Zoomorphology (2003) 122:145–159 DOI 10.1007/s00435-003-0080-5 ORIGINAL ARTICLE Antonio G. Checa · Antonio P. Jimnez-Jimnez Rib fabrication in Ostreoidea and Plicatuloidea (Bivalvia, Pteriomorphia) and its evolutionary significance Received: 24 January 2003 / Accepted: 8 May 2003 / Published online: 24 June 2003 Springer-Verlag 2003 Abstract Ribs of Ostreoidea and Plicatuloidea are de- Introduction fined as antimarginal, that is, perpendicular to the margin throughout growth. Morphogenetically, these ribs are Ribs are by far the most common sculptural elements of unique, since, unlike radial ribs, they are secreted by a the shell of Bivalvia. They can be classified into three homogeneous mantle margin. Based also on the recon- main morphological categories: radial, commarginal, and structed shell secretion cycle in Bivalvia, we propose that oblique (Fig. 1A–C). Radial ribs can be defined as ribs of Ostreoidea and Plicatuloidea are formed by a helicospirals that diverge from the umbo and represent the mantle margin which, upon extension from the shell growth trajectories of particular portions of the mantle margin, stretches and folds by taking the preformed ribs specialized for rib secretion, which were identified and as templates. In extending perpendicular to the margin (as defined by Stone (1998) as corpora spinosa (see below). in all Bivalvia growing isometrically), such a mantle Commarginal ribs run parallel to the margin and are extends the rib pattern antimarginally. Ribs of this kind secreted by periodic extension of the mantle all along its are purely mechanical structures, as their arrangement length above the shell margin. Commarginal is preferred depends on the mechanical properties of the mantle and over the less accurate term concentric (see Cox 1969). on the environmental conditions. This explains the high Both the radial and commarginal patterns characterize irregularity of such ribbing patterns. The presence of large groups of bivalves, for example, radial ribs are the antimarginal ribs in both the Ostreoidea and Plicatuloidea only ones present in Pectinidae and Arcoidea, whereas sheds light on their origin. The first known oyster, Crassatellidae secrete exclusively commarginal ribs. Both Actinostreon cristadifformis, probably derived from an antimarginally ribbed Prospondylidae gen. indet. in the Late Permian or Early Triassic. Antimarginally ribbed Triassic species formerly included in Placunopsis origi- nated both the Dimyidae Atreta in the Late Triassic and Enantiostreon in the Mid Triassic, which was transitional to Plicatulidae. Therefore, Dimyidae and Plicatulidae are closely connected and grouped under Plicatuloidea, to which Ostreoidea is phylogenetically unrelated. Keywords Bivalves · Oysters · Morphology · Shell · Evolution A. G. Checa ()) · A. P. Jimnez-Jimnez Departamento de Estratigrafa y Paleontologa, Facultad de Ciencias, Universidad de Granada, Avenida Fuentenueva s/n, 18071 Granada, Spain Fig. 1A–D The four main morphogenetic varieties of bivalve ribs. e-mail: [email protected] A Radial (Pecten, Pectinidae). B Commarginal (Bassina, Veneri- dae). C Oblique (Divaricella, Lucinidae). D Antimarginal (Cu- Tel.: +34-958-243201 bitostrea, Ostreidae) Fax: +34-958-248528 146 Fig. 2A–F Examples of antimarginal ribs in Ostreoidea (A, B, D– Upper Coniacian, Wadi Sudr, Sinai (Egypt), specimen in Malchus F) and Plicatuloidea (C). A Ostrea lamellosa Brocchi, 1814, left (1990), plate 1, Fig. 7. E Ambigostrea villei (Coquand, 1862), right valve, EPUGR.JJ-Ju-10, Pliocene, El Alquin, Almera (Spain). B valve, Uppermost Campanian, between Qena and Quseir (Egypt), Hyotissa hyotis (Linnaeus, 1758), right valve, EPUGR.JJ-Ju-12, specimen in Malchus (1990), plate 23, Fig. 3. F Agerostrea Pliocene, El Alquin, Almera (Spain). C Plicatula gibbosa ungulata (Schlotheim, 1813), left valve, Maastrichtian, Ammonite Lamarck, 1801, left valve, EPUGR.BV.510, Recent, Gasparilla Hills (Egypt), specimen in Malchus (1990), plate 15, Fig. 8 Island (Mxico). D Oscillopha dichotoma (Bayle, 1849), left valve, kinds of ribs may coexist in some other groups and, commarginal. Several varieties are subsumed under this occasionally, on the same shell, thus producing cancellate general term including the single oblique, divaricate, ornamentation. A third, less common type, is the oblique rasp-like, and straight ornaments (Seilacher 1972; Checa one. Oblique ribs can be defined as those having 2002), all of which are morphogenetically related, since directions that are intermediate between radial and they arise essentially by contact-guidance mechanisms 147 (Checa 2002). Oblique ribs are not exclusive to any sputter-coated with gold (Polaron E5000). Electron micrographs supraspecific taxon with the exception the Divaricellinae were obtained with a Zeiss DSM 950. (Lucinoidea). Authors describing ribs of Ostreoidea (mainly Ostrei- dae, since the Gryphaeidae are usually smooth) and Results Plicatuloidea have invariably considered them to be radial (see, for example, Slack-Smith 1998), but a careful Comparative morphology of radial and antimarginal ribs inspection reveals that ribs in both groups diverge from of Ostreoidea and Plicatuloidea the shell center to remain approximately perpendicular to the shell margin throughout growth (Figs. 1D, 2). Ribs of Besides Camptonectes (Waller 1986), Ostreoidea, and this kind can be termed antimarginal and were initially Plicatuloidea, we have encountered antimarginal sculp- recognized and defined in Camptonectes (Pectinidae) by tures in other Pectinidae (such as Cyclopecten), Galeom- Waller (1986). Antimarginal ribs only follow radial matidae (Galeomma, Ephippodonta), Mytilidae (Septifer, directions at the ventral margin, whereas toward the sides Crenella, Urumella, Lithophaga), Limidae (Divarilima), they curve laterally to form broader angles with the radial Lucinidae (Epicodakia), and in juvenile Neoleptonidae directions. Although antimarginal ribs fit into the oblique (Neolepton), Nuculidae (Nucula), and Phyllobryidae condition, they should be kept separate on a morphoge- (Phyllobrya) (see illustrations in Gofas 1991; Hayami netic basis. and Kase 1993; Gofas and Salas 1996; Salas and Gofas Antimarginal ribs of Ostreoidea and Plicatuloidea are 1998; Checa 2002; N. Malchus personal communication). unique among present-day bivalves. Their pattern of An extensive review of literature and museum material lateral divergence is not easy to understand and, since reveals that antimarginal ribs are the only kind found in their singularity has gone unnoticed to earlier authors, Recent and fossil Ostreoida. The same applies to Plicat- there are no morphogenetic studies dealing with them, uloidea, with the exception of radially ribbed species therefore constituting a morphological enigma. The assigned to Plicatula, which were relatively common present study is dedicated to unraveling their morpho- between the Hauterivian and the Eocene (see, for genesis and exploring their systematic and evolutionary example, Squires and Saul 1997; El-Hedeny et al. significance. 2001). Whether or not they belonged to a single or several offshoots of antimarginally ribbed Plicatulidae is a matter of future study. Antimarginal ribs of these two Materials and methods groups show features that make them distinct from the antimarginal sculpture of other Bivalvia, which is Observations have been made on a large number of Recent and restricted to the outer shell layers. In oysters, on the fossil species both from the literature and from collections. In contrary, ribs are plicae (following the terminology of particular, we have had access to material housed in the following Stenzel 1971) that affect the entire thickness of the shell institutions: Departamento de Estratigrafa y Paleontologa, Uni- margin and replicate mutually on both valves. There are versidad de Granada (labeled EPUGR), Museo Nacional de Ciencias Naturales, Madrid (MNCN), Geologisch-palontologi- nevertheless two ways in which the shell corrugates. In sches Institut, Philipps Universitt Marburg (GPIUM), and Staat- most Ostreoida and in many species of Plicatula (partic- liches Museum fr Naturkunde Stuttgart (SMNS). ularly thick-shelled ones) folds of the shell margin fade We observed specimens with soft parts of the oysters Ostrea out quickly toward the shell interior on the inner shell edulis Linnaeus, 1758, provided at Centro de Cultivos Marinos PEMARES, El Rompido (Huelva, Spain), Crassostrea gigas surface (Fig. 3A). The position of the mantle margin (Thunberg, 1793), sampled in the intertidal of Roche (Cdiz, within the shell in the resting position is usually marked Spain) and Santa Luza (Algarve, Portugal), and Saccostrea by an internal shell deposit forming a marginal flange, the echinata (Quoy and Gaimard, 1835), from Ehime (Matsuyama, shell interior being flat or almost flat along this line. On Japan). Specimens of two unidentified species of Plicatula with preserved soft parts from Baha (Brazil) and Perim Island (Yemen) the contrary, in a few Ostreoida, and in thin-shelled were on loan from the Musum National d’Histoire Naturelle de species of Plicatula, shell folds affect the whole shell Paris (MNHN). Soft parts of bivalves of other groups already thickness (Fig. 3B). From here on, we will use the term present in the EPUGR collection were also studied: Pecten antimarginal to refer to ribs of the kind found in maximus (Linnaeus, 1758), Aequipecten opercularis (Linnaeus, Ostreoidea and Plicatuloidea. 1758), Mimachlamys varia (Linnaeus, 1758) (Pectinidae), Anomia ephippium