JOURNALOFMORPHOLOGY254:195–209(2002) FabricationalMorphologyofObliqueRibsinBivalves AntonioG.Checa* DepartamentodeEstratigrafı´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(ChecaandJime´nez-Jime´nez, 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 ayPaleontolog´aı ,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 ©2002WILEY-LISS,INC. 196 A.G. CHECA 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