Fabricational Morphology of Oblique Ribs in Bivalves

Home , Acanthocardia aculeata, Chlamys (bivalve), Lithophaga lithophaga, Solecurtus, Solecurtus strigilatus, Tellina

JOURNALOFMORPHOLOGY254:195–209(2002)

FabricationalMorphologyofObliqueRibsinBivalves

AntonioG.Checa*

DepartamentodeEstratigraf´ı ayPaleontologı´a,FacultaddeCiencias,UniversidaddeGranada,18071Spain

ABSTRACTTheformationofobliqueribsofbivalve PeriglyptaorChione),producingcancellateorna- shellsusuallyhasbeenattributedtoprocessesofreaction- mentation.Athirdkind,herecalledoblique,isless diffusionofmorphogensfromcelltocellatthemantle commonthantheothertwotypes.Obliqueribscan marginorneuralactivationandlateralinhibitioninthe bedefinedashavingdirectionsthatareintermedi- mantle.Inparticular,suchribsappearwithhighratesof lateraldiffusion.Nevertheless,theoreticalmodelsfailto atebetweenradialandcommarginal.Thesemay explaineitherpartiallyorwhollysomevarietiesofoblique reverttocommarginaltowardstheanteriororpos- ribs.Aftersurveyingthemodesofformationoftheshell teriorsidesoftheshell,orboth.Severalvarietiesare andobliqueribsbythebivalvemantleandassociated includedwithinthisgeneralterm(Fig.1).Therecan fabricationaldefects,Ihavedeterminedthatthemantleis beoneormorebranchesobliquetothemargin,in abletodevelopanelaboratebehaviorinordertodisplace whichcasetheterms“singleoblique”and“divari- theribinaparticulardirectionduringgrowth.Theman- cate”(i.e.,divergent)arerespectivelyapplied.Some- tlemarginis,therefore,notonlytheshell-secretingorgan, timesdivaricateribsarecomposedofdiscreteele- butalsothemainmorphogeneticunit.Inparticular,there mentsthatalternateoverconsecutivegrowth aretwomainfabricationalstrategies.Informswithstrict contactguidance(SCG)themantleisabletoprojectfar stages,producingadiscontinuouspattern.Most enoughbeyondtheshellmarginssoastofeelthealready obliqueribschangetheirdirectionprogressivelyto formedreliefsandtoalignnewgrowthincrementsofthe maintainaconstantanglewiththemargin.Excep- ribsintheappropriatedirections.Theshellmarginis tionstothisrulearestraightribs,whichcanbe alwaysstronglyreflected.Inbivalveswithreducedcontact definedassingleobliqueordivaricateribsthatfol- guidanceplusconstantlateralshift(RCG),themarginis lowastraightalignment.Therefore,theybeginas usuallyacuteandtheinformationaboutribsavailableto paralleltothemarginandprogressivelyanglewith themantleisreduced.Duringribconstructionthemantle growth.Thelastvarietyisantimarginal(sensu extrudesslightlyfromtheshelledgeandthenpushes Waller,1986).Theseribsdivergefromtheshellcen- laterallybymuscularaction;inthisway,thenewgrowth incrementoftheribisdisplacedlaterallyonasmallscale. tertoremainperpendicularoratahighangletothe Thecontact-guidancemodelissupportedalsobytheho- shellmarginthroughoutgrowth.Ribsofthiskind mogeneousstructureoftheshell-secretingmantle.From arealsopeculiarinbeinghighlyirregularindistri- themorphogeneticstandpoint,obliqueribsarerelatedto butionandmorphology.Contrarytotheothertypes, commarginalonesandbothdiffercompletelyfromother thispatternistaxonomicallyrestricted,beingexclu- ribbingpatternsofbivalves.J.Morphol.254:195–209, sivetotheOstreoideaandPlicatuloidea.Antimar- 2002. ©2002Wiley-Liss,Inc. ginalribsaremorphogeneticallydistinctfromother typesofobliqueribs(ChecaandJimeńez-Jimeńez, KEYWORDS:constructionalmorphology;morphogene- 1999)and,consequently,willnotbeincludedinthis sis;shellsculpture;obliqueribs;bivalves study. Obliqueribsarenotexclusivetoanysupraspecific taxon,withtheexceptionofsomegeneraofthe Bivalvesdisplayessentiallythreeribbingpat- Divaricellinae(Lucinoidea).Atotalof176Recent terns:radial,commarginal,andoblique.Radialribs speciesdisplayingobliquepatternshasbeenre- canbedefinedashelicospiralsthatconvergeto- cordedfromtheliteratureandfrommuseumspeci- wardstheumboandcorrespondtothegrowthtra- jectoriesofdefiniteportionsofthemantlespecial- izedforribsecretion(seebelow).Commarginalribs areparalleltothemarginandaresecretedbya Contractgrantsponsor:DGESIC(MEC);Contractgrantnumber: PB97-0790;Contractgrantsponsor:ResearchGroup(PAI,JA);Con- mantlethatextrudesperiodicallyallalongitsexten- tractgrantnumber:RNM-0178. sionabovethenormalshellprofile.Bothpatterns characterizelargegroupsofbivalves;forexample, *Correspondenceto:AntonioG.Checa,DepartamentodeEstrati- pectinids,arcoids,orcardiidsallhavetheradialas graf´ı ayPaleontologáı ,FacultaddeCiencias,Universidadde theonlyribbingpattern,whereascrassatellidsor Granada,AvenidaFuentenuevas/n,18071Granada,Spain. tellinidsdisplayexclusivelycommarginalribs.In E-mail:[email protected] someothergroups(Lucinidae,Veneridae,Psammo- Publishedonline00Month2002in biidae)bothradialandcommarginalribsmaycoex- WileyInterScience(www.interscience.wiley.com) ist,occasionallyonthesameshell(e.g.,speciesof DOI:10.1002/jmor.10028

Fig. 1. Varieties of oblique ribs illustrated by selected bivalves. Single oblique and divaricate ribs maintain a more or less constant angle with respect to the shell margin, while in straight ribs this angle increases with size. The ribs of Tellina scobinata are discontinuous, composed of elements that alternate with growth episodes. Antimarginal ribs meet the shell margin transversely or at a high angle and are exclusive to the Ostreidae and Plicatulidae. mens, the taxonomic distribution of which is shown around Protobranchia, Palaeoheterodonta, and Het- in Figure 2. An uneven distribution appears among erodonta. At the superfamily level, the same applies subclasses and orders, most species clustering to Tellinoidea, Unionoidea, Veneroidea, Mytiloidea,

Fig. 2. Distribution of oblique ribs and their mode of formation in Recent bivalve species with oblique ribs. Ostreina (ϩ Pectinina ϭ Ostreoida), with exclusively antimarginal ribs, are not included. Systematic arrangement after Beesley et al. (1998). RCG, reduced contact-guidance plus constant lateral shift; SCG, strict contact-guidance. FABRICATION OF OBLIQUE RIBS IN BIVALVES 197 and Lucinoidea, in descending order. This distribu- els based on activation sites have been used to ex- tion hardly reflects the fossil record of bivalves with plain rib and pigment patterns on the shells of mol- oblique ribs. Ongoing research indicates that the luscs (Lindsay, 1982a, b). Other explanations history of oblique ribs began in the Middle Ordovi- address the formation of biological patterns. cian with some Modiomorphoida (now extinct). The Reaction-diffusion mechanisms were originally put scanty Paleozoic record is composed primarily of forth by Turing (1952) and have been widely applied pholadomyoids, together with a few pectinoids, pte- to morphogenetic processes (e.g., Murray, 1981, rioids, and nuculoids. Pholadomyoids and particu- 1988; Meinhardt, 1982). The application of reaction- larly trigonioids (which have no Recent species with diffusion mechanisms to model shell patterns began oblique ribs) dominate the marine Mesozoic record, with Meinhardt (1984) and expanded the field of whereas in freshwater environments unionoids with theoretical modeling. These models are based on the divaricate ribs were already abundant by Late Cre- principle that secretion of a structure is initiated taceous times. The Cenozoic (post-Paleocene) saw when the concentration of an activator substance the substitution of older groups by veneroids (telli- reaches a certain concentration within a cell or noideans, lucinoideans, and veneroideans), nucu- group of cells. The activator has an autocatalytic loids (nuculoideans, nuculanoideans), and mytiloids feedback on its own production. Inhibition of activa- (mytilids), which progressively yielded the Recent tor production may come either from depletion of a distribution (Fig. 2). Therefore, the two Recent spe- substrate (activator precursor) or from the forma- cies of pholadomyoids with oblique ribs recorded are tion of an inhibitor, which is produced simulta- but the relict of a formerly flourishing group. neously with the activator (see Meinhardt and Oblique ribs of the asymmetric type (which indicates Klinger, 1987). Under some conditions, both the ac- an adaptation for faster and more efficient burrow- tivator and the substrate/inhibitor can diffuse from ing; see below) were absent during the Paleozoic and one cell to the neighboring ones, which, in this way, Mesozoic, but were the most common type during become “infested.” Therefore, the signal for the for- the Cenozoic. The Cenozoic radiation of bivalves mation of the structure (rib or pigment line) shifts with asymmetric oblique ribs appears to have had a laterally with time, moving along oblique directions. major ecological cause and resulted from an adapta- According to the neural model of Ermentrout et al. tion to either the Phanerozoic increase in the diver- (1986), the activity of pigment-secreting cells of the sity of durophagous predators (e.g., Vermeij, 1977) mantle is regulated by nervous impulses, through or the accelerating rate of sediment reworking the neural network that interconnects mantle inner- (Thayer, 1983). In conclusion, oblique ribs emerged vations with the central ganglion(s). Therefore, several times in unrelated groups of both epibenthic long-range interactions are possible. The model in- and endobenthic bivalves and, therefore, they can corporates short-range excitation and long-range in- hardly be used as a high-ranking systematic and hibition, typical of neural nets. An innovation with evolutionary character. respect to previous models is that receptor cells of Oblique (and, in particular, divaricate ribs) have the mantle are able to discriminate between pig- been studied from two well-defined perspectives: mented and nonpigmented areas of the already-laid- function and formation. Constructional morphology down shell, the former stimulating the mantle to studies have focused primarily on the function of continue the pattern. Diagonal pigment strips are oblique ribs, which are apparently quite well suited obtained with very low excitatory, inhibitory, and for burrowing (Stanley, 1969, 1970, 1975, 1988; secretion thresholds, which also have gradual cut- Seilacher, 1972, 1973; Savazzi, 1983); this is partic- offs. Both reaction-diffusion and neural models yield ularly true of ribs with asymmetric profiles and that very similar results and have been particularly suc- are oriented transverse to the direction of burrow- cessful in reproducing shell color patterns, including ing. The fact that oblique ribs facilitate burrowing most varieties of oblique ones (e.g., Meinhardt, was also established quantitatively by Stanley 1995). (1975), although it has not yet been demonstrated In opposition to chemical models, mechanochemi- that their efficiency surpasses that of commarginal cal models of morphogenesis propose that signaling or radial ribs. Another function attributed to divari- mechanisms (involving chemical gradients set up by cate ribs in Solecurtus is that of minimizing damage diffusion) cause motile cells to clump together and to the valve margins during burrowing, by intercept- that the traction forces caused by aggregation can ing radial breaks and deflecting them back again bring about instabilities that lead to further pat- towards the margin (Checa, 1993). I have recorded terning (Oster et al., 1983, 1985; Oster and Murray oblique ribs on the shells of a few epibenthic bivalves 1989). Therefore, chemical and mechanical pro- (e.g., Mytilidae and Chamidae; Fig. 2), for which the cesses interact continuously to produce both the only hypothetical function is that of reinforcing the chemical pattern and the form-shaping movements. margin. Mechanochemical models have been applied to a A set of theoretical morphology studies has also variety of situations in embryology but their pro- dealt with oblique ribbing. Since the pioneering spective usefulness to model patterns of shell orna- work by Waddington and Cowe (1969), formal mod- ment remains to be investigated. 198 A.G. CHECA nating patterns the former scale inhibits additional scale formation (see below). In the search for alternative explanations, the methods of constructional morphology have been applied here to oblique ribbing patterns but from an essentially fabricational viewpoint. In our approach, a main point is the reconstruction of the fabrication process, i.e., the sequence of movements of the mantle margin during shell (and rib) secretion. To arrive at a fabricational model, we have integrated the information from the shell structure, the geometry of growth lines, and the “defects” that arose during the secretion process (fabricational noise sensu Seilacher, 1973).

MATERIALS AND METHODS Specimens (some including the soft parts) belonging to 45 bivalve species were studied (Table 1). The material comes essentially from three institutions: Departamento de Estratigraf´ıay Paleontolog´ıa, Universidad de Granada (EPUGR), Museúm Na- tional d’Histoire Naturelle de Paris (MNHN), and Museo Nacio- nal de Ciencias Naturales de Madrid (MNCN). The samples rep- resent the variety of oblique ribs and their systematic Fig. 3. Divaricella cumingi (MNHN, unreg.). Divaricate ribs distribution within the Bivalvia. form constant angles with growth lines throughout the shell. Surficial microornament and microstructure were observed both with SEM (Zeiss DSM 950) and binocular microscopy at After a prolonged halt in growth (arrow), the concordance be- ϫ ϫ tween ribs is lost and new ribs are offset with respect to the axis magnifications ranging from 10 to 2,000. Fractured shells of divergence. a, anterior direction; d, dorsal direction. were examined intact or polished (previously embedded in epoxy resin); they were studied unaltered or corroded with either 5% sodium hydroxide or 1% hydrochloric acid to remove the perios- Despite their success, theoretical models (partic- tracum and intercrystalline organic matter or calcium carbonate, respectively. The mantles of Solecurtus strigilatus (Linnaeus) ularly of the chemical type) currently fail to be test- and Digitaria digitaria (Linnaeus) were observed with SEM, able, since the activator and inhibitor/substrate which required fixation in cacodylate buffered (0.1 M, pH 7.4) substances (the so-called morphogens in reaction- 2.5% glutaraldehyde, followed by dehydration in increasing con- diffusion processes or excitation-inhibition sub- centrations of ethanol and critical-point drying. stances in the neural model) have not yet been detected. There is no biochemical proof that these RESULTS AND DISCUSSION models reproduce the process of formation, and not Observation and Inferred Mode of merely the pattern. In the case of animals with Fabrication of Oblique Ribs accretionary skeletons (e.g., bivalve molluscs) there are some naturally occurring rib patterns that are The mode of shell and rib fabrication was studied not explained by theoretical models. Reaction- extensively in some species, in which the availability diffusion models require constant rates of lateral of material permitted destructive techniques. Fabri- diffusion, so that ribs or color lines should maintain cational patterns in other species were inferred from a constant angle with the shell margin. This is not species showing identical external morphological the case with straight oblique ribs (Fig. 1), in which features. such angles reduce with growth. According to theo- Oblique ribs in Divaricellinae (Lucinoidea). retical models, the angle between ribs and growth The genera Divaricella, Divalinga, and Divalucina lines should also vary depending on the rate of local display archetypical divaricate patterns. In all the marginal growth. In bivalves, this angle should de- species examined the divergence axis of the ribs cline accordingly from the venter to the umbo along runs in a ventral, slightly anterior direction (Figs. 1, the margin corresponding to a given growth moment 3). Ribs, regardless of their position on the shell, in coincidence with the rate of marginal growth. form a similar angle with growth lines. In the This is not the case in actual shells (see below; Fig. unique case of Divaricella quadrisulcata, normal 3). Finally, some patterns are discontinuous and growth lines are replaced on the ribs by dorsally alternating (Figs. 1, 7, 8), while the cell-to-cell dif- concave and wider growth lines, which fade out on fusion model predicts a continuous structure. Nor the gentle slopes of the ribs (Fig. 4A). Transverse can a neural model be applied to these situations, sections reveal that these unusual growth lines cor- since it implies that the already secreted structure respond to deposits of aragonite fibers perpendicular should stimulate further structure formation, while to the shell surface (Fig. 4B), which cover the fibrous during the formation of actual discontinuous alter- prismatic shell and hidden shell growth lines. The FABRICATION OF OBLIQUE RIBS IN BIVALVES 199

TABLE 1. Details of taxa and specimens investigated No. of specimens, repository Taxon Locality and reg. no. Nuculoida Acila beringiana (Dall, 1919) Bering Sea 2 ϫ 1, EPUGR.BV.104 Acila castrensis (Hinds, 1843) NW Puget Sound 3 ϫ 2, EPUGR.BV.106–107 Acila divaricata (Hinds, 1843) Taiwan, offshore Taipei 3 ϫ 2, EPUGR.BV.108–109 Acila fultoni Smith, 1892 Bengal Bay, India 4 ϫ 2, MNHN (unreg.) Acila sp. Philippines (loc. unknown) 5 ϫ 2, MNHN (unreg.) Nuculana bicuspidata Gould, 1845 Senegal 4 ϫ 2, EPUGR.BV.102–103 Nuculana cellulite Dall, 1896 Tillamook Bay, Washington 3 ϫ 2, EPUGR.BV.110–111 Mytiloida Ischadium recurvum (Rafinesque, 1820) N America (loc. unknown) 6 ϫ 2, MNHN (unreg.) Gregariella sulcata (Risso, 1826) Marbella, SE Spain 1 ϫ 2, EPUGR.BV.130 Lithophaga lithophaga (Linnaeus, 1758) Mediterranean (loc. unknown) 23 ϫ 2, EPUGR.BV.300–322 Septifer bilocularis (Linnaeus, 1758) Phuket, Thailand 2 ϫ 2, EPUGR.BV.133–134 Unionoida Caelatura bakeri (Adams, 1866) Nyanza 17 ϫ 2, MNHN (unreg.) Lamprotula sp. China (loc. unknown) 7 ϫ 2, MNHN (unreg.) Lasmigona costata (Rafinesque, 1820) Ohio (loc. unknown) 1 ϫ 2, MNHN (unreg.) Veneroida Ctena bella (Conrad, 1837) W Australia (loc. unknown) 1 ϫ 2, EPUGR.BV.200 Divalinga eburnea Reeve, 1850 La Paz, Me´xico 1 ϫ 2, EPUGR.BV.201 Divalucina cumingi (Adams and Angas, 1863) a. South Coast of Natal, South Africa 37 ϫ 1, MNHN (unreg.) b. Loc. unknown 2 ϫ 2, MNHN (unreg.) Divaricella gibba (Gray, 1825) Port Gentil, Gabon 4 ϫ 1, MNHN (unreg.) Divaricella dentata (Wood, 1815) Florida Keys 43 ϫ 1, MNHN (unreg.) Divaricella quadrisulcata (Orbigny, 1842) Isla Mujeres, Me´xico 5 ϫ 1, EPUGR.BV.94–98 Digitaria digitaria (Linnaeus, 1758) Barbate, S Spain 5 ϫ 2, EPUGR.BV.62–68 Nemocardium lyratum (Sowerby, 1841) a. Philippines (loc. unknown) 4 ϫ 2, MNCN (unreg.) b. Laminusa Island, Philippines 1 ϫ 2, EPUGR.BV.206 Donax madagascariensis Wood, 1828 Durban, South Africa 1 ϫ 2, EPUGR.BV.207 Gari maculosa (Lamarck, 1818) a. Cebu´ , Philippines 4 ϫ 2, MNCN 15.07/0005, 15.07/0013, 15.07/0035 b. Philippines (loc. unknown) 3 ϫ 2, MNHN (unreg.) Gari squamosa (Lamarck, 1818) Philippines (loc. unknown) 9 ϫ 2, 1 ϫ 1, MNCN 15.07/0003, 15.07/0142 Solecurtus philipinensis (Dunker, 1861) Philippines (loc. unknown) 11 ϫ 2, MNCN 15.07/4768 Solecurtus strigilatus (Linnaeus, 1758) a. Almeria coast, SE Spain 3 ϫ 2, EPUGR.BV.142–145 b. Huelva coast, SW Spain 52 ϫ 1, EPUGR.BV.322–373 Abra petiti (Dautenberg) Natal South coast 1 ϫ 2, EPUGR.BV.208 Macoma dispar (Conrad, 1837) Santa Carolina, Mozambique 1 ϫ 2, EPUGR.BV.209 Strigilla carnaria (Linnaeus, 1758) a. Caribbean (loc. unknown) 5 ϫ 2, 1 ϫ 1, MNHN (unreg.) b. Venezuela (loc. unknown) 1 ϫ 2, EPUGR.BV.223 Strigilla pisiformis (Linnaeus, 1758) Caribbean (loc. unknown) 23 ϫ 1, MNHN (unreg.) Strigilla polyaulax (Tomlin and Shackelford, 1915) a. Pointe Noire, Congo Brazzaville 2 ϫ 2, EPUGR.BV.202–203 b. Luanda, Angola 1 ϫ 2, EPUGR.BV.204 Tellina linguafelis (Linnaeus, 1758) Bowenstand, Australia 1 ϫ 2, EPUGR.BV.210 Tellina palatum (Iredale, 1929) Siasi, Philippines 2 ϫ 2, EPUGR.BV.211–212 Tellina scobinata (Linnaeus, 1758) a. Bushy Island, Australia 1 ϫ 2, EPUGR.BV.213 b. Loc. unknown 1 ϫ 2, MNHN (unreg.) Tellina trilatera Gmelin Muizenberg, South Africa 2 ϫ 2, EPUGR.BV.214–215 Chamelea gallina (Linnaeus, 1758) Granada coast, SE Spain 103 ϫ 2, EPUGR.BV.373–475 Chamelea striatula (da Costa, 1778) Ma´laga coast, SE Spain 15 ϫ 2, EPUGR.BV.476–490 Circe intermedia Reeve, 1864 Al-nigaiyet, Kuwait 1 ϫ 2, EPUGR.BV.216 Circe rivularis Burn, 1778 Reevesby Island, S Australia 2 ϫ 2, EPUGR.BV.217–218 Gafrarium dispar (Dillwyn, 1817) Australia (loc. unknown) 1 ϫ 2, EPUGR.BV.219 Gafrarium pectinatum (Linnaeus, 1758) Madagascar (loc. unknown) 1 ϫ 2, EPUGR.BV.220 Gafrarium tumidum (Ro¨ding, 1798) a. Philippines (loc. unknown) 1 ϫ 2, EPUGR.BV.221 b. Guam Island 1 ϫ 2, EPUGR.BV.222 Venus verrucosa (Linnaeus, 1758) Almeria coast, SE Spain 12 ϫ 2, 7 ϫ 1, EPUGR.BV.490–508 Petricola carditoides (Conrad, 1837) California (loc. unknown) 2 ϫ 2, MNCN (unreg.) unreg., unregistered; ϫ1, loose valve; ϫ2, specimen with paired valves; EPUGR, Departamento de Estratigraf´ıa y Paleontolog´ıa, Universidad de Granada; MNHN, Museúm National d’Histoire Naturelle, Paris; MNCN, Museo Nacional de Ciencias Naturales, Madrid morphology of growth lines and the orientation of margin, each of these reflecting onto a rib as the fibers imply that these secondary deposits are cre- main shell margin was being secreted (Fig. 5). These ated by acute backward extensions of the mantle extensions take the form of pointed tongues, with 200 A.G. CHECA growth increments with the former rib by mere contact (contact-guidance mechanism). Assuming a constant diffusion rate, reaction-diffusion models pre- dict that ribs must deflect laterally during periods of reduced growth rate of the shell, since the rate of lateral displacement remains the same. This is never the case in lucinids—conversely, ribs maintain a constant angle with growth lines even at conspicuous regions of growth cessation. After some prolonged halts in growth a new shell forms below the old one and the abandoned margin remains raised. In this case, the mantle is inferred to lose contact with the former margin, producing a new, independent arrangement of ribs, which are now more closely spaced than previously (Fig. 3), and therefore resemble a more juvenile stage. How this new arrangement arises in the absence of the former template is unknown, but it could well be produced by muscular waves of the mantle edge. Only in Di- varicella dentata do ribs project markedly from the margin parallel to the shell surface, giving a dentic- ulate appearance in plain view. This provides contact-guidance across growth episodes separated by a raised margin. Straight ribs of Nemocardium lyratum (Car- dioidea) and Donax madagascariensis (Telli- noidea). In Nemocardium lyratum ribs develop only on the anterior and central areas of the shell. They run straight or slightly curved in either direction and are regularly spaced (Fig. 1). This pattern is unusual among bivalves in that each rib originates parallel to the margin and, upon growing, crosses the successive margins at increasing angles. This is especially evident towards the anteriormost side, where the angle of intersection may reach some 80°. Savazzi (1983) showed that terraces in N. lyratum are not continuous into the shell, but are deposits formed on the periostracum by a reflecting mantle, in a way similar to Divaricella quadrisulcata.In Donax madagascariensis (Fig. 1), ribs are commarginal at the posterior side of the shell but as soon as they cross the crest delineating the posterior area they run straight and become increasingly oblique to

Fig. 4. Divaricella quadrisulcata. Surface (A) and cross- sectional (B) views of oblique ribs. A: Specimen EPUGR.BV.95. The gentle slope of a single rib displays a smooth texture due to the presence of secondary prismatic deposits, which bear their own growth lines. The steep slope appears white. B: Specimen EPUGR.BV.96, left valve. Transverse section of the shell through a rib. Secondary deposits consist of prisms transverse to the shell’s surface (arrow). a, anterior direction; d, dorsal direction. one side aligned with the rib. This pattern implies that in this and the other above-mentioned lucinids the mantle keeps abreast of the reliefs occurring at Fig. 5. Model for the fabrication of ribs in Divaricella the shell’s edge and surface. In D. quadrisulcata, the quadrisulcata. The mantle reflects at the margin and sends out inferred mantle extensions could well align the new extensions, each onto a rib, which secrete secondary deposits. FABRICATION OF OBLIQUE RIBS IN BIVALVES 201 the growth lines until becoming transverse at the anteriormost end of the shell. The absence of secondary deposits and the extent of the periostracum indicate that the mantle margin reflects, but does not extend backwards enough to adhere to the outer shell surface. Since reaction-diffusion models cannot explain the formation of straight ribs (see above), the contact-guidance mechanism is the only plausi- Fig. 7. Fabrication model for discontinuous divaricate ribs in ble explanation: triangular tongue-like (in N. lyra- Tellina scobinata.Inafirst stage (left) the mantle progressively tum) or rounded (in D. madagascariensis) mantle advances and elevates (thus preforming scales) at the interscales of the previously formed shell margin. After the new growth extensions must reflect onto or adhere to each rib tip increment has been calcified (right) the process is repeated, but to appropriately align the new growth increments. the position of scales and interscales now alternates. Increasingly oblique ribs of Chamelea (Ven- eroidea) and Tellina palatum (Tellinoidea). In Chamelea gallina and C. striatula the relationship characterized by the formation of minute divarica- between growth lines and ribs varies throughout tions and interruptions, producing an apparently growth. Growth periods begin with purely commar- disorderly pattern. The cyclic and progressive na- ginal ridges, but later these ridges become progres- ture of these patterns is difficult to explain by the- sively oblique with respect to the shell margin to- oretical models, without the corresponding algo- wards the anterior part of the shell (Fig. 6). This rithm being artificially complicated. happens because the ridges become increasingly Discontinuous ribs in species of Tellina coarse anteriorwards, so that each rib extends for a (Tellinoidea). In Tellina scobinata and T. linguafe- greater number of growth lines here. Occasionally, lis, ornamentation is composed of scales projecting after conspicuous halts in growth, which bevel form- perpendicular to the shell’s surface. The scales al- ing ribs, these revert to being commarginal (Fig. 6). ternate in successive secretion episodes, giving a This pattern can be explained as being formed by discontinuous, rasp-like divaricate pattern (Fig. 1). mantle waves that propagate anteriorwards. As in After secretion of a set of scales the shell margin is lucinids, the shell margin is reflected backwards and wavy, elevated at the scales, and depressed in be- the mantle can touch the outer surface and gain tween. These differences can be detected easily by positional information about its surface relief. In the mantle, which now reverses the pattern, project- Tellina palatum, halts in growth are similarly ing outwards only where an interspace is detected marked by commarginal ribs. Further growth is (Fig. 7). This fabricational model explains why scales become larger with growth and why their numbers remain constant, since each interscale gives rise subsequently to one and only one scale; thus, no new elements are introduced, provided that shell growth is isometric. Fabricational noise in the form of imperfections also fits with a contact- guidance model. In T. scobinata, scales of successive growth increments locally become closely spaced, almost fused, during periods of reduced growth (Fig. 8A). Fused scales are perceived by the mantle as single large ones and this translates as a defect that is transmitted during further growth. In rare instances of jagged margins, scales are subsequently induced at the sites in which small pieces have been chipped away (Fig. 8B). Growth-rate-dependent oblique ribs of Nu- culidae, Astartidae, and some Tellinoidea. Oblique ribs in species of the genera Solecurtus, Strigilla, Gari, Nuculana, Digitaria, and Acila change their orientation with the shell’s growth rate. During periods of reduced growth (inferred from closely spaced growth lines) between growth cycles or at maturity, ribs deviate laterally and form angles that are more acute with respect to the growth lines (Fig. 9). Measurements by SEM in Fig. 6. Chamelea gallina (EPUGR.BV.387). Ribs become progressively oblique to growth lines until a prolonged halt in growth Digitaria digitaria indicate that the amplitude of (arrow) is reached. Thereafter, ribs reinitiate as commarginal. a, lateral jumps increases steadily with valve size, anterior direction; d, dorsal direction. while the distance between growth lines grows ac- 202 A.G. CHECA displacement with time. A contact-guidance mechanism is also implied by the fact that the new shell secreted after the margin has been extensively chipped lacks all or some of the ribs—i.e., once the former template is lost, there is no reference for the mantle to continue the pattern. Good examples of this are frequent in Solecurtus (Fig. 10) and, to a lesser extent, in Gari and Strigilla (see fig. 7, Mein- hardt and Klinger, 1987). In some of the above cases, two ribs may initiate spontaneously forming a “∧”

Fig. 8. Fabricational defects in Tellina scobinata. A: Specimen MNHN (unreg). Coinciding with periods of reduced growth (arrows), scales of successive growth increments become fused. Later, the mantle appears to sense them as a single scale, with the subsequent formation of unusually large scales and interscales. B: Specimen EPUGR.BV.213. Arcuate breaks of a jagged margin induce the formation of scales. A possible explanation is that the mantle responds to breaks as though they were incipient scales and completes them when growth is resumed. a, anterior direction; v, ventral direction. cording to a typical logistic pattern, explaining why the angle between ribs and growth lines decreases at Fig. 9. Acceleration of lateral displacement of ribs during maturity. If growth stopped completely, ribs may periods of reduced shell growth. A: Strigilla polyaulax even skip and reappear farther in the direction of rib (EPUGR.BV.204). B: Nuculana cellulite (EPUGR.BV.111). d, dor- displacement. This implies a constant rate of lateral sal direction; p, posterior direction. FABRICATION OF OBLIQUE RIBS IN BIVALVES 203 pattern; when the branch running opposite to the normal direction meets the next regular rib, these fuse to form a “V” pattern (Fig. 10). Additionally, in very rare instances ribs reinitiate with breaks, as if the sharp edges thus formed locally were taken for ribs by the organism (ﬁg. 16, Checa, 1993). Detailed observation reveals that ribs in the species listed clearly have a step-like appearance in plain view in the sense that ribs seem to shift laterally by small bursts, a situation that is inconsistent with a cell-to-cell activation model (Fig. 11). Thus, at every growth step the lateral jump precedes radial growth, as is evident in Acila (Fig. 11B), Strigilla, and particularly Digitaria (Fig. 11A). This pattern is obscured in Solecurtus, since the composite prisms forming the outer shell layer are larger than the presumed lateral jumps, judging by the distance between growth lines. How the bivalve calibrates lateral displacement is unclear, but it can be hypoth- esized that a pressure-sensitive mechanism may op- erate. If the extruded mantle of, for example, Digi- taria shifted laterally, it would become adpressed against the inner surface of the rib slope in the direction of advance (Fig. 12). Given the viscoelastic nature of the mantle, a compression lobe would develop here. This explains why in Digitaria digitata (and other species of the genera mentioned above) the proﬁles of ribs in the direction of advance are stepped, but in the opposite direction they are smooth (Fig. 11), since here the mantle margin would, on the contrary, be locally stretched.

Fig. 11. Outlines (in plain view) of growth-rate-dependent oblique ribs. Rib edges are lobulate in the direction of displacement, but smooth in the opposite direction. A: Digitaria digitaria (EPUGR.BV.65). Rib displacement is towards the anterior direction. B: Acila sp. (MNHN, unreg.). Rib displacement is towards the posterior direction. a, anterior direction; d, dorsal direction; p, posterior direction.

Fabricational Models Based on Mantle Fig. 10. Solecurtus philipinensis (MNCN 15.07/4768). Rib for- Sensitivity and Contact-Guidance mation is inhibited after the juvenile shell margin has been damaged, except for one retroverse (posteriorly directed) rib, I have proposed several possibilities by which bi- which extinguishes upon meeting the nearest proverse rib. The shell homologous to the damaged margin remains smooth but is valves may fabricate their different varieties of later invaded by ribs running anteriorly. d, dorsal direction; p, oblique ribs. In all cases the mantle epithelium is posterior direction. assumed to be quite sensitive (via mechanorecep- 204 A.G. CHECA margin, so that the information available to the mantle is reduced. Thus, the mantle appears to be able to sense the position of the rib, but not its orientation. From the material examined (Table 1), the Semelidae Abra petiti and the Tellinidae Ma- coma dispar and Tellina trilatera can be confidently included here; this applies, with all likelihood, to the three listed species of Unionoida. From the above, it is clear that, besides mantle behavior, the shape of the growth front is also a major constraint on the mode of rib fabrication. Inclusion of specimens from the literature in either group is difficult unless conclusive features are apparent in the illustrations. Such a classification is shown in Figure 2. First, it is clear that the RCG mode is comparatively more common and has a Fig. 12. Fabrication of ribs in Digitaria digitaria. The mantle wider systematic distribution (also in fossil groups; extrudes from the shell and pushes laterally, with the formation of a compression lobule in the direction of rib displacement. pers. obs.). In relation to this, RCG and SCG have some systematic significance in that they show some restriction to major bivalve groups. The RCG mode tors) and the mantle itself to be capable of complex is the only one in Nuculoida, Mytiloida, Unionoida, behavior, enabling it to align the new growth incre- and the two recorded species of Pholadomyoida. ments in the necessary direction. The above cases Within the Veneroida, lucinids and venerids and the can be classified into two main fabricational strate- only cardiid and donacid construct their oblique ribs gies according to the SCG mode and the same applies to Strict contact guidance (SCG). Bivalves in- neoleptonids, astartids, mactrids, semelids, psam- cluded in the first four fabricational cases above mobiids, and solecurtids. Tellinidae is the family belong here. All these forms have in common a re- containing the greatest number of species and the flected shell margin, which implies that the mantle only one combining both fabricational modes. All is able to project far enough onto the outer shell four tellinid species with RCG mode display discon- surface (species of Divaricellinae and Chamelea, and tinuous ornamentation of the kind found in Tellina in Nemocardium lyratum) or perpendicular to it scobinata (see above for comments on this species). (species of Tellina and Donax madagascariensis), so Unpublished results indicate that oblique ribs with as to sense the already-formed relief of the growth RCG mode of fabrication emerged as early as the margin (Fig. 13, left). In this view, the sensitive Middle Devonian. This mode dominated the Paleo- mantle is able to record this information, which, zoic and Mesozoic fossil record of oblique ribs and once processed in the cerebropleural and visceral emerged repeatedly both in epibenthic (Modiomor- ganglions (which innervate the anterior and poste- phoida, Pectinoida, Mytiloida, and Pterioida) and rior areas of the mantle, respectively), enables the mantle to align new growth increments of the ribs in the adequate directions: either at a 1a) constant, 1b) permanently, or 1c) periodically increasing angle to the growth margin or 2) in an alternating way between growth episodes. This implies elaborate genetically based behavior. This pattern can probably be attributed also to the species of Ctena and Gafra- rium listed in Table 1. Reduced contact guidance plus constant lateral shift (RCG). Each time a new growth increment is to be formed, the mantle extrudes slightly from the shell edge and pushes laterally by muscular action, being displaced laterally a certain distance. Of the six genera secreting growth-rate- dependent oblique ribs (see above), only in Gari (Fig. 13, right) and Strigilla is the mantle noticeably reflected. This is not the case in Acila, Nuculana, Digitaria, and Solecurtus, in which the shell edge is wedge-shaped and more or less pointed (Fig. 13, Fig. 13. Transverse shell profiles of bivalves with SCG (left) right). In these shells, rib undulations are impressed and RCG (right) modes of growth. Arrows indicate the maximum on the inner shell surface only towards the very extension of the mantle margin during rib construction. FABRICATION OF OBLIQUE RIBS IN BIVALVES 205 differs from the SCG fabricational model in that the shell edge is acute and not reflected as in, e.g., Nemocardium lyratum or Donax madagascariensis. In some specimens it is easy to see that riblets are parallel or almost parallel to tiny cracks produced on the shell (Fig. 14A,B). These cracks are determined by the arrangement of crystallites of the calcitic prismatic outer shell sublayer. In shells fractured

Fig. 14. Lithophaga lithophaga. A: Lateral view of specimen EPUGR.BV.311 showing straight ribs perpendicular to growth lines. Tiny cracks (thin black lines) coinciding with antimarginal riblets are visible where the black periostracum has been eroded. B: SEM view of the lateral area of another specimen (EPUGR.BV.303), which reveals cracks coinciding with the elongation of calcitic prisms of the outer shell layer, both being transverse to growth lines. p, posterior direction; v, ventral direction. endobenthic (Pholadomyoida, Nuculoida, Trigo- nioida, and Veneroida) bivalves. The first record of ribs with undoubted SCG mode of fabrication is Lower Eocene (Divaricellinae) and since then this mode has been restricted to the same families as it is today. Fig. 15. Aspect of the shell-secreting mantle surface in bivalves with oblique (A) and longitudinal (B) ribs. A: Digitaria digitaria (EPUGR.BV.68). The distance shown spans five to seven ribs and the mantle surface is homogeneous at this mag- Other Patterns nification. B: Acanthocardia aculeata (EPUGR.BV.261, left valve mantle). The mantle shows three expansions, each secreting a The microornamentation of Lithophaga lith- longitudinal rib. a, anterior direction; d, dorsal direction; pg, ophaga can be classified as straight (Fig. 14A), but periostracal groove. 206 A.G. CHECA

Fig. 16. Ontogeny of oblique ribs in several bivalve species. A: Gari squamosa (MNCN 15.07/0142). B: Strigilla polyaulax (EPUGR.BV.202). C: Digitaria digitaria (EPUGR.BV.62). D: Acila castrensis (EPUGR.BV.106). In A, B, and C oblique ribs initiate as commarginal and later diverge progressively. Early ribs in D are already commarginal. a, anterior direction; d, dorsal direction; p, posterior direction. transversely, prisms reach the shell’s surface at an patterns, but such a fabricational model cannot be angle of some 30° (see also Carter et al., 1990), established here due to lack of evidence. while, in surface view, they are transverse to growth lines (Fig. 14B). Therefore, rib elongation coincides Morphogenetic Classification of Ribbing with the surficial component of crystal growth. Patterns in Bivalves Hayami and Okamoto (1986) also observed concordance between growth directions of calcite laths and The present fabricational models are based on microornamentation in the pectinid Delectopecten. mantle sensitivity and behavior and imply that The possibility exists that crystal growth governs when a new increment of growth is to be secreted the the orientation of particular antimarginal ribbing surface of the extruded mantle has to deform in FABRICATION OF OBLIQUE RIBS IN BIVALVES 207 order to adapt to the previously formed relief of the outer shell surface. After shell secretion, the mantle has to revert to a flat, undifferentiated shape. There- fore, replication of rib profiles by the mantle is only temporary, restricted to periods of active rib secretion. SEM observation of the mantle surface of Digi- taria digitaria (Fig. 15A), Chamelea gallina, and Solecurtus strigilatus support this model. In the three cases, the surface of the shell-secreting mantle epithelium is smooth at low magnification (at the appropriate higher magnification epithelial sensory structures, e.g., ciliary tufts, are characteristic of the bivalve mantle; e.g., Waller, 1980) and without Fig. 18. From the standpoint of constructional morphology, traces of the corresponding ribs (Fig. 15A). A homo- the morphogenesis of oblique ribs is the interaction of three mutually influential biological parameters. Biomineralization de- geneous, undifferentiated mantle is also found in termines the shape and extent of the shell growth front. Mantle venerids with commarginal ribs (observations on Ve- structure influences the pattern of biomineralization and re- nus verrucosa, V. nux, and Dosinia exoleta) at this stricts the fabricational possibilities of the mantle. Genetically magnification. This contrasts with what is observed based mantle behavior determines the mode of fabrication and, in in bivalves having purely radial ribs at a similar turn, depends on mantle structure. magnification. In two species of Cardiidae (Acantho- cardia aculeata [Fig. 15B], Cerastoderma edule) and three of Pectinidae (Pecten jacobeus, Chlamys oper- 16A], Strigilla polyaulax [Fig. 16B], and Tellina lin- cularis, and Chlamys varia), particular relief is vis- guafelis) or incomplete (Digitaria digitaria [Fig. ible on the mantle margin corresponding each to a 16C], Nemocardium lyratum) commarginal ribs. Ex- longitudinal rib. These can be interpreted confi- ceptions are Acila castrensis (Fig. 16D) and Donax dently as areas of the mantle specialized for rib madagascariensis, in which initial ribs are already secretion. oblique. A morphogenetic relationship between oblique Checa and Jimeńez-Jimeńez (1999) established a and commarginal ribs can be established also on the fourth morphogenetic model for the ribs of ostreoids, basis of two other facts. First, the bivalves display- which were interpreted as antimarginal folds ing intermediate patterns have been discussed (see formed by an allometrically growing mantle margin above for comments on Chamelea and Tellina pala- (see above). These authors noted that the mantle tum). Additionally, nine species show the ontogeny margins in Ostrea edulis and Crassostrea angulata of oblique ribs, which initiate as complete (Divalu- are also undifferentiated, resembling those of spe- cina cumingi, Caelatura bakeri, Gari squamosa [Fig. cies with oblique ribs. Therefore, ribs of bivalves can be classified into four main morphogenetic categories (Fig. 17): 1) radial, 2) commarginal, 3) oblique, and 4) antimarginal. Only radial ribs are secreted by a mantle developing particular and permanent rib-secreting areas, while in categories 2–4 the mantle is undifferentiated. Commarginal and oblique ribs cannot be separated completely from the morphogenetic standpoint for the reasons stated above.

CONCLUSIONS The present models, based on contact-guidance mechanisms, explain most, if not all, modalities of oblique ribs. On the contrary, earlier interpreta- tions, based either on reaction-diffusion processes or neural activation, cannot cope with some of the most typical divaricate patterns (e.g., straight and discontinuous) or details of others (rib orientation in lucinids, serrated profiles in Digitaria or Acila, progres- Fig. 17. Morphogenetic classification of bivalve ribs. Radial sive obliquity in Chamelea). ribs are secreted by differentiations of the mantle, while antima- While reaction-diffusion models propose an origin rginal, commarginal, and oblique (sensu stricto) ribs correspond to different fabricational strategies of an undifferentiated mantle. at the molecular (cellular) level, the present contact- Some cases are intermediate between oblique and commarginal guidance model considers the mantle to be the mor- (e.g., Chamelea ribs, see text). phogenetic unit. In this regard, it is consistent with 208 A.G. CHECA the neural model, which is based on the nonlocal Salas (Universidad de Ma´laga, Spain; S.G., formerly properties of nerve nets and relate directly to the at the Museúm National d’Histoire Naturelle, anatomy of the mantle. In addition, the net neural Paris), and Jose´ Templado (Museo Nacional de Cien- stimulation depends on the ability of the mantle to cias Naturales, Madrid). The manuscript signifi- sense the pigment previously secreted. This organ, cantly benefited from the critical revision of two therefore, has a much more complex behavior than anonymous referees. David Nesbitt revised the En- previously thought. Contact-guidance mechanisms glish text. have also been invoked to explain some morphological features in gastropods (Hutchinson, 1989; Savazzi, 1990; Checa et al., 1998) LITERATURE CITED Nevertheless, some aspects of the formation of oblique ribs remain to be explained by our fabrica- Beesley PL, Ross GJB, Wells A, editors. 1998. Mollusca: the southern synthesis, vol. 5, part A. Melbourne: CSIRO Publish- tional models. In particular, after damage to the ing. margin has led to non-ribbed areas in the subse- Carter JG, Lutz RA, Tevesz MJS. 1990. Shell microstructural quently formed shell, the remaining ribs usually data for the Bivalvia. Part VI. Orders Modiomorphoida and (but by no means always; Fig. 10) accelerate their Mytiloida. In: Carter JG, editor. Skeletal biomineralization: lateral displacement in order to invade the adjacent patterns, processes and evolutionary trends, vol. I. New York: Van Nostrand Reinhold. p 391–411 empty space and to distribute more uniformly (fig. 7, Checa AG. 1993. Non-predatory shell damage in Recent deep- Meinhardt and Klinger, 1987). In other instances endobenthic bivalves from Spain. Palaeogeogr Palaeoclimatol new ribs are able to develop spontaneously within Palaeoecol 100:309–331. the smooth area (forming a “∧” pattern). Both fea- Checa AG, Jimeńez-Jimeńez AP. 1999. A mechanical model for rib formation in Ostreoidea. Biol Evol Bivalvia (Abstr). Mala- tures are adequately simulated by theoretical mod- cological Society of London. p 12. els (e.g., Meinhardt, 1995)—that is, long refractory Checa AG, Jimeńez-Jimeńez AP, Rivas P. 1998. Regulation of periods lead to increased activator concentration, spiral coiling in the terrestrial gastropod Sphincterochila:an thereby triggering pattern formation. An alternative experimental test of the road-holding model. J Morphol 235: explanation could be that features of this kind are 249–257. Ermentrout B, Campbell J, Oster G. 1986. A model for shell controlled by the intimate structure of the mantle patterns based on neural activity. Veliger 28:369–388. margin. For example, muscular waves could deter- Hayami I, Okamoto T. 1986. Geometric regularity of some oblique mine rib distribution (wavelength), whereas fiber sculptures in pectinids and in other bivalves: recognition by arrangement could control the direction of rib prop- computer simulations. Paleobiology 12:433–449. Hutchinson JMC. 1989. Control of gastropod shell shape; the role agation. Future research will be devoted to deter- of the preceding whorl. J Theor Biol 140:431–444. mine the underlying mantle structure in particular Lindsay DT. 1982a. Simulating molluscan shell pigment lines bivalve species with oblique ribs. and states: implications for pattern diversity. Veliger 24:297– It should be stressed that the present model ac- 299. counts only for oblique ribs, but cannot be applied to Lindsay DT. 1982b. A new programmatic basis for shell pigment patterns in the bivalve mollusc Lioconcha castrensis (L.). Dif- color bands or lines, which constitute a morphoge- ferentiation 21:32–36. netically unrelated subject. Meinhardt H. 1982. Models of biological pattern formation. New The present study is based on the methods of York: Academic Press. Seilacher’s (Seilacher’s 1970, 1973, 1991) construc- Meinhardt H. 1984. Models for positional signalling, the threefold subdivision of segments and the pigmentation pattern of mol- tional morphology or morphodynamics, which con- luscs. J Embryol Exp Morphol 83 (Suppl):289–311. siders fabricational defects to be essential informa- Meinhardt H. 1995. The algorithmic beauty of sea shells. Berlin: tion for reconstructing the morphogenetic process. Springer-Verlag. From this perspective, the morphogenesis of oblique Meinhardt H, Klinger M. 1987. A model for pattern formation on ribbing patterns in bivalves results from the inter- the shell of molluscs. J Theor Biol 126:63–89. Murray J. 1981. A pre-pattern formation mechanism for animal action of three factors (Fig. 18): 1) the growth pat- coat patterns. J Theor Biol 88:161–199. tern (in particular, the pattern of biomineraliza- Murray J. 1988. How the leopard gets its spots. Sci Am 258:80– tion); 2) the quality of biological materials (mantle 87. structure); and, intimately related to this, 3) mantle Oster G, Murray J. 1989. Pattern formation models and develop- mental constraints. J Exp Zool 251:186–202. behavior. Mantle behavior is undoubtedly geneti- Oster G, Murray J, Harris A. 1983. Mechanical aspects of cally based and constitutes an intermediate stage mesenchimal morphogenesis. J Embryol Exp Morphol 78:83– between the genetic-molecular level and the pheno- 125. type. Oster G, Murray J, Maini P. 1985. A model for chondrogenic condensations in the developing limb: the role of extracellular matrix and cell tractions. J Embryol Exp Morphol 89:93–112. ACKNOWLEDGMENTS Savazzi E. 1983. Constructional morphology of cardiid bivalves: an overview. Boll Soc Paleontol Ital 22:87–91. I am particularly indebted to all those who pro- Savazzi E. 1990. Biological aspects of theoretical shell morphol- vided material relevant to this study: Reinhard ogy. Lethaia 23:195–212. Seilacher A. 1970. Arbeitskonzept zur Konstruktions-Morphologie. Schmidt-Effing (Philipps Marburg Universita¨t, Ger- Lethaia 3:393–396. many), Richard Kilburn (Natal Museum, Pieterma- Seilacher A. 1972. Divaricate patterns in pelecypod shells. ritzburg, South Africa), Serge Gofas and Carmen Lethaia 5:325–343. FABRICATION OF OBLIQUE RIBS IN BIVALVES 209

Seilacher A. 1973. Fabricational noise in adaptive morphology. Thayer CW. 1983. Sediment-mediated biological disturbance and Syst Zool 22:451–465. the evolution of marine benthos. In: Tevesz MJS, McCall PL, Seilacher A. 1991. Self-organizing mechanisms in morphogenesis editors. Biotic interactions in Recent and fossil benthic commu- and evolution. In: Schmidt-Kittler N, Vogel K, editors. Con- nities. New York: Plenum Press. p 497–625. structional morphology and evolution. Berlin: Springer-Verlag. Turing AM. 1952. The chemical basis of morphogenesis. Philos p 251–271. Trans R Soc Lond B 237:37–72. Stanley SM. 1969. Bivalve mollusk burrowing aided by discor- Vermeij GJ. 1977. The Mesozoic marine revolution: evidence from dant shell ornamentation. Science 166:634–635. snails, predators and grazers. Paleobiology 2:245–258. Stanley SM. 1970. Relation of shell form to life habit in the Waddington C, Cowe R. 1969. Computer simulation of a mollus- Bivalvia. Geol Soc Am Mem 125:1–296. can pigmentation pattern. J Theor Biol 25:219–225. Stanley SM. 1975. Why clams have the shape they have: an Waller TR. 1980. Scanning electron microscopy of shell and man- experimental analysis of burrowing. Paleobiology 1:48–58. tle in the order Arcoida (Mollusca: Bivalvia). Smithsonian Stanley SM. 1988. Adaptive morphology of the shell in bivalves Contr Zool 313:1–58. and gastropods. In: Trueman ER, Clarke MR, editors. The Waller TR. 1986. A new genus and species of scallop (Bivalvia: Mollusca, vol. 11. Form and function. San Diego: Academic Pectinidae) from off Somalia, and the deﬁnition of a new tribe Press. p 105–141. Decatopectinini. Nautilus 100:39–46.