel Diz, Robert Hersh-ler, Carole Hickman and Silvia de Paula for their expedient helpin literature acquisition. Special gratitude goes to Timo Noackfor technical help with the image processing. This research

received support from the SYNTHESYS Project http://www.syn-thesys.info/, which is financed by the European CommunityResearch Infrastructure Action under the FP7 ‘Capacities’ Pro-gram. It contributes to the FWF-project P 25365–B25 ‘Freshwa-ter systems in the Neogene and Quaternary of Europe: Changesin gastropod biodiversity, provinciality, and faunal gradients’.We are grateful to David Reid and Luciana G�enio for their con-structive input, the anonymous reviewers and the editor, PeterDoyle, who provided valuable suggestions for improving thequality of the article.

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Microstructural details in shells of the gastropod genera ... · interfaces and fractured sections...

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