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Periostracal Mineralization in the Gastrochaenid Bivalve Spengleria Antonio G

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Periostracal Mineralization in the Gastrochaenid Bivalve Spengleria Antonio G Acta Zoologica (Stockholm) doi: 10.1111/azo.12019 Periostracal mineralization in the gastrochaenid bivalve Spengleria Antonio G. Checa1 and Elizabeth M. Harper2 Abstract 1Departamento de Estratigrafıa y Paleonto- Checa, A.G. and Harper, E.M. 2012. Periostracal mineralization in the logıa, Universidad de Granada, Avenida gastrochaenid bivalve Spengleria.—Acta Zoologica (Stockholm) 00: 000–000. Fuentenueva s/n, Granada, 18071, Spain; 2Department of Earth Sciences, University We investigated the spikes on the outer shell surface of the endolithic gastrochae- of Cambridge, Downing Street, Cam- nid bivalve genus Spengleria with a view to understand the mechanism by which bridge, CB2 3EQ, UK they form and evaluate their homology with spikes in other heterodont and pal- aeoheterodont bivalves. We discovered that spike formation varied in mecha- Keywords: nism between different parts of the valve. In the posterior region, spikes form biomineralization, molluscs, aragonite, peri- within the translucent layer of the periostracum but separated from the calcare- ostracum ous part of the shell. By contrast those spikes in the anterior and ventral region, despite also forming within the translucent periostracal layer, become incorpo- Accepted for publication: 20 November 2012 rated into the outer shell layer. Spikes in the posterior area of Spengleria mytiloides form only on the outer surface of the periostracum and are therefore, not encased in periostracal material. Despite differences in construction between these gastrochaenid spikes and those of other heterodont and palaeoheterodont bivalves, all involve calcification of the inner translucent periostracal layer which may indicate a deeper homology. Antonio G. Checa, Departamento de Estratigrafıa y Paleontologıa, Universidad de Granada, Avenida Fuentenueva s/n, 18071, Granada, Spain. E-mail: [email protected] anomalodesmatans is the product of mineralization of the Introduction internal periostracal translucent layer (Harper et al. 2009; The periostracum is the largely proteinaceous layer that is Checa and Harper 2010) such that these layers may be found on the outer surface of shelled molluscs (see Saleuddin regarded as intraperiostracal. In other bivalves, it has long and Petit 1983; Salas et al. 2012). It is the first formed part of been known that calcification may occur in isolated units also the shell and plays a number of critical roles in biomineraliza- foundwithintheperiostracum(Aller 1974; Carter and Aller tion of the calcareous portion of the shell. Key of these are the 1975), although Aller (1974) mistakenly suggested that calci- separation of the site of calcification from the contaminating fied spikes in Laternula had been prefabricated by the mantle effect of the ambient fluid, formation of the gross template and introduced pre-formed into the periostracum, a supposi- onto which biominerals are secreted and in some taxa protec- tion corrected by Carter and Aller (1975). In recent years, the tion from corrosion of shell material in environments, such as number of recorded instances of such intraperiostracal calcifi- freshwater or the deep sea, in which waters are unsaturated cation in extant bivalves has increased dramatically, e.g., in with respect to calcium carbonate (Taylor and Kennedy anomalodesmatans (Aller 1974; Checa and Harper 2010), 1969; Harper 1997). For many taxa, it has been assumed that some gastrochaenids (Carter and Aller 1975; Carter 1978), the outermost calcified shell layers are deposited directly onto certain mytiloids (Carter and Aller 1975; Bottjer and Carter the inner surface of the periostracal sheet and indeed this has 1980) and lucinids (Bottjer and Carter 1980; Taylor et al. been demonstrated within the bivalves for oysters and pteri- 2004), veneroids (Glover and Taylor 2010) and unionoids oids (Checa et al. 2005) and the astartid Digitaria digitaria (Zieritz et al. 2011). Intraperiostracal spikes have also been (Salas et al. 2012). However, in other bivalves for example, reported from fossil forms, for example, in the Modiomorphi- the external granular prismatic layer of many dae and Permophoridae (Carter 1990; Schneider and Carter © 2012 The Authors Acta Zoologica © 2012 The Royal Swedish Academy of Sciences 1 Spike formation in Spengleria Checa and Harper Acta Zoologica (Stockholm) 0: 1–13 (December 2012) 2001) although the vagaries of fossil preservation make it diffi- their secretion was initiated by the inner surface of the outer cult to study their genesis. mantle fold and that spikes grew progressively as the free peri- Periostracal calcifications are of interest for a number of ostracum moved towards the shell margin. The form of these reasons. They represent a relatively neglected field of mollus- spikes appears very similar to those which occur in many can biomineralization studies and their possible functions and anomalodesmatan bivalves, a fact which led Carter (1978) to potential for use as characters in phylogenetic analyses all sug- discuss the possibility of a close evolutionary relationship gest that the phenomenon requires investigation and docu- between the two taxa. Following detailed work on the mor- mentation. In respect to their phylogenetic significance, phology, crystallography and genesis of spikes in the anoma- Schneider and Carter (2001) introduced the possibility that lodesmatans (Checa and Harper 2010), we have taken the periostracal calcification might be a plesiomorphic character opportunity to undertake a comparative examination of the of the Bivalvia. However, the only intraperiostracal structures spikes of Spengleria. In particular, we used scanning electron which have been studied in detail are ‘flaps’ and granules of microscopy (SEM) of shell material combined with optical Lucina pennsylvanica (Taylor et al. 2004), the spikes of anom- and transmission electron microscopy (TEM) to focus on alodesmatans (Aller 1974; Prezant 1979; Checa and Harper their relation with the different layers of the periostracum and 2010) and the needles and pins of venerids (Glover and Tay- with the shell, and compared the pattern with what is known lor 2010) and it is clear in each of these instances that the from other spiky bivalves. mode of formation of these structures is different and, there- Huber (2010) records only three species of Spengleria but fore, they are not homologous. Our purpose here was to the genus, which ranges across a broad subtropical belt in expand our knowledge of periostracal calcification in another Americas, Africa and the Indopacific, is in certain need of taxon, the gastrochaenoids that were investigated by Carter revision (Paul Valentich Scott, personal communication). In (1978), who suggested that they might have phylogenetic sig- reality only one species, Spengleria rostrata has been studied in nificance. any detail. The thin and inequilateral valves of Spengleria have The Gastrochaenoidea comprises a single family, the Gas- a marked diagonal radial line which passes from the umbo to trochaenidae, of endolithic heterodont bivalves. Traditionally, a point on the posterior-ventral margin (Fig. 1). This line sep- they are placed within the order Myoida allied to the Hiatelloi- arates two different styles of surface ornamentation, with the dea (Newell 1969) but this has not been supported by molec- more pronounced ornament being in the posterior sector. ular phylogenetic analyses (see Taylor et al. 2007) and as a result recent classifications haveremovedtheGastrochaeni- Material and methods dae from the Myoida (Bieler and Mikkelsen 2006; Giribet 2008; Bieler et al. 2010). Material Gastrochaenids first appear in the fossil record in the Jurassic (Carter et al. 2008). Huber (2010) lists eight extant Our principal study was on material (2 specimens) of Spengle- genera (Gastrochaena, Rocellaria, Lamychaena, Dufiochaena, ria rostrata (Spengler, 1783) collected from Panama City, Spengleria, Curcurbitula and Eufistulana), to which Carter (in Florida (USA) from a coral substrate at 60 m (ex Santa Bar- Carter 2011) added a new genus Spenglerichaena, which are bara Museum). However, no soft parts were available to com- distributed in the tropics and subtropics in shallow water. All plete our study on all aspects of spike formation. As a result bore into calcareous substrata (both limestone rock and skele- tal carbonates of corals and molluscs) (Morton 1983). Some taxa are well known for the presence of spikes on the outside of the shell. Although most gastrochaenids are spike-free, some members of the genus Gastrochaena produce them as juveniles (Carter 1978) and those of all species of Spengleria produce spikes throughout ontogeny. The spikes of Spengleria rostrata have been studied in some depth by Carter and Aller (1975) and Carter (1978). Carter (1978) discovered that the spikes on the outer sur- face of Spengleria rostrata consisted of aragonite and showed considerable variation in their size and morphology across dif- ferent parts of the valve. Those in the posterior region were apparently embedded entirely within the periostracum whereas those at the anterior appeared to be partly embedded in the shell material below and the periostracum here had Fig. 1—Complete right valve of Spengleria rostrata (FMNH 188359, markedly thinned. Earlier work by Carter and Aller (1975) length 27.3 mm) from Bonefish Key, Florida. Photograph courtesy of indicated that these spikes were covered by periostracal mate- RudigerBieler(FieldMuseumofNaturalHistory).pvb,posterior- rial. This study did not explain their formation but stated that ventral
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