Fabricational Morphology of Oblique Ribs in BivalvesAntonio G. Checa*

Departamento de Estratigrafı́a y Paleontologı́a, Facultad de Ciencias, Universidad de Granada, 18071 Spain

ABSTRACT The formation of oblique ribs of bivalveshells usually has been attributed to processes of reaction-diffusion of morphogens from cell to cell at the mantlemargin or neural activation and lateral inhibition in themantle. In particular, such ribs appear with high rates oflateral diffusion. Nevertheless, theoretical models fail toexplain either partially or wholly some varieties of obliqueribs. After surveying the modes of formation of the shelland oblique ribs by the bivalve mantle and associatedfabricational defects, I have determined that the mantle isable to develop an elaborate behavior in order to displacethe rib in a particular direction during growth. The man-tle margin is, therefore, not only the shell-secreting organ,but also the main morphogenetic unit. In particular, thereare two main fabricational strategies. In forms with strictcontact guidance (SCG) the mantle is able to project farenough beyond the shell margins so as to feel the alreadyformed reliefs and to align new growth increments of theribs in the appropriate directions. The shell margin isalways strongly reflected. In bivalves with reduced contactguidance plus constant lateral shift (RCG), the margin isusually acute and the information about ribs available tothe mantle is reduced. During rib construction the mantleextrudes slightly from the shell edge and then pusheslaterally by muscular action; in this way, the new growthincrement of the rib is displaced laterally on a small scale.The contact-guidance model is supported also by the ho-mogeneous structure of the shell-secreting mantle. Fromthe morphogenetic standpoint, oblique ribs are related tocommarginal ones and both differ completely from otherribbing patterns of bivalves. J. Morphol. 254:195–209,2002. © 2002 Wiley-Liss, Inc.

KEY WORDS: constructional morphology; morphogene-sis; shell sculpture; oblique ribs; bivalves

Bivalves display essentially three ribbing pat-terns: radial, commarginal, and oblique. Radial ribscan be defined as helicospirals that converge to-wards the umbo and correspond to the growth tra-jectories of definite portions of the mantle special-ized for rib secretion (see below). Commarginal ribsare parallel to the margin and are secreted by amantle that extrudes periodically all along its exten-sion above the normal shell profile. Both patternscharacterize large groups of bivalves; for example,pectinids, arcoids, or cardiids all have the radial asthe only ribbing pattern, whereas crassatellids ortellinids display exclusively commarginal ribs. Insome other groups (Lucinidae, Veneridae, Psammo-biidae) both radial and commarginal ribs may coex-ist, occasionally on the same shell (e.g., species of

Periglypta or Chione), producing cancellate orna-mentation. A third kind, here called oblique, is lesscommon than the other two types. Oblique ribs canbe defined as having directions that are intermedi-ate between radial and commarginal. These mayrevert to commarginal towards the anterior or pos-terior sides of the shell, or both. Several varieties areincluded within this general term (Fig. 1). There canbe one or more branches oblique to the margin, inwhich case the terms “single oblique” and “divari-cate” (i.e., divergent) are respectively applied. Some-times divaricate ribs are composed of discrete ele-ments that alternate over consecutive growthstages, producing a discontinuous pattern. Mostoblique ribs change their direction progressively tomaintain a constant angle with the margin. Excep-tions to this rule are straight ribs, which can bedefined as single oblique or divaricate ribs that fol-low a straight alignment. Therefore, they begin asparallel to the margin and progressively angle withgrowth. The last variety is antimarginal (sensuWaller, 1986). These ribs diverge from the shell cen-ter to remain perpendicular or at a high angle to theshell margin throughout growth. Ribs of this kindare also peculiar in being highly irregular in distri-bution and morphology. Contrary to the other types,this pattern is taxonomically restricted, being exclu-sive to the Ostreoidea and Plicatuloidea. Antimar-ginal ribs are morphogenetically distinct from othertypes of oblique ribs (Checa and Jiménez-Jiménez,1999) and, consequently, will not be included in thisstudy.

Oblique ribs are not exclusive to any supraspecifictaxon, with the exception of some genera of theDivaricellinae (Lucinoidea). A total of 176 Recentspecies displaying oblique patterns has been re-corded from the literature and from museum speci-

Contract grant sponsor: DGESIC (MEC); Contract grant number:PB97-0790; Contract grant sponsor: Research Group (PAI, JA); Con-tract grant number: RNM-0178.

*Correspondence to: Antonio G. Checa, Departamento de Estrati-grafı́a y Paleontologı́a, Facultad de Ciencias, Universidad deGranada, Avenida Fuentenueva s/n, 18071 Granada, Spain.E-mail: acheca@ugr.es

Published online 00 Month 2002 inWiley InterScience (www.interscience.wiley.com)DOI: 10.1002/jmor.10028

JOURNAL OF MORPHOLOGY 254:195–209 (2002)

© 2002 WILEY-LISS, INC.

mens, the taxonomic distribution of which is shownin Figure 2. An uneven distribution appears amongsubclasses and orders, most species clustering

around Protobranchia, Palaeoheterodonta, and Het-erodonta. At the superfamily level, the same appliesto Tellinoidea, Unionoidea, Veneroidea, Mytiloidea,

Fig. 1. Varieties of oblique ribs illustrated by selected bivalves. Single oblique and divaricate ribs maintain a more or less constantangle with respect to the shell margin, while in straight ribs this angle increases with size. The ribs of Tellina scobinata arediscontinuous, composed of elements that alternate with growth episodes. Antimarginal ribs meet the shell margin transversely or ata high angle and are exclusive to the Ostreidae and Plicatulidae.

Fig. 2. Distribution of oblique ribs and their mode of formation in Recent bivalve species withoblique ribs. Ostreina (� Pectinina � Ostreoida), with exclusively antimarginal ribs, are notincluded. Systematic arrangement after Beesley et al. (1998). RCG, reduced contact-guidance plusconstant lateral shift; SCG, strict contact-guidance.

196 A.G. CHECA

and Lucinoidea, in descending order. This distribu-tion hardly reflects the fossil record of bivalves withoblique ribs. Ongoing research indicates that thehistory of oblique ribs began in the Middle Ordovi-cian with some Modiomorphoida (now extinct). Thescanty Paleozoic record is composed primarily ofpholadomyoids, together with a few pectinoids, pte-rioids, and nuculoids. Pholadomyoids and particu-larly trigonioids (which have no Recent species withoblique ribs) dominate the marine Mesozoic record,whereas in freshwater environments unionoids withdivaricate ribs were already abundant by Late Cre-taceous times. The Cenozoic (post-Paleocene) sawthe substitution of older groups by veneroids (telli-noideans, lucinoideans, and veneroideans), nucu-loids (nuculoideans, nuculanoideans), and mytiloids(mytilids), which progressively yielded the Recentdistribution (Fig. 2). Therefore, the two Recent spe-cies of pholadomyoids with oblique ribs recorded arebut the relict of a formerly flourishing group.Oblique ribs of the asymmetric type (which indicatesan adaptation for faster and more efficient burrow-ing; see below) were absent during the Paleozoic andMesozoic, but were the most common type duringthe Cenozoic. The Cenozoic radiation of bivalveswith asymmetric oblique ribs appears to have had amajor ecological cause and resulted from an adapta-tion to either the Phanerozoic increase in the diver-sity of durophagous predators (e.g., Vermeij, 1977)or the accelerating rate of sediment reworking(Thayer, 1983). In conclusion, oblique ribs emergedseveral times in unrelated groups of both epibenthicand endobenthic bivalves and, therefore, they canhardly be used as a high-ranking systematic andevolutionary character.

Oblique (and, in particular, divaricate ribs) havebeen studied from two well-defined perspectives:function and formation. Constructional morphologystudies have focused primarily on the function ofoblique ribs, which are apparently quite well suitedfor burrowing (Stanley, 1969, 1970, 1975, 1988;Seilacher, 1972, 1973; Savazzi, 1983); this is partic-ularly true of ribs with asymmetric profiles and thatare oriented transverse to the direction of burrow-ing. The fact that oblique ribs facilitate burrowingwas also established quantitatively by Stanley(1975), although it has not yet been demonstratedthat their efficiency surpasses that of commarginalor radial ribs. Another function attributed to divari-cate ribs in Solecurtus is that of minimizing damageto the valve margins during burrowing, by intercept-ing radial breaks and deflecting them back againtowards the margin (Checa, 1993). I have recordedoblique ribs on the shells of a few epibenthic bivalves(e.g., Mytilidae and Chamidae; Fig. 2), for which theonly hypothetical function is that of reinforcing themargin.

A set of theoretical morphology studies has alsodealt with oblique ribbing. Since the pioneeringwork by Waddington and Cowe (1969), formal mod-

els based on activation sites have been used to ex-plain rib and pigment patterns on the shells of mol-luscs (Lindsay, 1982a, b). Other explanationsaddress the formation of biological patterns.Reaction-diffusion mechanisms were originally putforth by Turing (1952) and have been widely appliedto morphogenetic processes (e.g., Murray, 1981,1988; Meinhardt, 1982). The application of reaction-diffusion mechanisms to model shell patterns beganwith Meinhardt (1984) and expanded the field oftheoretical modeling. These models are based on theprinciple that secretion of a structure is initiatedwhen the concentration of an activator substancereaches a certain concentration within a cell orgroup of cells. The activator has an autocatalyticfeedback on its own production. Inhibition of activa-tor production may come either from depletion of asubstrate (activator precursor) or from the forma-tion of an inhibitor, which is produced simulta-neously with the activator (see Meinhardt andKlinger, 1987). Under some conditions, both the ac-tivator and the substrate/inhibitor can diffuse fromone cell to the neighboring ones, which, in this way,become “infested.” Therefore, the signal for the for-mation of the structure (rib or pigment line) shiftslaterally with time, moving along oblique directions.According to the neural model of Ermentrout et al.(1986), the activity of pigment-secreting cells of themantle is regulated by nervous impulses, throughthe neural network that interconnects mantle inner-vations with the central ganglion(s). Therefore,long-range interactions are possible. The model in-corporates short-range excitation and long-range in-hibition, typical of neural nets. An innovation withrespect to previous models is that receptor cells ofthe mantle are able to discriminate between pig-mented and nonpigmented areas of the already-laid-down shell, the former stimulating the mantle tocontinue the pattern. Diagonal pigment strips areobtained with very low excitatory, inhibitory, andsecretion thresholds, which also have gradual cut-offs. Both reaction-diffusion and neural models yieldvery similar results and have been particularly suc-cessful in reproducing shell color patterns, includingmost varieties of oblique ones (e.g., Meinhardt,1995).

In opposition to chemical models, mechanochemi-cal models of morphogenesis propose that signalingmechanisms (involving chemical gradients set up bydiffusion) cause motile cells to clump together andthat the traction forces caused by aggregation canbring about instabilities that lead to further pat-terning (Oster et al., 1983, 1985; Oster and Murray1989). Therefore, chemical and mechanical pro-cesses interact continuously to produce both thechemical pattern and the form-shaping movements.Mechanochemical models have been applied to avariety of situations in embryology but their pro-spective usefulness to model patterns of shell orna-ment remains to be investigated.

197FABRICATION OF OBLIQUE RIBS IN BIVALVES

Despite their success, theoretical models (partic-ularly of the chemical type) currently fail to be test-able, since the activator and inhibitor/substratesubstances (the so-called morphogens in reaction-diffusion processes or excitation-inhibition sub-stances in the neural model) have not yet been de-tected. There is no biochemical proof that thesemodels reproduce the process of formation, and notmerely the pattern. In the case of animals withaccretionary skeletons (e.g., bivalve molluscs) thereare some naturally occurring rib patterns that arenot explained by theoretical models. Reaction-diffusion models require constant rates of lateraldiffusion, so that ribs or color lines should maintaina constant angle with the shell margin. This is notthe case with straight oblique ribs (Fig. 1), in whichsuch angles reduce with growth. According to theo-retical models, the angle between ribs and growthlines should also vary depending on the rate of localmarginal growth. In bivalves, this angle should de-cline accordingly from the venter to the umbo alongthe margin corresponding to a given growth momentin coincidence with the rate of marginal growth.This is not the case in actual shells (see below; Fig.3). Finally, some patterns are discontinuous andalternating (Figs. 1, 7, 8), while the cell-to-cell dif-fusion model predicts a continuous structure. Norcan a neural model be applied to these situations,since it implies that the already secreted structureshould stimulate further structure formation, whileduring the formation of actual discontinuous alter-

nating patterns the former scale inhibits additionalscale formation (see below).

In the search for alternative explanations, themethods of constructional morphology have been ap-plied here to oblique ribbing patterns but from anessentially fabricational viewpoint. In our approach,a main point is the reconstruction of the fabricationprocess, i.e., the sequence of movements of the man-tle margin during shell (and rib) secretion. To arriveat a fabricational model, we have integrated theinformation from the shell structure, the geometryof growth lines, and the “defects” that arose duringthe secretion process (fabricational noise sensuSeilacher, 1973).

MATERIALS AND METHODS

Specimens (some including the soft parts) belonging to 45 bi-valve species were studied (Table 1). The material comes essen-tially from three institutions: Departamento de Estratigrafı́a yPaleontologı́a, Universidad de Granada (EPUGR), Muséum 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 systematicdistribution within the Bivalvia.

Surficial microornament and microstructure were observedboth with SEM (Zeiss DSM 950) and binocular microscopy atmagnifications ranging from �10 to �2,000. Fractured shellswere examined intact or polished (previously embedded in epoxyresin); they were studied unaltered or corroded with either 5%sodium hydroxide or 1% hydrochloric acid to remove the perios-tracum and intercrystalline organic matter or calcium carbonate,respectively. The mantles of Solecurtus strigilatus (Linnaeus)and Digitaria digitaria (Linnaeus) were observed with SEM,which required fixation in cacodylate buffered (0.1 M, pH 7.4)2.5% glutaraldehyde, followed by dehydration in increasing con-centrations of ethanol and critical-point drying.

RESULTS AND DISCUSSIONObservation and Inferred Mode ofFabrication of Oblique Ribs

The mode of shell and rib fabrication was studiedextensively in some species, in which the availabilityof material permitted destructive techniques. Fabri-cational patterns in other species were inferred fromspecies showing identical external morphologicalfeatures.

Oblique ribs in Divaricellinae (Lucinoidea).The genera Divaricella, Divalinga, and Divalucinadisplay archetypical divaricate patterns. In all thespecies examined the divergence axis of the ribsruns in a ventral, slightly anterior direction (Figs. 1,3). Ribs, regardless of their position on the shell,form a similar angle with growth lines. In theunique case of Divaricella quadrisulcata, normalgrowth lines are replaced on the ribs by dorsallyconcave and wider growth lines, which fade out onthe gentle slopes of the ribs (Fig. 4A). Transversesections reveal that these unusual growth lines cor-respond to deposits of aragonite fibers perpendicularto the shell surface (Fig. 4B), which cover the fibrousprismatic shell and hidden shell growth lines. The

Fig. 3. Divaricella cumingi (MNHN, unreg.). Divaricate ribsform constant angles with growth lines throughout the shell.After a prolonged halt in growth (arrow), the concordance be-tween ribs is lost and new ribs are offset with respect to the axisof divergence. a, anterior direction; d, dorsal direction.

198 A.G. CHECA

morphology of growth lines and the orientation offibers imply that these secondary deposits are cre-ated by acute backward extensions of the mantle

margin, each of these reflecting onto a rib as themain shell margin was being secreted (Fig. 5). Theseextensions take the form of pointed tongues, with

TABLE 1. Details of taxa and specimens investigated

Taxon LocalityNo. of specimens, repository

and reg. no.

NuculoidaAcila beringiana (Dall, 1919) Bering Sea 2 � 1, EPUGR.BV.104Acila castrensis (Hinds, 1843) NW Puget Sound 3 � 2, EPUGR.BV.106–107Acila divaricata (Hinds, 1843) Taiwan, offshore Taipei 3 � 2, EPUGR.BV.108–109Acila fultoni Smith, 1892 Bengal Bay, India 4 � 2, MNHN (unreg.)Acila sp. Philippines (loc. unknown) 5 � 2, MNHN (unreg.)Nuculana bicuspidata Gould, 1845 Senegal 4 � 2, EPUGR.BV.102–103Nuculana cellulite Dall, 1896 Tillamook Bay, Washington 3 � 2, EPUGR.BV.110–111MytiloidaIschadium recurvum (Rafinesque, 1820) N America (loc. unknown) 6 � 2, MNHN (unreg.)Gregariella sulcata (Risso, 1826) Marbella, SE Spain 1 � 2, EPUGR.BV.130Lithophaga lithophaga (Linnaeus, 1758) Mediterranean (loc. unknown) 23 � 2, EPUGR.BV.300–322Septifer bilocularis (Linnaeus, 1758) Phuket, Thailand 2 � 2, EPUGR.BV.133–134UnionoidaCaelatura bakeri (Adams, 1866) Nyanza 17 � 2, MNHN (unreg.)Lamprotula sp. China (loc. unknown) 7 � 2, MNHN (unreg.)Lasmigona costata (Rafinesque, 1820) Ohio (loc. unknown) 1 � 2, MNHN (unreg.)VeneroidaCtena bella (Conrad, 1837) W Australia (loc. unknown) 1 � 2, EPUGR.BV.200Divalinga eburnea Reeve, 1850 La Paz, México 1 � 2, EPUGR.BV.201Divalucina cumingi (Adams and Angas, 1863) a. South Coast of Natal, South Africa 37 � 1, MNHN (unreg.)

b. Loc. unknown 2 � 2, MNHN (unreg.)Divaricella gibba (Gray, 1825) Port Gentil, Gabon 4 � 1, MNHN (unreg.)Divaricella dentata (Wood, 1815) Florida Keys 43 � 1, MNHN (unreg.)Divaricella quadrisulcata (Orbigny, 1842) Isla Mujeres, México 5 � 1, EPUGR.BV.94–98Digitaria digitaria (Linnaeus, 1758) Barbate, S Spain 5 � 2, EPUGR.BV.62–68Nemocardium lyratum (Sowerby, 1841) a. Philippines (loc. unknown) 4 � 2, MNCN (unreg.)

b. Laminusa Island, Philippines 1 � 2, EPUGR.BV.206Donax madagascariensis Wood, 1828 Durban, South Africa 1 � 2, EPUGR.BV.207Gari maculosa (Lamarck, 1818) a. Cebú, Philippines 4 � 2, MNCN 15.07/0005, 15.07/0013,

15.07/0035b. Philippines (loc. unknown) 3 � 2, MNHN (unreg.)

Gari squamosa (Lamarck, 1818) Philippines (loc. unknown) 9 � 2, 1 � 1, MNCN 15.07/0003,15.07/0142

Solecurtus philipinensis (Dunker, 1861) Philippines (loc. unknown) 11 � 2, MNCN 15.07/4768Solecurtus strigilatus (Linnaeus, 1758) a. Almeria coast, SE Spain 3 � 2, EPUGR.BV.142–145

b. Huelva coast, SW Spain 52 � 1, EPUGR.BV.322–373Abra petiti (Dautenberg) Natal South coast 1 � 2, EPUGR.BV.208Macoma dispar (Conrad, 1837) Santa Carolina, Mozambique 1 � 2, EPUGR.BV.209Strigilla carnaria (Linnaeus, 1758) a. Caribbean (loc. unknown) 5 � 2, 1 � 1, MNHN (unreg.)

b. Venezuela (loc. unknown) 1 � 2, EPUGR.BV.223Strigilla pisiformis (Linnaeus, 1758) Caribbean (loc. unknown) 23 � 1, MNHN (unreg.)Strigilla polyaulax (Tomlin and Shackelford, 1915) a. Pointe Noire, Congo Brazzaville 2 � 2, EPUGR.BV.202–203

b. Luanda, Angola 1 � 2, EPUGR.BV.204Tellina linguafelis (Linnaeus, 1758) Bowenstand, Australia 1 � 2, EPUGR.BV.210Tellina palatum (Iredale, 1929) Siasi, Philippines 2 � 2, EPUGR.BV.211–212Tellina scobinata (Linnaeus, 1758) a. Bushy Island, Australia 1 � 2, EPUGR.BV.213

b. Loc. unknown 1 � 2, MNHN (unreg.)Tellina trilatera Gmelin Muizenberg, South Africa 2 � 2, EPUGR.BV.214–215Chamelea gallina (Linnaeus, 1758) Granada coast, SE Spain 103 � 2, EPUGR.BV.373–475Chamelea striatula (da Costa, 1778) Málaga coast, SE Spain 15 � 2, EPUGR.BV.476–490Circe intermedia Reeve, 1864 Al-nigaiyet, Kuwait 1 � 2, EPUGR.BV.216Circe rivularis Burn, 1778 Reevesby Island, S Australia 2 � 2, EPUGR.BV.217–218Gafrarium dispar (Dillwyn, 1817) Australia (loc. unknown) 1 � 2, EPUGR.BV.219Gafrarium pectinatum (Linnaeus, 1758) Madagascar (loc. unknown) 1 � 2, EPUGR.BV.220Gafrarium tumidum (Röding, 1798) a. Philippines (loc. unknown) 1 � 2, EPUGR.BV.221

b. Guam Island 1 � 2, EPUGR.BV.222Venus verrucosa (Linnaeus, 1758) Almeria coast, SE Spain 12 � 2, 7 � 1, EPUGR.BV.490–508Petricola carditoides (Conrad, 1837) California (loc. unknown) 2 � 2, MNCN (unreg.)

unreg., unregistered; �1, loose valve; �2, specimen with paired valves; EPUGR, Departamento de Estratigrafı́a y Paleontologı́a,Universidad de Granada; MNHN, Muséum National d’Histoire Naturelle, Paris; MNCN, Museo Nacional de Ciencias Naturales,Madrid

199FABRICATION OF OBLIQUE RIBS IN BIVALVES

one side aligned with the rib. This pattern impliesthat in this and the other above-mentioned lucinidsthe mantle keeps abreast of the reliefs occurring atthe shell’s edge and surface. In D. quadrisulcata, theinferred mantle extensions could well align the new

growth increments with the former rib by mere con-tact (contact-guidance mechanism). Assuming a con-stant diffusion rate, reaction-diffusion models pre-dict that ribs must deflect laterally during periods ofreduced growth rate of the shell, since the rate oflateral displacement remains the same. This isnever the case in lucinids—conversely, ribs main-tain a constant angle with growth lines even atconspicuous regions of growth cessation. After someprolonged halts in growth a new shell forms belowthe old one and the abandoned margin remainsraised. In this case, the mantle is inferred to losecontact with the former margin, producing a new,independent arrangement of ribs, which are nowmore closely spaced than previously (Fig. 3), andtherefore resemble a more juvenile stage. How thisnew arrangement arises in the absence of the formertemplate is unknown, but it could well be producedby muscular waves of the mantle edge. Only in Di-varicella dentata do ribs project markedly from themargin parallel to the shell surface, giving a dentic-ulate appearance in plain view. This providescontact-guidance across growth episodes separatedby a raised margin.

Straight ribs of Nemocardium lyratum (Car-dioidea) and Donax madagascariensis (Telli-noidea). In Nemocardium lyratum ribs developonly on the anterior and central areas of the shell.They run straight or slightly curved in either direc-tion and are regularly spaced (Fig. 1). This pattern isunusual among bivalves in that each rib originatesparallel to the margin and, upon growing, crossesthe successive margins at increasing angles. This isespecially evident towards the anteriormost side,where the angle of intersection may reach some 80°.Savazzi (1983) showed that terraces in N. lyratumare not continuous into the shell, but are depositsformed on the periostracum by a reflecting mantle,in a way similar to Divaricella quadrisulcata. InDonax madagascariensis (Fig. 1), ribs are commar-ginal at the posterior side of the shell but as soon asthey cross the crest delineating the posterior areathey run straight and become increasingly oblique to

Fig. 5. Model for the fabrication of ribs in Divaricellaquadrisulcata. The mantle reflects at the margin and sends outextensions, each onto a rib, which secrete secondary deposits.

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 tothe presence of secondary prismatic deposits, which bear theirown growth lines. The steep slope appears white. B: SpecimenEPUGR.BV.96, left valve. Transverse section of the shell througha rib. Secondary deposits consist of prisms transverse to theshell’s surface (arrow). a, anterior direction; d, dorsal direction.

200 A.G. CHECA

the growth lines until becoming transverse at theanteriormost end of the shell. The absence of second-ary deposits and the extent of the periostracum in-dicate that the mantle margin reflects, but does notextend backwards enough to adhere to the outershell surface. Since reaction-diffusion models cannotexplain the formation of straight ribs (see above),the contact-guidance mechanism is the only plausi-ble explanation: triangular tongue-like (in N. lyra-tum) or rounded (in D. madagascariensis) mantleextensions must reflect onto or adhere to each rib tipto appropriately align the new growth increments.

Increasingly oblique ribs of Chamelea (Ven-eroidea) and Tellina palatum (Tellinoidea). InChamelea gallina and C. striatula the relationshipbetween growth lines and ribs varies throughoutgrowth. Growth periods begin with purely commar-ginal ridges, but later these ridges become progres-sively oblique with respect to the shell margin to-wards the anterior part of the shell (Fig. 6). Thishappens because the ridges become increasinglycoarse anteriorwards, so that each rib extends for agreater number of growth lines here. Occasionally,after conspicuous halts in growth, which bevel form-ing ribs, these revert to being commarginal (Fig. 6).This pattern can be explained as being formed bymantle waves that propagate anteriorwards. As inlucinids, the shell margin is reflected backwards andthe mantle can touch the outer surface and gainpositional information about its surface relief. InTellina palatum, halts in growth are similarlymarked by commarginal ribs. Further growth is

characterized by the formation of minute divarica-tions and interruptions, producing an apparentlydisorderly pattern. The cyclic and progressive na-ture of these patterns is difficult to explain by the-oretical models, without the corresponding algo-rithm being artificially complicated.

Discontinuous ribs in species of Tellina(Tellinoidea). In Tellina scobinata and T. linguafe-lis, ornamentation is composed of scales projectingperpendicular to the shell’s surface. The scales al-ternate in successive secretion episodes, giving adiscontinuous, rasp-like divaricate pattern (Fig. 1).After secretion of a set of scales the shell margin iswavy, elevated at the scales, and depressed in be-tween. These differences can be detected easily bythe mantle, which now reverses the pattern, project-ing outwards only where an interspace is detected(Fig. 7). This fabricational model explains whyscales become larger with growth and why theirnumbers remain constant, since each interscalegives rise subsequently to one and only one scale;thus, no new elements are introduced, provided thatshell growth is isometric. Fabricational noise in theform of imperfections also fits with a contact-guidance model. In T. scobinata, scales of successivegrowth increments locally become closely spaced,almost fused, during periods of reduced growth (Fig.8A). Fused scales are perceived by the mantle assingle large ones and this translates as a defect thatis transmitted during further growth. In rare in-stances of jagged margins, scales are subsequentlyinduced at the sites in which small pieces have beenchipped 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 Acilachange their orientation with the shell’s growthrate. During periods of reduced growth (inferredfrom closely spaced growth lines) between growthcycles or at maturity, ribs deviate laterally and formangles that are more acute with respect to thegrowth lines (Fig. 9). Measurements by SEM inDigitaria digitaria indicate that the amplitude oflateral jumps increases steadily with valve size,while the distance between growth lines grows ac-

Fig. 6. Chamelea gallina (EPUGR.BV.387). Ribs become pro-gressively oblique to growth lines until a prolonged halt in growth(arrow) is reached. Thereafter, ribs reinitiate as commarginal. a,anterior direction; d, dorsal direction.

Fig. 7. Fabrication model for discontinuous divaricate ribs inTellina scobinata. In a first stage (left) the mantle progressivelyadvances and elevates (thus preforming scales) at the interscalesof the previously formed shell margin. After the new growthincrement has been calcified (right) the process is repeated, butthe position of scales and interscales now alternates.

201FABRICATION OF OBLIQUE RIBS IN BIVALVES

cording to a typical logistic pattern, explaining whythe angle between ribs and growth lines decreases atmaturity. If growth stopped completely, ribs mayeven skip and reappear farther in the direction of ribdisplacement. This implies a constant rate of lateral

displacement with time. A contact-guidance mecha-nism is also implied by the fact that the new shellsecreted after the margin has been extensivelychipped lacks all or some of the ribs—i.e., once theformer template is lost, there is no reference for themantle to continue the pattern. Good examples ofthis are frequent in Solecurtus (Fig. 10) and, to alesser 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. 9. Acceleration of lateral displacement of ribs duringperiods of reduced shell growth. A: Strigilla polyaulax(EPUGR.BV.204). B: Nuculana cellulite (EPUGR.BV.111). d, dor-sal direction; p, posterior direction.

Fig. 8. Fabricational defects in Tellina scobinata. A: SpecimenMNHN (unreg). Coinciding with periods of reduced growth (ar-rows), scales of successive growth increments become fused.Later, the mantle appears to sense them as a single scale, withthe subsequent formation of unusually large scales and inter-scales. B: Specimen EPUGR.BV.213. Arcuate breaks of a jaggedmargin induce the formation of scales. A possible explanation isthat the mantle responds to breaks as though they were incipientscales and completes them when growth is resumed. a, anteriordirection; v, ventral direction.

202 A.G. CHECA

pattern; when the branch running opposite to thenormal direction meets the next regular rib, thesefuse to form a “V” pattern (Fig. 10). Additionally, invery rare instances ribs reinitiate with breaks, as ifthe sharp edges thus formed locally were taken forribs by the organism (fig. 16, Checa, 1993).

Detailed observation reveals that ribs in the spe-cies listed clearly have a step-like appearance inplain view in the sense that ribs seem to shift later-ally by small bursts, a situation that is inconsistentwith a cell-to-cell activation model (Fig. 11). Thus, atevery growth step the lateral jump precedes radialgrowth, as is evident in Acila (Fig. 11B), Strigilla,and particularly Digitaria (Fig. 11A). This pattern isobscured in Solecurtus, since the composite prismsforming the outer shell layer are larger than thepresumed lateral jumps, judging by the distancebetween growth lines. How the bivalve calibrateslateral 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 adpressedagainst the inner surface of the rib slope in thedirection of advance (Fig. 12). Given the viscoelasticnature of the mantle, a compression lobe would de-velop here. This explains why in Digitaria digitata(and other species of the genera mentioned above)the profiles of ribs in the direction of advance arestepped, but in the opposite direction they aresmooth (Fig. 11), since here the mantle marginwould, on the contrary, be locally stretched.

Fabricational Models Based on MantleSensitivity and Contact-Guidance

I have proposed several possibilities by which bi-valves may fabricate their different varieties ofoblique ribs. In all cases the mantle epithelium isassumed to be quite sensitive (via mechanorecep-

Fig. 10. Solecurtus philipinensis (MNCN 15.07/4768). Rib for-mation is inhibited after the juvenile shell margin has beendamaged, except for one retroverse (posteriorly directed) rib,which extinguishes upon meeting the nearest proverse rib. Theshell homologous to the damaged margin remains smooth but islater invaded by ribs running anteriorly. d, dorsal direction; p,posterior direction.

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

203FABRICATION OF OBLIQUE RIBS IN BIVALVES

tors) and the mantle itself to be capable of complexbehavior, enabling it to align the new growth incre-ments in the necessary direction. The above casescan be classified into two main fabricational strate-gies

Strict contact guidance (SCG). Bivalves in-cluded in the first four fabricational cases abovebelong here. All these forms have in common a re-flected shell margin, which implies that the mantleis able to project far enough onto the outer shellsurface (species of Divaricellinae and Chamelea, andin Nemocardium lyratum) or perpendicular to it(species of Tellina and Donax madagascariensis), soas to sense the already-formed relief of the growthmargin (Fig. 13, left). In this view, the sensitivemantle is able to record this information, which,once processed in the cerebropleural and visceralganglions (which innervate the anterior and poste-rior areas of the mantle, respectively), enables themantle to align new growth increments of the ribs inthe adequate directions: either at a 1a) constant, 1b)permanently, or 1c) periodically increasing angle tothe growth margin or 2) in an alternating way be-tween growth episodes. This implies elaborate ge-netically based behavior. This pattern can probablybe attributed also to the species of Ctena and Gafra-rium listed in Table 1.

Reduced contact guidance plus constant lat-eral shift (RCG). Each time a new growth incre-ment is to be formed, the mantle extrudes slightlyfrom the shell edge and pushes laterally by muscu-lar action, being displaced laterally a certain dis-tance. Of the six genera secreting growth-rate-dependent oblique ribs (see above), only in Gari (Fig.13, right) and Strigilla is the mantle noticeably re-flected. This is not the case in Acila, Nuculana,Digitaria, and Solecurtus, in which the shell edge iswedge-shaped and more or less pointed (Fig. 13,right). In these shells, rib undulations are impressedon the inner shell surface only towards the very

margin, so that the information available to themantle is reduced. Thus, the mantle appears to beable to sense the position of the rib, but not itsorientation. From the material examined (Table 1),the Semelidae Abra petiti and the Tellinidae Ma-coma dispar and Tellina trilatera can be confidentlyincluded here; this applies, with all likelihood, to thethree listed species of Unionoida.

From the above, it is clear that, besides mantlebehavior, the shape of the growth front is also amajor constraint on the mode of rib fabrication.

Inclusion of specimens from the literature in ei-ther group is difficult unless conclusive features areapparent in the illustrations. Such a classification isshown in Figure 2. First, it is clear that the RCGmode is comparatively more common and has awider systematic distribution (also in fossil groups;pers. obs.). In relation to this, RCG and SCG havesome systematic significance in that they show somerestriction to major bivalve groups. The RCG modeis the only one in Nuculoida, Mytiloida, Unionoida,and the two recorded species of Pholadomyoida.Within the Veneroida, lucinids and venerids and theonly cardiid and donacid construct their oblique ribsaccording to the SCG mode and the same applies toneoleptonids, astartids, mactrids, semelids, psam-mobiids, and solecurtids. Tellinidae is the familycontaining the greatest number of species and theonly one combining both fabricational modes. Allfour tellinid species with RCG mode display discon-tinuous ornamentation of the kind found in Tellinascobinata (see above for comments on this species).Unpublished results indicate that oblique ribs withRCG mode of fabrication emerged as early as theMiddle Devonian. This mode dominated the Paleo-zoic and Mesozoic fossil record of oblique ribs andemerged repeatedly both in epibenthic (Modiomor-phoida, Pectinoida, Mytiloida, and Pterioida) and

Fig. 13. Transverse shell profiles of bivalves with SCG (left)and RCG (right) modes of growth. Arrows indicate the maximumextension of the mantle margin during rib construction.

Fig. 12. Fabrication of ribs in Digitaria digitaria. The mantleextrudes from the shell and pushes laterally, with the formationof a compression lobule in the direction of rib displacement.

204 A.G. CHECA

endobenthic (Pholadomyoida, Nuculoida, Trigo-nioida, and Veneroida) bivalves. The first record ofribs with undoubted SCG mode of fabrication isLower Eocene (Divaricellinae) and since then thismode has been restricted to the same families as it istoday.

Other Patterns

The microornamentation of Lithophaga lith-ophaga can be classified as straight (Fig. 14A), but

differs from the SCG fabricational model in that theshell 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 areparallel or almost parallel to tiny cracks produced onthe shell (Fig. 14A,B). These cracks are determinedby the arrangement of crystallites of the calciticprismatic outer shell sublayer. In shells fractured

Fig. 15. Aspect of the shell-secreting mantle surface in bi-valves with oblique (A) and longitudinal (B) ribs. A: Digitariadigitaria (EPUGR.BV.68). The distance shown spans five toseven ribs and the mantle surface is homogeneous at this mag-nification. B: Acanthocardia aculeata (EPUGR.BV.261, left valvemantle). The mantle shows three expansions, each secreting alongitudinal rib. a, anterior direction; d, dorsal direction; pg,periostracal groove.

Fig. 14. Lithophaga lithophaga. A: Lateral view of specimenEPUGR.BV.311 showing straight ribs perpendicular to growthlines. Tiny cracks (thin black lines) coinciding with antimarginalriblets 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 elon-gation of calcitic prisms of the outer shell layer, both being trans-verse to growth lines. p, posterior direction; v, ventral direction.

205FABRICATION OF OBLIQUE RIBS IN BIVALVES

transversely, prisms reach the shell’s surface at anangle of some 30° (see also Carter et al., 1990),while, in surface view, they are transverse to growthlines (Fig. 14B). Therefore, rib elongation coincideswith the surficial component of crystal growth.Hayami and Okamoto (1986) also observed concor-dance between growth directions of calcite laths andmicroornamentation in the pectinid Delectopecten.The possibility exists that crystal growth governsthe orientation of particular antimarginal ribbing

patterns, but such a fabricational model cannot beestablished here due to lack of evidence.

Morphogenetic Classification of RibbingPatterns in Bivalves

The present fabricational models are based onmantle sensitivity and behavior and imply thatwhen a new increment of growth is to be secreted thesurface of the extruded mantle has to deform in

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 ascommarginal and later diverge progressively. Early ribs in D are already commarginal. a, anterior direction; d, dorsal direction; p,posterior direction.

206 A.G. CHECA

order to adapt to the previously formed relief of theouter shell surface. After shell secretion, the mantlehas to revert to a flat, undifferentiated shape. There-fore, replication of rib profiles by the mantle is onlytemporary, restricted to periods of active rib secre-tion. SEM observation of the mantle surface of Digi-taria digitaria (Fig. 15A), Chamelea gallina, andSolecurtus strigilatus support this model. In thethree cases, the surface of the shell-secreting mantleepithelium is smooth at low magnification (at theappropriate higher magnification epithelial sensorystructures, e.g., ciliary tufts, are characteristic of thebivalve mantle; e.g., Waller, 1980) and withouttraces of the corresponding ribs (Fig. 15A). A homo-geneous, undifferentiated mantle is also found invenerids with commarginal ribs (observations on Ve-nus verrucosa, V. nux, and Dosinia exoleta) at thismagnification. This contrasts with what is observedin bivalves having purely radial ribs at a similarmagnification. In two species of Cardiidae (Acantho-cardia aculeata [Fig. 15B], Cerastoderma edule) andthree of Pectinidae (Pecten jacobeus, Chlamys oper-cularis, and Chlamys varia), particular relief is vis-ible on the mantle margin corresponding each to alongitudinal rib. These can be interpreted confi-dently as areas of the mantle specialized for ribsecretion.

A morphogenetic relationship between obliqueand commarginal ribs can be established also on thebasis of two other facts. First, the bivalves display-ing intermediate patterns have been discussed (seeabove for comments on Chamelea and Tellina pala-tum). Additionally, nine species show the ontogenyof oblique ribs, which initiate as complete (Divalu-cina cumingi, Caelatura bakeri, Gari squamosa [Fig.

16A], Strigilla polyaulax [Fig. 16B], and Tellina lin-guafelis) or incomplete (Digitaria digitaria [Fig.16C], Nemocardium lyratum) commarginal ribs. Ex-ceptions are Acila castrensis (Fig. 16D) and Donaxmadagascariensis, in which initial ribs are alreadyoblique.

Checa and Jiménez-Jiménez (1999) established afourth morphogenetic model for the ribs of ostreoids,which were interpreted as antimarginal foldsformed by an allometrically growing mantle margin(see above). These authors noted that the mantlemargins in Ostrea edulis and Crassostrea angulataare also undifferentiated, resembling those of spe-cies with oblique ribs.

Therefore, ribs of bivalves can be classified intofour main morphogenetic categories (Fig. 17): 1) ra-dial, 2) commarginal, 3) oblique, and 4) antimar-ginal. Only radial ribs are secreted by a mantledeveloping particular and permanent rib-secretingareas, while in categories 2–4 the mantle is undif-ferentiated. Commarginal and oblique ribs cannotbe separated completely from the morphogeneticstandpoint for the reasons stated above.

CONCLUSIONS

The present models, based on contact-guidancemechanisms, explain most, if not all, modalities ofoblique ribs. On the contrary, earlier interpreta-tions, based either on reaction-diffusion processes orneural activation, cannot cope with some of the mosttypical divaricate patterns (e.g., straight and discon-tinuous) or details of others (rib orientation in lucin-ids, serrated profiles in Digitaria or Acila, progres-sive obliquity in Chamelea).

While reaction-diffusion models propose an originat the molecular (cellular) level, the present contact-guidance model considers the mantle to be the mor-phogenetic unit. In this regard, it is consistent with

Fig. 17. Morphogenetic classification of bivalve ribs. Radialribs are secreted by differentiations of the mantle, while antima-rginal, commarginal, and oblique (sensu stricto) ribs correspondto different fabricational strategies of an undifferentiated mantle.Some cases are intermediate between oblique and commarginal(e.g., Chamelea ribs, see text).

Fig. 18. From the standpoint of constructional morphology,the morphogenesis of oblique ribs is the interaction of threemutually influential biological parameters. Biomineralization de-termines the shape and extent of the shell growth front. Mantlestructure influences the pattern of biomineralization and re-stricts the fabricational possibilities of the mantle. Geneticallybased mantle behavior determines the mode of fabrication and, inturn, depends on mantle structure.

207FABRICATION OF OBLIQUE RIBS IN BIVALVES

the neural model, which is based on the nonlocalproperties of nerve nets and relate directly to theanatomy of the mantle. In addition, the net neuralstimulation depends on the ability of the mantle tosense the pigment previously secreted. This organ,therefore, has a much more complex behavior thanpreviously thought. Contact-guidance mechanismshave also been invoked to explain some morpholog-ical features in gastropods (Hutchinson, 1989;Savazzi, 1990; Checa et al., 1998)

Nevertheless, some aspects of the formation ofoblique ribs remain to be explained by our fabrica-tional models. In particular, after damage to themargin has led to non-ribbed areas in the subse-quently formed shell, the remaining ribs usually(but by no means always; Fig. 10) accelerate theirlateral displacement in order to invade the adjacentempty space and to distribute more uniformly (fig. 7,Meinhardt and Klinger, 1987). In other instancesnew ribs are able to develop spontaneously withinthe smooth area (forming a “∧” pattern). Both fea-tures are adequately simulated by theoretical mod-els (e.g., Meinhardt, 1995)—that is, long refractoryperiods lead to increased activator concentration,thereby triggering pattern formation. An alternativeexplanation could be that features of this kind arecontrolled by the intimate structure of the mantlemargin. For example, muscular waves could deter-mine rib distribution (wavelength), whereas fiberarrangement could control the direction of rib prop-agation. Future research will be devoted to deter-mine the underlying mantle structure in particularbivalve species with oblique ribs.

It should be stressed that the present model ac-counts only for oblique ribs, but cannot be applied tocolor bands or lines, which constitute a morphoge-netically unrelated subject.

The present study is based on the methods ofSeilacher’s (Seilacher’s 1970, 1973, 1991) construc-tional morphology or morphodynamics, which con-siders fabricational defects to be essential informa-tion for reconstructing the morphogenetic process.From this perspective, the morphogenesis of obliqueribbing patterns in bivalves results from the inter-action of three factors (Fig. 18): 1) the growth pat-tern (in particular, the pattern of biomineraliza-tion); 2) the quality of biological materials (mantlestructure); and, intimately related to this, 3) mantlebehavior. Mantle behavior is undoubtedly geneti-cally based and constitutes an intermediate stagebetween the genetic-molecular level and the pheno-type.

ACKNOWLEDGMENTS

I am particularly indebted to all those who pro-vided material relevant to this study: ReinhardSchmidt-Effing (Philipps Marburg Universität, Ger-many), Richard Kilburn (Natal Museum, Pieterma-ritzburg, South Africa), Serge Gofas and Carmen

Salas (Universidad de Málaga, Spain; S.G., formerlyat the Muséum National d’Histoire Naturelle,Paris), and José Templado (Museo Nacional de Cien-cias Naturales, Madrid). The manuscript signifi-cantly benefited from the critical revision of twoanonymous referees. David Nesbitt revised the En-glish text.

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