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Microstructural Details in Shells of the Gastropod Genera Carychiella and Carychium of the Middle Miocene

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Microstructural Details in Shells of the Gastropod Genera Carychiella and Carychium of the Middle Miocene Microstructural details in shells of the gastropod genera Carychiella 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 shells of 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 two carychiid species from the early Middle Miocene of Styria, SE Austria. The proto- conchs of the shells of Carychiella eumicrum (Bourguignat 1857) and Carychium gibbum (Sandberger 1875) show different types of microstructure on the embryonic shell 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 exhibit aragonitic microstructure. Diagenetic effects, prismatic, homogeneous and crossed lamellar microstructures are detectible in both species. Rheomorphic folding and dense pitting within the columella of Carychiella eumicrum suggest a structure– function relationship for tensile strength and bulk weight reduction in carychiid snails. We hypothesize that total superficial pitting on the shell of C. eumicum, seen here for the first time in the Carychiidae, suggests paedomorphosis as a life-history strategy to palaeoecological conditions of the Rein Basin during the early Middle Miocene. □ Carychiella, Carychium, middle Miocene, mollusc assemblage, Rein Basin (Styria Austria), shell structure. Adrienne Jochum [[email protected]], Naturhistorisches Museum der Burgergemeinde Bern, Bernastr. 15, Bern CH-3005, Switzerland Institute of Ecology and Evolution, University of Bern, Baltzerstrasse 6, Bern CH-3012, Switzerland; Thomas A. 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 received on 29/04/2014; manuscript accepted on 11/03/2015. The Carychiidae represent a fascinating taxon of die- potential new characters for phylogenetic analysis in hard, terrestrial gastropods. Although it is assumed congruence with recent molecular analyses of extant they have a sketchy 330- to 300-million-year-old fos- species (Weigand & Jochum 2010; Weigand et al. sil record (Tracy et al. 1993; Bandel 1994), they are 2011, 2012a,b, 2013) and fossil Carychiidae. well represented in the rich mollusc assemblages of Carychium Muller€ 1773, frequently dominates the Neogene of Europe (Boettger 1870; Wenz 1923; mollusc assemblages and often characterizes com- Strauch 1977; Meijer 1986; Prisyazhnyuk & Stworze- munities, such as the ‘Carychium beds’ of the Vienna wicz 1995; Stworzewicz 1999; Harzhauser & Kowalke Basin (Jirıcek & Senes 1974; Bernor et al. 2004). 2002; Bernor et al. 2004; Binder 2004; Harzhauser & Carychiidae are considered facies indicators for Binder 2004; Harzhauser & Piller 2004; Frank 2006; moist lakeshore habitats during the warm temperate Salvador 2015; Harzhauser et al. 2014a). As the to marginally tropical early Middle Miocene Bade- Carychiidae are amongst the earliest gastropod nian stage (Lueger 1981; Harzhauser & Kowalke groups to have completed the transition from a mar- 2002). Extant Carychium inhabit shady, moist, inter- ine/estuarine habitat to a terrestrial mode of life, stitial layers of leaf, grass and wood litter of mesic they provide a model for studying the adaptations environments in riparian zones, damp meadows, and ecology characterizing the radiation of terrestrial mountain forests and tropical woodlands. The Cary- pulmonates (Barker 2001). The purpose of this study chiidae show a Holarctic distribution (Pilsbry 1948; was to examine and report discernible microstruc- Morton 1955) and today comprise two genera: Cary- tures found in carychiid fossils of this well-docu- chium (epigean) and Zospeum (troglobitic). mented mollusc assemblage of the early Middle Understanding the Carychiidae has as much to do Miocene. In this study using SEM, we describe shell with carychiid evolutionary history, ontogeny, bio- microstructures preserved in the two known cary- chemistry and palaeoecology as with their reciprocal chiid species of the Rein Basin, Styria, SE Austria influences in the constructional morphology of the (Harzhauser et al. 2014a). This investigation is part remarkably thin and translucent carychiid shell. of an ongoing search for ecological information and Luchtel et al. (1997) emphasized that gastropod shell DOI 10.1111/let.12134 © 2015 Lethaia Foundation. Published by John Wiley & Sons Ltd 2 A. Jochum et al. LETHAIA 10.1111/let.12134 structure varies from species to species, and within comprise a microstructure identifiable and charac- each species, distinctive details are specifically con- teristic for specific taxa at the genus to family levels figured for general shape, pigment, mineral organi- (Hedegaard & Wenk 1998; Fuchigami & Sasaki zation and other features. Kano et al. (2008) 2005; Medakovic & Popovic 2012). Although knowl- observed that the smaller the snail’s body size, the edge of the structure and composition of the organic more simplified anatomical structures become and components constituting the biominerals within the that a more specialized ecology is required to sustain crystalline composites has grown considerably, that it. Within the Ellobioidea, the degree of inner shell of their fossilization process is still sparse (Guzman resorption varies within the different sub-families, et al. 2009). Moreover, the specificity of structural whereby shell sculpture is considered most informa- organization reflects structure–function relation- tive at lower taxonomic levels and varies between ships, which have recently become increasingly use- genera (Martins 2007). To comprehend the Cary- ful in designing models for material sciences chiidae and their role as baseline taxa in molluscan (Ehrlich et al. 2011). assemblages, it is essential to recognize and compare Our knowledge of mineralogy in the Carychiidae the peculiarities of shell structure in both extant and is limited to three studies (Medakovic et al. 1999; fossil taxa. Although advanced assessment tech- Slapnik & Medakovic 2007; Medakovic & Popovic niques such as X-ray diffraction (XRD), scanning 2012), whereby X-ray powder diffraction (XRD) was electron microscopy (SEM), nanocomputer tomog- used on Zospeum shells to investigate mineral com- raphy (NanoCT), transmission electron microscopy position and phase fractions. A high concentration (TEM) and atomic force microscopy (AFM) have of aragonite and a small fraction of calcite in the given many authors insight into the complex struc- shells were detected. As calcite is a better insulator ture of calcareous mollusc shells (Berman et al. than aragonite, these authors attributed the calcite 1993; Hedegaard & Wenk 1998; Chateigner et al. fraction to adaptation to the fluctuating tempera- 2000; Hess et al. 2008; De Paula & Silveira 2009; tures in certain cave habitats. As very little is known Fryda et al. 2009; Furuhashi et al. 2009; Guzman about ellobioid, let alone extant or fossil carychiid et al. 2009; Vendrasco et al. 2010; Rodrıguez-Navar- microstructure, our investigation presents new ro et al. 2012; Hickman 2013), very few studies (Jo- information about the microstructure of the Cary- chum 2011; Medakovic & Popovic 2012; Jochum chiidae. et al. 2013) have been conducted at the microstruc- tural level on terrestrial ellobioid taxa. It is well Carychiid taxonomy and systematics known that environmental influences play a pivotal role in shell mineralization and thus, influence shell As fossil and extant carychiid gastropods are known form, development and repair (McMahon & to be highly morphologically variable (Watson & Whitehead 1987; De Paula & Silveira 2009; Medak- Verdcourt 1953; Strauch 1977; Burch & Van Dev- ovic & Popovic 2012; Hickman 2013). As the Cary- ender 1980; Stworzewicz 1999; Weigand & Jochum chiidae inhabit semi-subterranean, subterranean and 2010; Weigand et al. 2012a,b; Weigand et al. 2013), extreme subterranean habitats, some existing 980 m they have been subject to frequent taxonomic re- below the surface (Weigand et al. 2013), their shells evaluation. Consequently, the plethora of forms has harbour a potential reservoir of valuable informa- systematically been shuffled and reshuffled into gen- tion. era and sub-genera, based on the degree of character Mollusc shells are polycrystalline complexes of expression in shell size, shape, form, dentition, whorl calcium carbonate, diverse proteins rich in acidic number, whorl height and, most specifically, the amino acids and glycoproteins (Lowenstam & Wei- degree of sinuosity of the columellar lamella ner 1989; Berman et al. 1993; Hedegaard & Wenk (Strauch 1977; Lueger 1981; Prisyazhnyuk & Stwor- 1998). Gastropod and bivalve shells demonstrate a zewicz 1995; Salvador 2015). For the herein treated comparable range of shell mineralogy and micro- carychiids, we follow the latest taxonomic and sys- structure (Carter et al. 1998), whereby gastropod tematic revisions of Miocene freshwater deposits by shells comprise an outer organic periostracal sheet Harzhauser et al. (2014a,b). Although recent molec- and an inner carbonate layer (Saleuddin & Petit ular analyses focusing on phylogenetic and phylo- 1983; Slapnik & Medakovic 2007). Their rigidity and geographical studies of extant
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