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Biology and Evolution of the Mollusca

Winston F. Ponder, David R. Lindberg, Juliet M. Ponder

Shell, Body, and Muscles

Publication details https://www.routledgehandbooks.com/doi/10.1201/9781351115667-3 Winston F. Ponder, David R. Lindberg, Juliet M. Ponder Published online on: 01 Nov 2019

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Some caudofoveates in burrow ‘ecological’) anatomical the from differs often orientation Life its (or orientation. adult life assumes animal when the metamorphosis after may axes body entation of occur the reori axes. embryonic A third body original the obscures and flexure indicative gut U-shaped of ano-pedal characteristic the anteriorly. and ventrally opening This produces anal ary - second the displaces shell gland dorsal of formation the the from resulting migration proliferation and cell further taxa, approximately 90 shifted blastopore has posterior originally no the longer and linear, is embryonic A-P axis original stage, trochophore the luscan Wollesen Wanninger & 2002; 2015).et al. by mol Thus, the anteriorly (Biggelaar then blastopore and ventrally places the - which dis surface embryonic dorsal on the migration and is driven by proliferation cell larvae tion trochophore of the - forma the during embryonic of A-P the reorientation axis this (Biggelaar et al. 2002). opening mouth the In molluscs,forms position anterior-ventraltial an to position where it typically its ini from vegetal posterior blastopore is rotated initially (A). the anterior pole the as In protostomes, animal the and (P) embryo vegetalof posterior the the pole the as establishing thus anus, the blastopore deuterostomes, becomes the In 2002). vegetal atthe blastopore pole forms (Biggelaar et al. the gastrulation, polarity, during animal-vegetal and an has embryonic blastula the animals symmetrical most bilaterally 8,in ontogeny.ing Chapter in more detail in described As dur which transform orientations body distinct three to up be can there and complicated, are axes Molluscan body 3.1 chapter. taxon appropriate the in group,themto a singlewith confined deal we are they as but features, external important also coleoid are cephalopods, suckers such the found as many in structures, Some external muscles. and on cartilage information general motion, and (offoot operculum and gastropods), mucoid loco secretions, the structures, associated and epidermis the growth, tion and its- forma shell and the of mantle, molluscs, the comprising chapter, we provide overview body an In this external of the 3 BODY SYMMETRY AND AXES Shell, Body, and Muscles to the ventral surface. In shelled In shelled surface. ventral the ° to to 90 ° to depending ° depending - - - - - (Figure 3.1). 90 afull is rotated axis body the squid, into a helical coil. ahelical into asymmetrically but usually coiled, extended is also body sally the dor In gastropods, moreviscera. efficientthe of packing enable to coiled been elongated has ammonites) tube this the dorsally. In it is elongated cephalopods, and shell valves. In scaphopods forspace expansive an enclosing cavity the between mantle bivalves, dorsally, and it laterally allowing is compacted (visceral body, mass)viscera along the is distributed but in ment, asinoysters (seeFigure 3.3andChapter 15). largely resultfrombyssal,asinmussels,orcementattach- surrounds allormostofthebody. Changesinorientation siderable lateralcompression,andthemantlecavity typically Their shellisdivided intotwo valves, accompaniedwithcon- 20). and Chapters 4 lung), cavity (see is lost heterobranchs some this other in and cavitymantle modified have the to a (as opening aposterior side right along body. of the the Some ‘pulmonate’ gastropods movement the which in results cavity posteriorly mantle of the 3.2), including detorsion, (Figure gastropods in occur axes example body changes of in Numerous twisting. additional torsion is afamous during larvae head-foot gastropod in on the viscera of the displacement. The rotation and metry by asym evolution organ molluscan characterised been has life. throughout maintained is body of orientation the dorsal and ventral the animals, 3.1). most of these In monoplacophorans (Figure and rans, a low with chitons, aplacopho in as axis dorsoventral axis, anterior-posterior extended body molluscan alongearly an relationship is favored,annelid of adult orientation the the mollusc- traditional putative the outgroups. sister If and taxon largely on and the depends mollusc early isthe less certain of anterior-posterior axis of adult orientation the the although the ventral axis is rotated about 60 is rotated axis ventral the Nautilus In swimming taxon. on the 1 Not necessarily true if Brachiozoa are the sister taxon. sister the are Brachiozoa if true Not necessarily Early molluscsEarly were probably In chitons, aplacophorans, and monoplacophorans the monoplacophorans the chitons, and aplacophorans, In Bivalves have alsoundergone considerable modification. axes, ecological body changes and in Besides anatomical Nautilus (and fossil such many as cephalopods 1 bilaterally symmetrical, symmetrical, bilaterally ° , while in cuttlefish and cuttlefish in , while and crawling octopods, crawling octopods, and in its life orientation its orientation life ° in 55 - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Mollusca Yonge, of C.M., Physiology Wilbur and K.M. in pp. 1–58, the Mollusca, of Yonge, J.E. and Morton, and structure C.M., Classification 3.2 FIGURE Original. horizontally. lie others orientation, FIGURE 3.1 56 Olivid (Caenogastropod) , Vol. 1, New York, Press, Academic 1964.

Anatomical axes in Mollusca. All animals in life orientation. Some aplacophorans are buried in an inclined or near vertical vertical near or inclined an in buried are Some aplacophorans orientation. life in animals All Mollusca. in axes Anatomical Axis of symmetry in Gastropoda showing body and shell axes relative to life orientation. Redrawn and modified from from modified and Redrawn orientation. relative life axes to shell and showing body Gastropoda in of symmetry Axis Early planispiral gastropod P olyplacophor Gastropoda --- dorso antero (Caenogastropod) dorso-ventralaxis a Heteropod -ventral axisofbody -posterior axisofbody Patellid (Patellogastropod) --- Monoplacophor , includingviscera axisofvolution C ephalopoda Cephalaspidian (Heterobranch) Trochid (Vetigastropod) Scaphopoda a --- life-orientationaxis Biology and Evolution of the Mollusca of the Evolution and Biology Aplacophor gut Doridid (Heterobranch) (Caenogastropod) a Vermetid Bivalvia Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 cophorans, scaphopods, gastropods, and cephalopods have cephalopods and a gastropods, scaphopods, cophorans, Bivalviawere true (see Chapter 13). (520 mya) Cambrian the in ofappeared these not all although Bivalvedmonoplacophorans, gastropods. or early shells also shell plates being of as animals, chiton-like interpreted been have and period this ‘shells’coiled present during also are or simple and curved plates, cap-shaped, Disarticulated mya). (535–530 Cambrian early the from fossil are record spicules,with or hairs. scales, chitons have covered by agirdle eight shell plates surrounded molluscs, exclusively only aplacophorans have spicules, while spicules (see or not isfused debated Chapter 13). still In living shells were from these formed marker.molluscan Whether public. the and collectors, and ists, artists well as natural as disciplines disparate many scientists from of interest awide of range the Molluscan shells have attracted 3.2 FIGURE 3.3 Muscles and Body, Shell, Bivalves have shell valves, two hinged monopla while - putative mollusc shells (Rostroconchia)The earliest the in shell or spicules most obvious is the carbonate A calcium SHELLS AND SPICULES V enerid (Heterodonta) Axes of symmetry in bivalves. in Original. of symmetry Axes Ostreid (Pteriomorphia) INF A UNAL (Heterodonta) Solenid ------anteroposterioraxis dorsoventral axis Pt eriid (Pteriomorphia) - calcite and/or aragonite. A small part (0.01 part A small aragonite. and/or calcite polymorphs ofof the layers comprised of carbonate calcium shell of is comprised the part 2017).(Checa et al. The hard not homologous,if cuticle the to of aplacophorans chitons and is atleast analogous, and ofis composed sclerotised proteins layer, which outercovered organic by athin periostracum, the generally It is animal. of the surface upper of the some all to slugs some heterobranch in (see Chapter 20). present also spicules are dermal Calcareous hairs. into oped (spines, it is devel some taxa scales) in it, and in is embedded ornamentation girdle of the chitons and surface dorsal the ers cov also acuticle in A cuticle ded covering epidermis. the by shell gland. the not secreted are valves they because not true shells are second these culum, (e.g., hipponicids bivalved and sacoglossans). oper the Like shell is formed primary shell the valve accessory after an two groups. latter ofsome members the single shell (univalved), lost in shell is secondarily the and Pe The molluscan shell is a calcareous structure that covers that structure shell is acalcareous The molluscan is covered body the by spicules- embed In aplacophorans, univalved, afew are most secrete gastropods While ct inid (Pteriomorphia)

EPIF AU NAL Mytilid (Pteriomorphia) % –5 % by weight) 57 - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 having a fragile internal shelly skeleton internal for lophophore,having the afragile bivalves from markedly differ in brachiopods Articulate axis. anteroposterior their through most bivalves symmetrical are while dorsoventral axis, their through symmetrical bilaterally having twoin valves morphologically different which are resemble superficially bivalves,from most differ bivalvesbut have skeletons.(Ectoprocta) shells calcareous Brachiopod some bryozoans and tubes polychaetes calcareous secrete bivalve their with Brachiopoda afew the shell, while are like most shells, mollusc- the which lophotrochozoans secrete the Among kingdom. animal the in is common carbonate calcium of composed exoskeletal an secrete to structure The ability c 3.2.1 habits (see or habitats Section 3.2.3). similar shell indicate morphologies do not necessarily similar always is by no means as this case habitat, lifestyle the and is aderived condition. gastropods, and cephalopods Reduction subsequent and loss shell, of notably some the in Ponder 1996). (Lindberg & primitive as regarded be essarily - dently nec asingle derived from subdivided shell so cannot continues. shell edge, shell the layer butfrom deposition innermost of the is withdrawn margin mantle when the edges ceases at the (or shell. Growth the underlies inner that dorsal) mantle thin edge,of but the by mantle deposited by outer surface the the shell layer innermost shell, rest is of not secreted the the the 2014). (Checa et al. may mineralised shell, be and the Unlike layerthe outermost and forms of first is secreted periostracum edgesshell of valves the and abivalve). in The organic agastropod in (at aperture edges of margin the the mantle the at formed by shell material enlarged shell edgesing of are the (Figure 3.4). surfaces inner edges and The grow tions their to glycoproteins. mainly periostracum, the from (Lowenstam & Weiner shellof is organic the 1989) apart and, Original. tropods. FIGURE 3.4 58 While shell morphology can often be correlated with with correlated be often shell morphology can While multiple plates of chitons may have indepen been The addi by incremental produced shells molluscan are All o

m p Accretionary shell trajectories in bivalves in gas and trajectories shell Accretionary a rison

wit h O utgroups - - - - Princeton, NJ, 1993. Princeton, NJ, s 3.2.2 (see 2000) et al. Chapter 13).(Marin purposes other serving place and in were already eralisation pathways chemical for required biomin the if any credibility with explained only be (544 mya). Cambrian early This can the in years, evolved 30 million less than in groups many in complex, askeleton produce to but, surprisingly, ability the matrix. organic lack an but typically shell structures, molluscs, calcitic have like and tubes, aragonitic eous both &Zato (Vinn scars cle attachment Bryozoa),with mus- and shell pores, vesicular structure, wall (also shared calcitic shell microstructures includeters three - layer. fibrous prismatic shell charac shared Other secondary layer inner an and two shell layers, outer cryptocrystalline an have brachiopods chamber. Many articulate crystallisation off the which seals shells have periostracum outer organic an molluscs, calcite. in As and brachiopod up ofis made proteins it Articulata butthe in chitin, of phosphate and calcium posed shell is com the Inarticulata, brachiophore. In the the called G.J., G.J., from Vermeij, modified and Redrawn curve. the to atangent and radius the between angle the aconstant, αis origin. of the right the (origin) θ and centre the to curve onthe point the from distance by r–the mined FIGURE 3.5 a shell, while aspiral factor in results factor.stant A small by acon adjacent between increases coils distance which the in (Figure 3.5) spiral alogarithmic Shell approximate coils most gastropods). in –as (i.e., cal or conispiral anisostrophic i.e., or asymmetri ammonites; symmetrical), it is bilaterally Nautilus in –as plane same the –in planispiral (i.e., or which isostrophic may symmetrical be aspiral in extension an results and curve of the is curved some limpets apex of The symmetrical. be cone which may or may not shell is form asimple grow. they as or markedly The limpet change slightly can juvenile from shape others adult, to same the most while maintain and, aperture expanding an around principles. Shells growth grow by differential mathematical of shape most afew to and shells conform basic The growth The chemical machinery involved machinery is calcification in chemical The A Natural History of Shells of History Natural A h ell

, the angle between a radius and a horizontal line to to line a horizontal and aradius between angle , the A logarithmic spiral is generated by a curve deter by acurve generated is spiral A logarithmic G eo m etry Biology and Evolution of the Mollusca of the Evolution and Biology r θ α , Princeton University Press, University Press, , Princeton ń 2012). calcar Annelid and many many and ------Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, Redrawn and modified from Lindberg, Lindberg, D.R.,from Malacol. Rev., modified and Redrawn FIGURE 3.6 occupied (Raup & Michelsonoccupied (Raup & 1965; 1990). Schindel have morphospaces other whereas never by extinct been taxa, but have by taxa, living not occupied been morphospace’ are 1990) Schindel ‘theoretical have of the shown some parts that possibilities (e.g., theoretical with geometries 1985a; Hickman Figure 3.7. in illustrated shelland actual correlate to Attempts Table 3.2 in is summarised much variation and ofthemes, that (1993). on these Most variations shell result shapes from by Vermeij is neatly summarised much literature early of the 1989; Stone 1996; 1998; Rice Noshita 2014; Urdy 2015) and Michelson 1965; Savazzi 1985; 1987, Illert 1989; Ackerly workersnumerous (e.g., & Raup 1962, 1966, 1967; Raup left (Table 3.1; is on the aperture the if duced Figure 3.6). is (left-handed) pro coil asinistral shell while coiled results, (right-handed) adextral animal of toward right the the inclined but it results, coil if is aplanispiral is not offset, aperture the shell. ascaphopod If factorin aslightlarge as produces curve, The mathematics of shell coiling has been studied by studied been has of shell coiling mathematics The

Shell measurements required for the derivation of the Raup (1962) four parameter model of shell coiling. Also see Table 3.1. see (1962) Raup Also of the of coiling. derivation model for shell the required parameter four measurements Shell Aperture Curvature Apertural Growth rate Shell Shape and Coiling and Parameters Shape Shell 3.2 TABLE Z-axis (spire) moving on expansion NA NA Narrow cone Low d1 Simple Cone

radius aper position ofgenerating

NA NA Broad cone High ture ture curv

aper 2 e (d2) ture translation

18, 1985b. 1–8, 1 NA Loose coiling Loose coiling Low -

Note: Source: Whorl translation(T) Position ofgeneratingcurve (D) Whorl expansion rate(W) Apertural shape(S) Parameter Coiling Based on the Measurements in Figure 3.6 Measurements the on Coiling Based Calculation of Raup’s (1962) of Shell Parameters Four 3.1 TABLE Planispiral ating curve, y = translation,andr radius. a Lindberg, D.R.,Malacol.Rev., 18,1–8,1985b. = apertural dimension,w NA Tight coiling Tight coiling High w5 w4 Low spire Loose coiling Loose coiling Low w3 = whorl expansion, d w2 Conispiral Measurements from Figure 3.6 High spire Tight coiling Tight coiling High d a r d a y w w whorl 1 2 1 2 1 2 +… w w 1 21 3 = position ofgener n − 1 + wn wn − 59 - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3

modified from Rice, S.H., Paleobiology from modified and figures). two (as right-hand result Redrawn the in vex will spire age, con with a rate growth in decrease is a there if figure), while left-hand (as age, the aconcave results with in spire increases rate growth the If the left. figure on second the in as results, spire conical a simple occurs growth exponential When of growth. rates different FIGURE 3.8 expansion and rate –some parts growth the between ship arelation also simple. from far There is relationships are astraight-sided produces cone. these exponential rate Thus, aconvex produces rate growth an cone,A constant while is concave. age, spire the increasing with accelerates growth if profile, down adome-shaped while has later, spire the ple, is relatively when growth life, but early rapid slows in shell. For exam gastropod of shape a conical the alter can Figure 3.8 factors shows of growth different how timing the life. changes throughout growth as occur shell also shape (whorls not touching) or even shell. in Changes uncoiled an the coiling at open with, extreme, shell aflatter forms ing looser coil while shapes, conical tall, and lapping sutures over in results Tighter coiling. shell coiling and shape in 1966. 1178–1190, Raup, from D.M., J. Paleontol. modified and Redrawn axis. the to curve generating the from curve), distance of agenerating and (the height translation aperture), of the shape the to equivalent is curve –whorl generating expansion (the of the shape parameters 3.7 FIGURE 60 Increasing expansion rate expansion Increasing Small changes in growth parameters result in changes result in parameters growth changes in Small

Variation in spire outline in a gastropod results from from results agastropod in outline spire Variation in Shell models generated with different growth growth different with generated models Shell , 24, 133–149,, 24, 1998.

Increasing translation Increasing distance from axis , 40, , 40, - - - - - is dextral. it it right, if is on the and shell is sinistral, the left, is on the observer facing the opening aperture the and uppermost spire shell is viewed a longer the with aconispiral spire. When hence and coiling shells, tighter enabling conispiral with mals shells, it torsion advantages ani to is more likely that afforded have or planispiral some gastropods Although limpet-shaped 3.2.2.1 being thebestknown example (Landmanet al.2017). to have re-evolved tightlycoiledshells,Scaphitidaeperhaps coiling. Someheteromorphammonitesarealsohypothesised (1994) foundthatthereinvented coilingdiffered fromnormal anothercaseinvolving avermetid, GouldandRobinson In 2002), andthesehypotheses remainuntestedwithnew data. Trochita atvariance. withsomeotherresults(Simone This is (Crepidula) whenalineagegave risetothecoiledgenus ing was apparentlyreinvented inuncoiledslipperlimpets provided anexample in Calyptraeidae showing thatcoil- toacoiledsnail.CollinandCipriani(2003) could not revert cannot be‘reinvented’ soanuncoiledlimpet,forexample, exclusively are no families coiled. open (Rex &11 families Boss of 1976), gastropods living although atleast across taxa certain in occur contact not in or partially (Cerithioidea). Very whorls shells the coiled with open wholly cochliopids), Vermetidae (Vermetoidea), Siliquariidae and such Truncatelloideagroups, as (e.g., some and Caecidae severalexpansion. in unrelated shells occur uncoiled Also, aperture ‘anterior’ exceeding lateral usually and rior’ dilation ‘poste with reverse the is true limpets but patellogastropod in expansion, few aperture equals) species ‘posterior’ lateral and ‘anterior’ (i.e., post-torsional anterior) exceeds (or dilation a in limpets most gastropod evolvedoften In lineages. many in shell have shape conical For example, and tropods. limpet the (Vermeij more inflated 1990). slows older, age so that are increasing with individuals larger away fastest. growing apex usually the from shellof edge grow the relatively faster, further points with dextral coiling werecommoninearly gastropods, dextral taxa record shows that although both sinistral and gists. The fossil gastropods exhibit dextral- coilinghaslongpuzzled malacolo common inthePaleozoic. Why thevast majorityofmodern marine gastropods (Vermeij 1975),althoughitwas sometimes uppermost. spire the with when orientated sinistral shell is apparently the while dextral, remains animal the cally anatomi although shell, sinistral it be to dextral would appear way same a the as shell is orientated ahyperstrophic if Thus, (the of coiling Z-axis) (Figure 3.10). axis vertical tion along the 2009). development early ing (Figure 3.9) et al. 2005; Kuroda (Levin of(e.g., cleavage direction the dur which determine nodal) Shell coiling direction ( direction Shell coiling generallythoughtthat,oncecompletelylost,coiling It is Various shell have shapes evolved- gas multiple in times bivalves, many growth as valves the inflated become In Planispiral coilingisrather rare,particularlyinliving - opposite direc the shell in coils the In hyperstrophic snails, The Direction of the Coil of (Handedness) the The Direction Biology and Evolution of the Mollusca of the Evolution and Biology chirality ) is determined by proteins by proteins ) is determined - - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, taxa, and itisdifficultto seewhy asinistral animalinasinistral tral animals,torsion occursinthereverse directiontodextral effects of torsion on the body, but in sinistral taxa with sinis- 2005). Various authorshave relatedthisdextral biastothe Davison being dextral (Schilthuizen & ing coiled gastropods later becamebyfar thedominantformwithover 90 % Vic. Mus. Linsley, from Nat. R.M., Mem. modified FIGURE 3.10 Nature FIGURE 3.9 , 457, 1007–1011, 2009.

Chirality in snails is determined by the early cleavage pattern. Redrawn and modified from Grande, C. and Patel, and Patel, N.H.,C. Grande, from modified and Redrawn cleavage early by the pattern. determined is snails in Chirality Shell and body coiling. Diagram illustrating orthostrophy, hyperstrophy, and hypostrophy. Middle vertical row redrawn and and row redrawn hypostrophy. hyperstrophy, vertical orthostrophy, and Middle illustrating Diagram coiling. body and Shell (sinistral body homostrophy orthostrophy hyperstrophy (dextral shell dextral shell) and body) Sinistral Dextral Dextral , 39, 33–54, 1978c. Sinistral ofliv- pod genuspod fresh-water the caenogastro in and gastropods heterobranch ciency wherethechiralityofanimalandshelldiffered. dextral shell. It is, however, easier to imagine reduction in effi - shell would beinherentlylessefficientthanadextrala onein Hyperstrophy occurs in the larval stages of most marine stages of most marine larval the in occurs Hyperstrophy Dextra l Lanistes (Ampullariidae). Heterostrophy occurs occurs Heterostrophy (Ampullariidae). homostrophy (sinistral shell hyperstrophy sinistral shell) (dextral body orthostrophy and body) Sinistral Dextral Sinistral 61 - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 2 namely,lies, Triphoridae, coiled but theshellsofmembersafew gastropod fami- (Figure 3.11). gastropods some heterobranch is obvious versus protoconchs teleoconchs of the the in as growth, during direction coiling is achangewhen in there 1993a. 12–18, Notes R., York New Club Shell from Robertson, modified and FIGURE 3.11 62 normally seen on one valve appear on the other. on one valve on seen the appear normally 1996) features hinge so the (Matsukuma is transposed hinge bivalves where symmetrical the uncommonly, bilaterally in 1919) (Odhner bivalves Chamidae like asymmetrical or, (Checa & Jiménez-Jiménez 1997). toward weighted the side pattern coiling the achange in in vertically, of near resulted instead angle shells atan lie to the planorbid shells were weightednispiral on one side, causing pla- which near in Experiments gastropods. in patterns ing 2007, et al. (Schilthuizen populations 2014). interbreeding in numbers approximately equal in occur often Amphidromis snail land exceptions for occur, as example, stylommatophoran the in Davison 2005), (e.g., although direction ing Schilthuizen & coil achange in selection against act Thus, would normally side wrong on the body. of the are genitalia their because of opposite chirality between partners difficult becomes ing mat gastropods, fertilising internally Davison 2005). In ciation (e.g., Gittenberger 1988; 1993; Asami Schilthuizen & spe promotes occasionally and responsiblebe for chirality a single someshown stylommatophorans gene in may that have snails on land Studies taxa. non-marine in particularly class, the in repeatedly occurred has chirality change in that shells, usuallyhave adextral animal. sinistral sports,oroccasionaltaxathatnormallyhave sinistral Davison 2005).Such pods, but arerare(e.g.,Schilthuizen & Freak coilingreversals (tosinistral)occurinmany gastro- taxa,theanimalwithinshellisalsosinistral. In sinistral tral (Vermeij 1975; Gould 1985; Robertson 1993a, 1993b). other families scatteredthroughthegastropods arealsosinis- somespeciesorgenerain are sinistrallycoiled.In addition, some generaandspeciesofstylommatophoranlandsnails as mostatlantidheteropodsandthecosomepteropods, There are a few dextral triphorids. afew dextral There are As noted above, most modern gastropods are dextrally Reversal of bivalve of polarity some valves in seen be can coil affecting only influence not the factors are Genetic indicates gastropods in of sinistrality distribution The

Examples of heterostrophic protoconchs. Redrawn Redrawn protoconchs. of heterostrophic Examples where both left and right coiled snails snails coiled right left and where both 2 Planorbidae,Physidae, as well , 329, - - - - the uncoiled heteromorph ammonites (see Chapter 17). ammonites heteromorph uncoiled the of Mesozoic appearance the in the with noids occurred also ammo in 2017).et al. parameters coiling changes in Further 3 views. Orginal eral FIGURE 3.12 to rocks,burrowing snailswithstreamlinedshells,etc.),often apertures clingingtowave-swept platforms,oysters cemented justify this general observation (e.g., gastropods with large with habitsandhabitat. While many suchexamples seemto ofashellisoftenthought tobecorrelated The morphology s 3.2.3 arcid arcid example known best the being the axis, anteroposterior the Cyrtodaria hiatellid the bivalves extinct Bakevelliidae, the and (Arcidae, Mytilidae, torsion afew in So-called species. on the depending is used, however, rudists, and valve. chamids the either Within valve completely to always left flattened by partially cemented the evolving oysters while Pectinoidea, are multiple within times valve by right the despite attached cementation are inoideans pect cementing example, asymmetrical cementation. For with another. associated More extremeoften examples are or one inflation valve in differences overlapping small ing examples includ- extreme, to minimal with may minimal be afamily. within Asymmetry constant class, be butthe can across divided is roughly equally and commonly rather occurs biont may sclero have from resulting pathological variations been (Vermeij number in 1975). Some coiling changes of in these about equal taxa dextral and shells sinistral coiled with ral (nautiloidsshelled cephalopods ammonoids) and conispi had (Figure 3.12). Organisms living on hard substrates such as shells. as such substrates hard on living Organisms Asymmetry of bivalveAsymmetry shell valves right left and between In the Silurian and Devonian, five and lineages of or Silurian six the In 3 infestation during the life of the ammonites (Stilkerich ammonites of life the the during infestation Trisidos h ell

(McGhee 1978; (McGhee 1983b; Morton Savazzi 1984) S The ‘twisted arc,’ Trisidos The ‘twisted ha pe

Biology and Evolution of the Mollusca of the Evolution and Biology a ) involves valves of the twisting around nd H ab it

tortuosa , dorsal and lat and , dorsal - - - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 does not slope (orthocline), the shell lies horizontally on the (orthocline), on the not slope does shell horizontally lies the where it those obliquely. shell apex the inclined with In crawls snail the aperture, prosocline asteeplywith inclined negative ( angle Shell, Body, and Muscles and Body, Shell, Paleobiology Linsley, from by (1977). Linsley R.M., modified and Redrawn 3.13 FIGURE ( of coiling axis the to angle moderate to a steep side, from range the can below discussed (see Section 3.2.4). further are types apertural These aperture. which is impossible aradial with substratum, the clamp to can aperture atangential with tropod A gas- most most cephalopods. bellerophontids, coiled in and including older in fossil taxa, common but gastropod are they omalogyrids, tiny the in and architectonicids, Angariidae), in vetigastropods (e.g., and such Liotiidae some as trochoideans found being some living in gastropods, living in uncommon (Figure 3.13). plane same whorl the are in lie apertures Radial last of the ventral-most the part and aperture so the gastropod last whorl the to is tangent of the of a‘tangential’ aperture plane the of while coiling, axis the through its passes plane is ‘radial’ if 1977). (Linsley or tangential aperture radial An it –whether is aperture of the nature the to related is also example. Clausilliidae whichlive onrocksortreetrunksbeingonesuch tall-spired shellshave very different lifestyles,theterrestrial to thismodeoflife(e.g.,theglobular Naticidae). Also, some different shellmorphologyappeartobeequallywelladapted sand burrowers suchas Terebridae, but othergroupswithvery gate tall-spiredgastropod shellsareoftenfoundinshallow eral lineagesofcarnivorous caenogastropods. Similarly, elon- bivalves and the whelk-like shells that have appeared in sev- cockle-shaped shellsofseveral groupsofshallow-burrowing other examples ofconvergent shellmorphology, including are many &Lindberg 1997). There simplification (Ponder or wave actionselectforlimpet-shapedshellsareanover- very different habitatsandsuggestionsthatstrongcurrents starfish. Thus,limpet-shaped shells functionwellinmany Other limpet-like gastropods areparasitesonbivalves or genic substrata,athotvents, andinquietlakes andponds. and infast-flowing rivers, but alsoon various deep-seabio- in avariety ofhabitatsincludingwave-swept rockplatforms thus frustrating attempts to correlate them. Limpets are found lar shellmorphologiesfrequentlyoccurindifferent habitats, shell morphologyisnot readily correlated.For example, simi- The lip of a gastropod shell aperture, when viewed from shell aperture, of agastropod The lip relation substratum in the to of gastropods The orientation prosocline , 3, 196–206, 1977., 3, 196–206, R

adial aper The two main types of aperture recognised recognised of aperture types two main The opisthocline ), to parallel to it to ), ( parallel to tur plane ofaper e ). In conispiral gastropod shells gastropod conispiral ). In tur e orthocline Ta ngential aper ), or ata ture oval (e.g., openings Vermeij 1993). have usually simple to rounded apertures inclined with those have often group while elongate siphonate and/or apertures, is crawling. This latter animal when the surface substratum also argued that the lower the that foot shell of the angle to has the argued also (Vermeij 1971). aperture atangential maintaining Some have shell –by alowa ‘balanced’ adopting of and gravity centre employSnails achieve to acombination two of processes these ways (Figure 3.14): head-foot,of achieved such the be two ‘balance’ main in can over midline shell of of balanced the mass the centre the with foot Linsley on shell the as is ‘balanced’ (1977)the theorised, efficiency habitat. If habits with related achieved and is when is cor body on the how shell is carried gastropods, the In These ‘laws’These (from are Linsley 1977): spire. the to other the last aperture, twotwo relate and the to followed gastropods several ‘laws’. marine coiled first The that proposed and substratum and relation animal in the to Linsley (1977) investigated gastropods in shell orientation g 3.2.4 4 See Section 3.2.3 and Figure 3.13. and Section 3.2.3 See • • Law 1: The Law of Radial Apertures Radial of 1:Law The Law Law 5: The Law of Apertural Elongation Apertural of 5: The Law Law of AperturalLaw 4: Re-entrantsThe Law : Angulations 3: Balance Shell of The Law Law Tangential of Apertures 2: The Law Law called ‘regulatory detorsion’ ‘regulatory called by Linsley (1978b). foot of the –aprocess axis longitudinal the with parallel is approximately axis coiling shell so the the Swinging axis coiling Lowering the foot. of the axis posterior anterior- the to is subparallel axis this aperture; the posterior, to of long along the anterior axis ity from developand cavmantle the awater flowthrough only possess a single gill having elongated apertures anteriorly. or exhalant areas;inhalant areaswillbedirected or re-entrants on the aperture indicate inhalant mass. cephalopedal of the over midline the its shellof contents of is and mass the centre so the above body, is the supported pod positioned be it will substratum. the to parallel live aperture of plane the the with one volutionof more than apertures tangential with substratum. the to it Most is perpendicular typically substratum. the to parallel not live aperture of plane the the with do one volution apertures more than radial with a stropod S h ell O rient : If the shell of the agastro : If a tion 4

: Gastropods of : Gastropods in L : Gastropods : Gastropods : Gastropods : Gastropods ife - - 63 - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 gastropods. Inhalant canals are found in some cerithioideans, found some cerithioideans, in are canals Inhalant gastropods. shells. upprop their Xenophoridae, some which Strombidaeas to and spines use of A few coiling. axis employ groups such strategies, different the to is parallel plane apertural well the as do not conform also terebrids and such cerithioideans many forms as spired onHigh- one Conidae. side in markedly as placed aperture exceptions that Lawnoted 3included his to shells the with more rapid movement 1978a, (Linsley 1978b). Linsley (1977) andconsequently reduction benefitenables drag added of the 1985b.China, 1983 April Kong, 6–24 Hong China, Southern of and Kong Hong of Malacofauna Hong Kong, from pp. 217–234, gastropods feeding D., B. Dudgeon, in Morton & suspension- free-living ecology andof morphology C.S., Comparative Hickman, including sources from various modified and Redrawn in morphology. phylogenetic but showtrends series, not a figure are this in row, The examples Terebridae, Olividae. bottom Patellidae, Conidae, row, Cerithiidae, third Neritidae, Buccinidae, row, second Trochidae, Littorinidae, Helicidae, Pleurotomariidae, Ampullariidae, FIGURE 3.14 64 The fourth and fifth laws relate to the aperture of caeno lawsthe aperture relate fifth to and The fourth

Some examples of changes in gastropod shell orientation relative to the head-foot. Taxa from left to right are:- right Taxa row: to top left head-foot. relative from the to orientation shell gastropod in ofSome examples changes horizontal shellaxis ve rt ical shellaxis shell coilingaxis shell axisloweredrelativeto shell axisstraightensrelativeto - gravity of the shell of overgravity the foot. of the middle the sion last whorl of the which effectively of centre places the where it considerable with is combined Cypraeidae, expan and Ovulidae some all such Strombidae, in many and seen as although caenogastropods, other in but uncommon pods, elongation neogastro in Haliotidae). is common Apertural Scissurelloidea, (Pleurotomariidae, two with ctenidia tropods some shell slits vetigas or in holes- occur Bursidae. Exhalant developed and conoideans, some many triphoroideans, in well- especially being less common, are canals exhalant Distinct neogastropods. and tonnoideans, triphoroideans, fo Proceedings of the Second International Workshop on the the on Workshop International Second the of Proceedings ot , Vol. 1 Hong Hong Kong Kong, 2, University and Press, fo ot Biology and Evolution of the Mollusca of the Evolution and Biology shell axisraisedrelativeto shell spirelengthened fo ot - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, 5 shell plate anlage which arod-shaped in chamber a crystallisation creates and environment external the from ( villus flat enormous plate fieldshave develop that cells an shell plates.the The ridges (the depressions the the between plate fields) secrete cuticle, secrete up of while ridges that made cells transverse (seeaccepted below). is rarely shells were this although independentlyderived, Scheltema prompting groups (1988a) suggest to their that conchiferan so-called of those the with compared formed Chapter 13. given shells are (protoconchs) in time larval through tropod evolution of the chapters.Aspects taxon the in and of- gas shells is given Chapter 8 in larval and on larvae information feeding. More detailed planktonic during growing latter the shell, initial the as formed former the II), I and prodissoconch shells (protoconch or larval the in distinguished be stages can growth larval (planktotrophic), two separate plankton the in bivalve istics. and feed that For example, gastropod in larvae character history life easily accessible determine to marker provide adult bivalves can in an and gastropods and retained is caecum-like. patellogastropods, shell or, is coiled in larval the gastropods, In ammonites. ‘ammonitella’ extinct of larval the planispiral unusual very exception interesting is the another itscaphopods is tubular; in although it is cap-shaped, taxa of these oconch. In most tele on the symmetrically shell rests larval the cephalopods valves. the ing In monoplacophorans, shelled and scaphopods, shell on one valve aflexible lacking hinge onlyconnect and bivalves from differ Rostroconchia group having alarval in bivalved plane. The fossil anteroposterior the in than rather lateral the in aligned prodissoconchs cap-shaped have paired bivalves.soconchs in bivalves shell and lack alarval Chitons - prodis and gastropods in shells) protoconchs onic called are Chapter 8 for shells (sometimes embry details). called Larval (see shell gland the from initially shell is produced The larval l 3.2.5 external influences. The shell gland of gastropods is simple, gland of gastropods The shell influences. external (the chamber lisation extrapallial chamber encloses and edge shell of gland acrystal the distal at the is secreted The periostracum shell is secreted. larval when the which subsequently evaginates ectoderm thickened inated, development in early formed shell gland, the invag from ture, 1980). (Kniprath properiostracum the coveredthen the field, is andplate outer layer, the organic by region plate of the central subsequently the by in cells added layer layer hypostracum tum ventral is plate, of the while the tegmen the producing rod, edges of the atthe initiated is then growth (Figure 3.15). accretionary rod, of formation the After structure. a particular develops into that embryo of the part or primordium, A The chiton larva developsthenseven larva and six dorsal first The chiton in how are differences chiton shells significant There are protoconch is lost but adult scaphopods, is in often The - have struc usually shell-secreting the larvae Conchiferan a rv a l S h ells stragulum

a nd T h ) which seals each plate each field) which seals eir F or ma tion ) closed off from 5 forms forms ------stronger than non-crystalline aragonite (Jackson aragonite 1988). et al. non-crystalline stronger than times is over of form aragonite, 1000 acrystalline nacre, example, an As strong structure. amechanically produce combinationin that crystals carbonate of calcium figurations con different complex and combination of material organic is a soft body. the supporting The shell and protecting thus cavity (see mantle the covers and cally Chapter 4), viscera the (see by mantle the Section 3.9) is secreted The shell typi and s 3.2.6 molluscs. Their conclusions are summarised below. conclusionsmolluscs. summarised Their are involved of groups spicule shell different and in in formation form. crystals the that matrix this of it macromolecules, and is using in space awide variety lial (see extrapal Section 3.2.6.2) the within which is elaborated is much It involves more complex that. than matrix organic an have but studies recent process shown the periostracum, that the edge and mantle the between space extrapallial the in solution asupersaturated from shell crystallised uping the sition shell of (see the below). depo the pellicle whichorganic (properiostracum) facilitates groove’ athin a‘properiostracal produces plates formed that shell the to proximal cells epithelial chitons, specialised in They suggested is similar. that, conchiferans chitons and both 1979) et al. workers concluded shell (Haas in formation that hinge line. but bivalves in a groove which is develops formed the into Monoplacophora mak For some crystals that it was time, assumed generally Conchifera Aplacophora Polyplacophora reviewedScheltema (2006) Schander strategies and the Although they noted these differences, Haas (1981) Haas differences, these noted they Although co- and to one relationship between prisms and mantle cells. mantle and oneto relationship prisms between shell aone edges with atthe periostracum the under deposition. internal and accretion edge. is by Shellmantle marginal growth agroove in on the periostracum as cle is secreted (Ivanov 1996). covering of cuticle athin has each and Okusu 2002) 1981; invagination of the asinglein (Haas cell extracellularly secreted are they aragonite, are ules spic chitons, the - in As by epidermis. the secreted shellof plates. the surfaces ventral on the and margins deposited atthe are shell crystals and margin, a groove mantle atthe in cells by epidermal secreted properiostracum thin Scheltema 1993). valves covered are by a The shell spiculeof the is covered 1981;cuticle with (Haas region packet)cell proximal the and (Figure 3.15), single (the cell formative cell) of or (the agroup cells invagination of an either a in Spicules produced are embedded. eight shell plates are the dorsal and dle spicules aragonitic gir of the the shell plates and the h ell : Do not have spicules, and the mantle cuti not have mantle : Do spicules, the and F : Also have: Also acuticle covered mantle or : The mantle secretes acuticle which secretes in : The mantle ma : Calcium carbonate is deposited carbonate : Calcium tion / S ecretion - - 65 - - - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Roux. Arch. Dev. Biol. Dev. Arch. Roux. E., Kniprath, Haas, from W., Malacologiamodified FIGURE 3.15 66 Nautilus mantle edge epithelial cells, fuse together, fuse cells, then edge epithelial and mantle on groove. SEM study made on an Based periostracal the to just cells dorsal mantle individual within form that found. cavity been has No extrapallial 2009b). 1959; Wingstrand et al. Checa (Lemche & layer prismatic the under cells by mantle the secreted layer inside, a nacreous (foliatedFurther aragonite) is spine rudimen vesicles lled with organic secreting cell basal CaC secreting cell basal CaC Nautilus material epithelial microvilli microvilli : The shell is composed of aragonite structures structures of is composed aragonite : The shell microvilli cell nucleus

Dev on thegirdleof Spicule and shell formation in polyplacophorans. The left-hand figures show the development the and of a spicule. Redrawn figures show The left-hand polyplacophorans. in formation shell Spicule and s organic pellicle O elopment ofalargespicule(spine) O embryos, the crystals grow out of the crystals embryos, the Initial stageofspine (modi ed fromHaas1981) t of spine Growing spine L epidochitona cinerea , 189, 97–106, 1980. , 21, 403–418, 1981, and the right-hand figures show the formation of shell plates. Modified from Modified of plates. shell , 21, the formation 403–418, 1981, figures show right-hand the and fo par calcareous rmation t ofspine Three stagesinshellplatefo microvilli 6 Transmission Electron Microscope. Electron Transmission cuticle that the prisms were initially formed in intracellular intracellular in formed were initially prisms the that juvenile adolescent early showed and individuals from (2005) on al. material ies by et Westermann matic and nacreous layers, nacreous and respectively.matic TEM - pris into incorporated which once assembled are proto-platelets, and occur, proto-prisms of crystals (Arnold 1992). periostracum the to fuse Two forms shell plate rudimen plate eld (modi ed fromKniprath1980) t Af stragulum Af Af ter 20hours ter hatching ter 9hours Biology and Evolution of the Mollusca of the Evolution and Biology rmation inIschnochitonrissoa intersegmental ridg cuticle vesicles mucoi d condensed laye mucoi laye shell plate r d e 6 r stud - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, or slows, the outer periostracum continues to be secreted so secreted or slows, be to continues outer periostracum the fold ceases by outer mantle shell the growth epithelium. When bivalves, layer groove other in cal as inner the is secreted and sists of two- layers. periostra the layer The outer in is secreted of fresh-water mussels periostracum thick (Unionidae) con 2003). et al. (see Scardino ( some bivalves in musselsand, such atleast, some marine as shell erosion, notably fresh-water in bivalves gastropods and is absent. periostracum the ries, cow extending over in mantle as outerthe shell surface, the by is secreted shell where surface a polished off. In species flake and brittle shell, become itempty out on can an dried may flexible be life,in once periostracum has it the While some of species in Conus as is hidden, so any colour pattern a heavy, shell beneath it the obscures opaque periostracum with species 2005). In al. et (Pfenninger them possess that lution presumably provide and adaptive advantages taxa to mollusc in evo have arisen often hairs Periostracal pattern. in species-specific may complex often be that are and hairs away. eroded often or Some have sculpture species regular obvious, and smooth barelyand visible, be or it can thin, very it. in ded - embed it carbonate afew calcium but, has in protein, taxa, Luquet entirely of 2004). composed It is usually (Marin & involving process insoluble quinone becomes atanning via quickly solublewhich then polymer periostracin protein of form the the edge in mantle groove the in periostracal framework (see next Section). as a matrix an organic using occurs, the shellcalcification of space that in and environment, external the from space pallial edgesshell of which- extra isolates atthe the aseal forms periostracum The proteins. quinone-tanned cross-linked of is composed brown. It side shell of (the the ‘ostracum’) yellow is usually that dark to cuticle-like organic layer is an out on the The periostracum 3.2.6.1 component. carbonate calcium of the microstructure and formation the describe then components shell of and the following the the organic with firstly we sections, deal In Mytilus The periostracum usually consists of usually asingle layer,The periostracum but the assist slowing in can or preventing periostracum The and thick or rough and may smooth be The periostracum the in is secreted of conchiferans periostracum The Other Conchifera larly in an organic matrix. organic an larly in (seecum Section 3.2.6.1). extracellu form Crystals - fold epithelium periostra mantle ofthe the the and between space a fluid-filled in formed extrapallial formation. on shell literature mainstream largely the in ignored been has This finding adults.in confirmed not been of knowledge, shell method our has formation this form. final assembled their into extracellularly To be to vacuoles surface cell moved the and through Periostracum ), shown it biofouling been assist reducing to has in : In most conchiferans, the shell is the most conchiferans, : In consisting of highly conchiolin - - - - - . of CaCO of type the 2013).et al. role determining in a crucial They play by (Marie several of orders magnitude shell fractures to is suspended. outer layer crystals of carbonate calcium where the from periostracum of the surface includes inner the matrix 2012). 2010; et al. This organic Jackson Marin et al. Luquet 2005; (e.g., form tion, and 2003; Marin & Wilt et al. posi growth, their determines and nucleation crystals of the 2012), et al. of apoint (Marin form it as and acts crystals the which from involved minerals synthesis of amorphous the in is it as grows. This matrix crystal the included within are teins calcium carbonate calcium aframework on which as acts formation. This organic material shell, of involved it the processes controls many part shell in 5 (less than aminor comprising matrix organic Despite the 3.2.6.2 figure 4a). 1997b, layer (Harper amytilid in periostracal middle olated except unionids, including vacu for other asomewhat similar bivalves, other in reported not been has This situation 2000). (Checa layer middle the periostracum of the within occurs groove nucleation and by layers periostracal cum the secreted - periostra middle bivalve outer and has unionid the Amblema is present (see Section 3.2.6). layer organic acuticular although cum (the properiostracum) - periostra true fewChitons lack a it is calcified. gastropods, in someand bivalves, etc. ridges,with andhairs, a modified, of composed layers. is also It canperiostracum structurally be cold in living water, species thick the marine In some 2000). (Checa secreted shell are and periostracum both tion occurs, active shell. of When the shell interior secre the to added occasionally are layersinactive periostracum periods, of inner long (Checa During 2000). conspicuous lines become growth it folds forms groove, it as these leaves and periostracal the matrix inhibit crystallisation until they attach to asuitable to attach they until crystallisation inhibit matrix et al. et al. 1996; 2012). Marin The soluble shell the in proteins ently involved (e.g., control of the crystallisation in Belcher 2012). soluble Some insoluble, are others ­ and the et al. (Marin signalling cell in others and enzymes as function shell some formation, expressed during proteins many the Of 2005). Luquet (e.g., 2004, shell matrix organic the Marin & up glycoproteins, make proteoglycans that and saccharides, poly other and epithelium include chitin mantle proteins, the –notably nacre. structures is only reasonably simpleproteins in well shell understood of shell organisation matrix The complex form. and growth 7 1981; Cherns 2004) (see1981; Chapter 13). 2004) Cherns Cobcrephora Silurian the mollusc, putative of a phosphatic record ­questionable for except one carbonate of calcium composed are shells mollusc All The shell matrix proteins increase the resistance of the of the resistance the increase proteins shell matrix The In a departure from the situation in most conchiferans, most situation conchiferans, in the from adeparture In Organic compounds secreted into the extrapallial space by space extrapallial the into secreted compounds Organic

3 polymorph, as well as crystal nucleation and their nucleation their well as and crystal polymorph, as Compounds in Shell Formation in Shell Compounds Organic The Role of Other that was suggested to be a relative of chitons (e.g., of chitons a relative be to Bischoff suggested was that 7 is deposited, and some acidic pro of and is deposited, the latter appar latter % 67 - - - - ) - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 involved in cell signalling (Marin et al. 2012). et al. involved In (Marin signalling cell in may be others and enzymes as act cells. Some proteins lial epithe with interactions and interactions protein-protein minerals, trol. They include and proteins between interactions involved much con more complex are hormonal under and processes but nucleation the inhibition, growth tal and - crys just two mechanisms, was through be thought to tals (Dauphin 1996). in thenon-mineralisedgladiusofcoleoidsquidisbasic contrast,theorganic matrix matrix needstobeacidic.In Luquet 2004). (Marin & formation crystal in points nucleation where as act they matrix ofinsoluble the part 68 matrix is secreted by mantle cells. by mantle is secreted matrix organic extracellular The matrices. organic intracrystalline some the form and crystals, of the growth tion, and formation, involved also - are regula and the in cium carbonate-binding insoluble the havelike proteins, region ahydrophilic for cal (e.g., proteins matrix MSP-1, nacrein, or Asp-rich), which, soluble also There are crystals. of orientation the ation and nucle the probably and regulate framework, organic also line (calcium crystals),inorganic intercrystal the form carbonate (scaffolds) organic the between provide connection the and proteins these Thus, carbonate-binding. calcium enabling chitin) ahydrophilic-acidic region and and protein between lin-14, which have ahydrophobic region (enabling interaction MSI60, such- Pif, as proteins or prisma insoluble matrix Nagasawa and (2013),Suzuki scaffold contains chitin the by model proposed on ascaffold of insoluble In the chitin. precipitates carbonate Calcium matrix. organic an in formed 2009a). et al. layers or calcitic prismatic aragonitic (Furuhashi similar the superficially knownin with none in nacre, identified been only has fibroin silk protein gel The shells.molluscan first the in mayancient processes give and clues mineralisation to lone (Jackson et al. 2010). probably are common The genes in oyster aba- the pearl and the between only one was shared Lottia patellogastropod the in those to weresix similar 2013). genesabalone, only in biomineralisation these Within evolve 2010; rapidly (Jackson rather McDougall et al. et al. may they suggesting species, between that differ domains, genes, which silk/fibroin-like with express proteins shematrin species. For example, in the pearl oysters For example,species. ( pearl the in evenferences some shell in proteins, closely between related dif also There are 2007). stages experience (Jackson et al. these environments different the to response presumably in juveniles, adults, and larvae, the expressed in differentially genestion, responsible the for are expressing proteins the 2013). et al. (Miyamoto gastropods with In addi shared are of which only three proteins, of shell matrix at least 30 kinds oyster fucata pearl Pinctada molluscs.other In the 2013), in et al. is probably (Marie this similar and inhibitors protease and proteins, acidic calcium-binding chitinases, and anhydrases carbonic such peroxidases, as including enzymes proteins, unique and conserved highly both example, are there Until recently the control of the formation of- control formation of shellUntil the the crys recently Interestingly, for shell crystalstoform,the organic As described above, the shell microstructural elements are above, shell microstructural described As the Pinctada Lottia , there are are , there spp.), the , and , and , for ------These are: are: These 2006). al. of constituents bivalveorganic (Addadi nacre et crystal. included the in proteins some acidic of utilising the growth ofcommencement crystal followed the and byThis is nucleation matrix organic on the gel. silk replacesthe carbonate colloidal calcium amorphous an and by framework, the determined are crystal ofshape the The orientation and formed. be will crystal nacre which the in ‘hydrophobic organic an with gel silk’ so it space occupies the framework is which filled achitinous in matrix organic the involves step first (2006), the et al. Addadi to assemblythe of bivalves. pteriomorphian According cally, in formed nacre the and pumped (as pumped space.and ions) extrapallial the into required as mobilised granules, as tissues in cium is stored by work the of ion accumulated epithelial The cal pumps. are ions and (mainly calcium) by periostracum, the medium nal the from exter sealed is the chamber in fluid The extrapallial chamber. extrapallial the shell surface, the and periostracum the between a fluid-filled space form in crystals carbonate edge shell of when atthe the calcium occurs Shell growth 3.2.6.3 The most studied shell structure is nacre and, more specifi and, is nacre The most shell structure studied Chitin the have ofin groups proteins identified been main Three Mucin-like proteins Mucin-like proteins Silk-like proteins Acidic cation (Marin et al. 2000). et al. cation (Marin haveevidence mucins that aprobable role calcifi in shell layer nacreous nobilis the of Pinna of Haliotis nacre the from and absentis to nacre similar superficially are that et al. 2009b) layers or calcitic prismatic (Furuhashi aragoniticfrom identified not been gel has protein fibroin Silk before crystallisation. separated sheets probably helps organic The gel forms. the keep to water is removed that and mineral formation, the as was ahydrogel silk the that sumed before mineral 2012). pre (2006) et al. et al. (Takahashi Addadi such Atrina as bivalves of pteriomorphian nacre found the in (especially spider) have and silk been arthropod (Gotliv 2005). et al. carbonate calcium amorphous with associated acid is usually glutamic shell layers, aragonitic calcitic and both while in dant (e.g., acid is most Tong abun 2004). Aspartic et al. acid glutamic and aspartic like acids acidic amino in rich involved nucleation.are They are crystal in one (Jackson 2010). et al. have others and only matrix chitin offormation the someas molluscs have several genes involved the in considerably vary to shell framework appears the in role of chitin tablets. The crystal nacre individual underlie fibres chitin cells. These mantle vidual extend that well beyond chains indi parallel has : Chitin is insoluble β the is in : Chitin and Shell Secretion at the Mantle Edge at Mantle Secretion the Shell : Acidic proteins are highly diverse highly and : Acidic are proteins (Addadi et al. 2006) and in oysters in and 2006) (Addadi et al. : These proteins are similar to similar are proteins : These Biology and Evolution of the Mollusca of the Evolution and Biology : A report of a mucin-like protein in in protein of amucin-like : Areport (Jackson 2010). et al. -form which which -form was the first first was the ------Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, water against this large concentration gradient in fresh-water in gradient concentration large this water against the from 2008). must activelycalcium be Thus, transported fresh-water (0.1–1.0 mM) the medium in than higher (Deaton much 3.2 of from range concentrations calcium 8.5 mM, to haemolymph the of in fresh-water molluscs the In contrast, molymph of a marine mollusc is about 10 mMmolymph of amarine 8 of concentration Ca the because uptake calcium against water, gradient is no diffusion there not welllayers known. still shell of are the different in carbonate calcium ofduction crystalline of types factors but involved the formed, be cite alone, can pro the in cal layers sometimes although calcite, and and of aragonite below (Figure 3.17). illustrated are fluidand have four proposed been extrapallial ways movement of the of the to ions cells epithelial via possible Figure 3.16. Different in - path illustrated scenario 1979b). Even is complex, so, process the one with possible involving (Loest processes carbonates biomineralisation other in as deposited, be to ditions for carbonate calcium conthe providingions, ammonium by fluidraised is lial pp. 179–216, formation, shell can in Biological Calcification Bonucci, E. in Systems FIGURE 3.16 millimoles. - for of is essential Uptake calcium shell formation. In sea mollusc in shells is most aragonite, often mineral The is possible extrapal pH of the the because Crystallisation

A postulated metabolism of inorganic shell formation. Redrawn and modified from Wheeler,A.P., from of mollus modified and Mechanisms Redrawn formation. shell of inorganic metabolism A postulated A ADP AT HAEMOL -

A - CA or Active transportinplasmamembraneofmantlecells Adenosine diphosphate Any exchangedanion

HCO CO YMPH 2 3 - 2+ in seawater and in the hae the seawater in in and Ca passive diffusion 2 + AT via paracellularpathway MANTLE EPITHELIUM 8

(Deaton 2008). (Deaton metabolites A - CA

or

HCO CO 2 ATP 3 ADP ------Section 3.2.6.6) and shellrepair(seeSection 3.2.6.5). Detailed is lessinvestigated, except inrelation to pearl formation(see of materialtotheinnerlayers oftheshellbydorsalmantle processesoccurringatthemantle edge,but the addition the Most ofthe studies onshellformationhave focused on 3.2.6.4 2009). Steiner Samadi & Patel 2009; 2003; et al. Grande & 2008; et al. Iijima shell (Hinman shape edge shell of field,andthe the Dpp engrailed gastropods, in of shell mineralisation Hox1 are Examples known. of some genes is The function 2007). rapidly (Jackson et al. evolve can derived and are expressed but proteins the served, con genes are signalling factors and whole, transcription the of shell (Takeuchi formation 2016). et al. mechanisms the On evidencealso for to expansion related being of gene families is there factors, and of anumber ing transcription genes and 2011). &Addadi presumably involving (Weiner active transport cavity, haemolymph extrapallial the the to from transported ions Calcium not known. are are gills and roles mantle of the sites respective Regarding of ion the calcium uptake, taxa. CA Shell formation requires complex genetic machinery involv complexShell genetic requires formation machinery AT CO EXTRAP Ca Ca the Shell by the Dorsal Mantle byDorsal Shell the the Addition Interior of to Shell the of 2 2 CA ATP , CRC Press, Boca Raton, FL, 1992. FL, Raton, Boca , CRC Press, + 2 HCO + FL + HCO UID ALLIAL 3 carbonic anhydrase Plasma membrane-bonded Adenosine triphosphate - 3 - H + and Hox4 and CaCO SHELL and nodal and 3 which control the onset which control the which control control which which defines defines which 69 - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 been experimentally demonstrated in shell repair in the land land the in shell repair in demonstrated experimentally been has shell structure resultant and matrix organic the changes in relationshipbetween followedbranes The by calcification. of mem formation organic the with commence Shell repairs involvesalso epithelium (Watabe mantle 1983). changes the to and different markedly is often sition matrix organic of the away compo edge), and mantle the from shell structure the away occur edge shell of (i.e., the the from repairs When &Vermeij shell (e.g., of 1983). those normal as Blundon strength have structural same the repairs the and mantle, the 1972).Saleuddin involve Such repairs or no change in little & (Wong periostracum lacks area repaired of the surface fresh-water Helisoma the planorbidsome, snail like in shell, rest of although the the to structure in similar rial sive review of Watabe (1983). below Much comprehen information the of is from the taxa. out terrestrial more quickly in italthough carried is generally shell, of the part location damaged of the the and taxon on the depending out differs how and quickly it is carried repair the of The nature area. damaged the in tion of new shell material of or broken cracked by shells is accomplished Repair deposi 3.2.6.5 histologically fromthecellsonshell-secretingmantleedge. be ofinterestbecausetheshell-secretingdorsalmantlediffers comparative investigations ofthemechanismsinvolved would Vol.1, Bay, pp. Palm 43–76, CRC Press, and FL, 2017. Press Apple Academic S., Physiology Molluscs of Mukai, S. and Saleuddin, in aspects, 2: Cellular Part shells, onmolluscan K., Developing perspectives Simkiss, from and modified fluid. Redrawn extrapallial the to haemolymph movement the ions from of calcium facilitates that acidity in increase FIGURE 3.17 70 Repairs to the shell edge are usually composed of composed mate usually shell edge are the to Repairs Elec

septate junc Shell Repair troph H HCO

2 H H CO + Four possible involvingFour movement systems the Electrophysiology involves option of ions sites of at formation. shell an + ysiology 3 3 - - tion

paracellular route vesicle with amorphous Ca CO Ve + ex 3 sicular rout

osomes

endoplasmic ex

reticulum trapallial uid haemolymph e , the outer , the - - - - -

failure (e.g.,failure 1981; Vermeij and 2007), et al. Skovsted et al. and frequency of indicator predation an as used been often fossil and on recent shells have Such surface. scars the shell Watabe 1983 Chapter 2). and (see by including neurohormones hormones, mediated are Such damage to mantle. responses the changessue and and - connective tis in cells calcium from mainly shell repair, the is removed calcium and storage damage, with from forciated (Watabe temperature 1983).by influenced be also shell of can the parts composition repaired of the The mineral shells. normal present is in only rarely very carbonate calcium of shell. This form repaired the in aragonite, and/or calcite along with crystals, vaterite for are interest details). special Of (see Watabe matrix 1983 organic the to trauma from resulting probably markedly, differences differs these repair of the ture - shell struc the taxa many shell, in original the in as same the shell layers may repaired be the was aragonitic. While rial mate shell repair the and own matrix, organic ducing their were cells pro mantle snail the 24 hours eggshells, but after eggshell of werepresence the found membrane calcitic as in the in shell repairs initial The its foreign matrix. organic covered and chicken with eggshell with material, membrane ways: three left uncovered,were covered treated inert an with last whorl aspersum the shell of of the C. snail pump F acilitated di usio Shell repairs are usually readily observed as scars on scars as observed readily usually are Shell repairs asso usually are of number amoebocytes the in Increases + Cornu aspersum Cornu Calcium binding Ca2 /H+

calcium ions exchange n + Ca2 /Na+ Biology and Evolution of the Mollusca of the Evolution and Biology . Fernandez et al. (2016) et al. . Fernandez holes made in Calcium cell and these wounds these and deposi Ca HCO CO 3 3 - t - - - , Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 duced bymuch thesameprocessasnatural ones withvarious arepro- Cultured pearls ‘blisters’ onthe inner shell surface. bivalves, notablypteriids,beingthemostprized.Some form are uneven inshape,withsphericalpearlsfrom nacreous budded off fromthemantle(Figure 3.18). Many naturalpearls mantle tissuesecretesnacre. The pearl isformedinapearlsac mantle tissuesecretescolumnar aragonitewhilethemature pearloysters, juvenile the maturityofmantletissue.In inner layersmaydiffer fromtheouterlayers,depending on somepearls,the of theshell,whetheritisnacreornot.In covered withthesameshellmaterialthatformsinnerside of bivalves, but alsoingastropods, notablyabalone. They are (see Chapter 2). mollusc of response the immune of the viewedbe part as shell cover to invasive the object. More broadly, can this layers numerous secretes of thin object. The mantle organic by an is formation stimulated grain), pearl butsand usually (e.g., irritant inorganic an a be occasionally may also This shell. the and mantle lodged the between aparasite, often aforeign to aresponse as is formed object, pearl A natural 3.2.6.6 on Holocenepopulations ecosystems. steppe (hoofed mammals) ungulate changes in estimate to snails (2016)Snegin et al. of frequencies land have shell repair used sources. from various Modified FIGURE 3.18 Shell, Body, and Muscles and Body, Shell, aua erscnb omdnt onlyinawidevariety Natural pearlscanbeformednot

Pearl Formation Pearl

Diagram showing pearl formation in a bivalve and the comparison of the internal structure of a natural and a cultured pearl. pearl. acultured and of anatural structure internal of the comparison abivalve in the and formation showing pearl Diagram fo mantle body reig shell n Struc ture ofnaturalpear mantle cavit l y 9 vaterite rarely, or, of form or aragonite calcite the very either in be It can of carbonate. calcium down is laid crystals as Shell material s 3.2.7 history ofpearls. See Landmanet al. (2001)forfurtherdiscussionofthenatural ‘seeds’ usedthatformthecoreofpearl(seeChapter 10). attachments differs from the remainder of the shell and is called theshellstructureatpoint of muscle a shell.In addition, copy Silveira (Paula & 2009). - spectros infrared and X-ray diffraction, electron diffraction, including microanalysis, methods microscopy, analytical and electron including of scanning methods, by avariety obtained are on shell Such microstructure data properties. chemical shell physical of layers the features their and and graphic 2012). et al. molluscs in (Marin unknown ikaite)calcite, and are (protodolomite, monohydro of carbonate calcium morphs  spicules (Watabe 1983).spicules nudibranch some and of ampullariids capsules egg in and Section 3.2.6.5) (see shell of the parts repaired in found often also is Vaterite hr maybeseveral different crystallinestructuresin There have investigations many been crystallo on the There Struc ture ofculturedpear h ell M 9 (Spann et al. 2010). The other three poly three other 2010). al. (Spann et The icrostructure l periostracum pear pearl sa laye nacre uid ex outer shell trapallia laye r l r c l 71 - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 in shape, orientation, and size and several types of crystalline of crystalline several and types size and shape, orientation, in eral summarybelow. (2009) formoredetailedinformation tosupplementthegen- reviews andtomoregeneral reviews byPaula andSilveira isreferredtothese Geldmacher1996). The reader Bandel & Clark1985; Carter1990a;Hedegaard 1990,1997; Carter & Carter 1990a)andlower gastropods (e.g.,MacClintock1967; 1969; Tayloret al. Clark1985; 1973;Carter & Watabe 1988; from themyostracallayerofPatella vulgata(Wu et al.2017). gonitic andprismatic.CaCO isara- The myostracum layer withintheshell(Figure 3.19). is covered bytheinnershelllayer(s),soisretainedasadistinct areas advance whiletheretreatingportionofmyostracum the Approach. view, aneontological pp. 197–216,tropods, F. McKinney, M. L. Stehli, A Multidisciplinary in G. & Jones, D. Evolution: S.,in Heterochrony Bulletin Fish Commission Game and Weiner, Lowenstam & A. H. S., Biomineralization On FIGURE 3.19 72 The calcium carbonate crystals making up the shell vary shell vary up the making crystals carbonate The calcium Diverse shellstructuresareseeninmany bivalves (Taylor myostracum. As theshellgrows themuscleattachment muscle scar adduc ligamen Topics Geobiology in to

r Shell structure of a mytilid bivalve. Redrawn and modified from Lowenstam, H.A. & H.A. & Weiner, pp. 88–110, S.,from Lowenstam, Mollusca, modified bivalve.in and of amytilid Redrawn structure Shell t patellogastropod A generalised 3 , Plenum Publishing Corporation, New York, Corporation, 1988a. Publishing , Plenum spheruliteshave beenreported , 1–114, 1921, and a patellogastropod redrawn and modified from Lindberg, D.R., Heterochrony in gas , 1–114, Lindberg, D.R.,from Heterochrony modified and 1921, redrawn apatellogastropod and outer prismaticlaye pallial line periostracum inner prismaticlaye my , Oxford University Press, New York, University, Oxford Press, 1989, Weymouth, F.W., Fish California of State nacr ostracum e r r illustrated in Figure 3.20 as follows Figure 3.20 as in illustrated tight biological is under control. shell microstructures (see Watabe 1988, table 3.1). different of these The formation acomplex in resulting terminology subtypes subdivided into be can types shell structural These recognised. are structure 10

ture taxonomiesinclude Bandel(1990)and Vendrasco andCheca (2015). et al. (1969)andCarter andClark(1985). Alternative molluscanshellstruc- structure terminologyusedheregenerallyfollows thatof The shell Taylor nacr Prismatic: Uniformlyorientatedcolumnarprismsofcal- The main types of molluscan shell microstructure are are of shell molluscan microstructure types main The ‘mutually parallel, adjacent structural units (first order ‘mutually parallel,adjacentstructural units(firstorder and Polyplacophora.Simpleprismatic structureshave distributed intheBivalvia, Gastropoda, Scaphopoda, cite oraragoniteencasedinanorganic sheath,widely e a pteriomorphianbival Mytilus prismatic laye -anexampleof brillar laye f Biology and Evolution of the Mollusca of the Evolution and Biology oliated laye crossed-lamella muscle scar my shell ostracum r laye r r r ve 10 r : - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, Carter.) calcitic; foliated,calcitic.Bottomrow -crossedlamellar, aragonitic;sheetnacre,aragontic;columnararagonitic.(CourtesyofJ. FIGURE 3.20

(see Taylor 1973). Taylor (see Mollusca the across foliated structures and lamellar, overlies crossed nacre, inner shell structure This Pojeta 1985). (Runnegar & structure nitic, prismatic arago an outermolluscan shell be layer to appears (Wallernitic 1990). for state the The plesiomorphic bivalves heteroconch calcitic, in while it is arago once. the shellmargins andmayhave evolved morethan but couldhave originatedasarepairmechanismalong from a prismato-nacreous ancestor asoften thought, derived suggested thatthisshellstructuremaynot be &Clark1985). Waller (1990) recognised (Carter some neritimorphgastropods (Hedegaard 1996). prisms orthicker withelongated prisms,asfoundin maybethinwithalmostequidimensional The layer have theirlongaxes perpendiculartotheshellsurface. resemblesalayerofcloselypacked rodswhich It 52). &Clark1985,p. mutual boundaries’(Carter interdigitate along their prisms) that do not strongly This shell microstructure in Pteriomorphia is Pteriomorphia in shell microstructure This Several subtypesofprismaticmicrostructureare SEM illustrationsoftypesshellstructure.Fromlefttoright: Top row -homogeneous,aragonitic;simpleprismatic, - - Nacre ated structures are also iridescent. The distribution The distribution iridescent. also are structures ated of calcitic foli shells, interior and the to restricted is also structure cone complex lamellar crossed of composed aragonite; are Most shell structures shell some structures. with other shared also are ties putative proper in rence but ‘primitive’ these taxa, (iridescence), occur well as their as appearance and composition (aragonite), position shell layers), (inner in homologous be thought to similarity shared they as monoplacophorans. in rarely and Cephalopoda, some bivalves, in nacre columnar Vetigastropoda, some monoplacophorans bivalves; and both in for occurs foliated Sheet nacre. nacre aragonite sheet term the proposed and nacre columnar from nacre sheet (2009a) nacre). distinguished nar et al. Checa may overlapping be (sheet nacre) (colum or stacked The plates Cephalopoda. and Bivalvia, Gastropoda some present in It is microstructure. of nacre tures fea - characteristic the are shell surface the to parallel layer organic laid by and athin separated each sheets Nacres in different molluscan classes molluscan were different in Nacres : Thin, horizontal aragonitic plates (tablets) aragonitic horizontal or : Thin, - - - - 73 Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 includes the Hyolitha and Brachiopoda as outgroups. Original. outgroups. as Brachiopoda Hyolitha and the includes tree probably homoplastic. The are of nacre occurrences The classes. molluscan in of microstructure shell types main oftion the 3.21 FIGURE 74 Foliate T ypes ofshell is absent in polyplacophorans, scaphopods, and and ispolyplacophorans, absent scaphopods, in microstructure calcitic. but This nacre, to are lar different’. fundamentally Mollusca are its derivatives and of nacre the across variants the deposition the of guide that ‘molecular mechanisms the that indicating properties, its crystallographic in of bivalves differs shellgastropods structure and like Jackson et al. (2010, p. 605) nacre- the who that noted by are supported findings monoplacophorans. These in structure nacre-like the and nacre gastropod and bivalve, clearly distinguish characters cephalopod, combinations of subcladeunique these nacres, between differentiates properties individual the none of While examined. taxa the in groups these within variation little be to appears subclades, there major the molluscan between differ they although non-homologous. probably thus and derived, are they separately that 3.21 suggests Figure bivalve in tree on the nacres monoplacophoran, and cephalopod, of gastropod, struc Nacre properties are presented in Table 3.3, in presented and are properties Nacre lamellar crossed prismatic f nacreous oliate : Foliate structures are sheet-like crystals simi sheet-like crystals are : Foliate structures tur e

A diagrammatic representation of the distribu of the representation diagrammatic A

Aplacophor Brachiopod Polyplacophora Hyolitha Gastropoda Monoplacophor Scaphopoda Cephalopoda Bivalvi a a a - a - lamellar Crossed While elongation in different directions may be an may an elongation be directions different While in have derived several been times. structures lamellar observations, concluded they crossed that only three on Based directions. crystallographic different in ferent relative elongated orientation shell are the to dif with structures lamellar crossed aragonitic in 1990). (Hedegaard Fissurellidae but absent in 1990),Hedegaard neritimorphs, in rare 1967; (Patellogastropoda) (MacClintock Lottiidae in common It is commarginal. than is less common structure 1990). lamellar crossed radial Aragonitic 1930;(Bøggild 1967; MacClintock Hedegaard Fissurellidae ubiquitous and Patellogastropoda in 1930;(Bøggild Taylor 1969, et al. 1973). almost It is bivalves and gastropods many in occurs structure 1976). Kohn (Currey & structure convoluted micro criss-cross pathway the through a forced take to are fractures because is absorbed (e.g.,breakage ‘crack as 2004) energy’ Hou et al. to is resistant shell structure lamellar Crossed (570 mya). Cambrian or early Precambrian late the molluscs) in Hyolitha monophyletic are not and Hyolitha (see Chapter 13) Mollusca and (assuming divergence the have extinct of the preceded may structures 2009a). al. lamellar Crossed et (Furuhashi shell structures other in than chitin including 2000), more Denis (Dauphin & material organic alittle has structure other.each This shell layers in to at angles running elongate crystals with similar, simple complex. are and types Both Two present: are recognised. been types main calcitic examples have rare although aragonitic, always is nearly structure derivatives. This shell lamellar crossed all are shellluscan structures mol earliest The cephalopods. than other erans conchif found polyplacophorans and in structure homogeneous shell microstructures. or prismatic, fibrous spherulitic prismatic, mediate inter through developed or indirectly either directly could have group, foliated onmicrostructure ing the ofhypothesis Waller,- depend but cautioned that, lost). (1990b) secondarily been Carter the accepted have layer to prismatic the appears groups many in always developed below layer a prismatic (although foliated layer the that and mineralogy same the share layer, layers both observations that on the based calcitic prismatic was the derived from structure Waller nacre. in (1976) foliated suggested micro that than matrix less organic on aroof. tiles There is the resembles structure crystal one to another, the allel par arranged crystals ofComposed tile-like calcite Paleozoic the Platyceratidae. and patellogastropods bivalves some in such and oysters as scallops, and but some pteriomorphian present in cephalopods, Wilmot et al. (1992) al. crystals that demonstrated et Wilmot lamellar crossed commarginal Aragonitic : This is the most common shell most common is the : This Biology and Evolution of the Mollusca of the Evolution and Biology ------Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 A Summary of the Properties of the Different Nacres in Four Molluscan Classes Molluscan in Nacres Four Different of the Properties of the A Summary 3.3 TABLE Shell, Body, and Muscles and Body, Shell, Note: AA = Amino acid;CA Carbonic Anhydrase activity. Numberoftaxaobserved aregiven inparaenthesesforthelastthreecharacters. Sources of Information: Crystal axistoward the Character Axes intabletplane Twinning No. ofcrystalsintablet ‘Pores’ ‘Pore’ shape Radial membranes Central accumulation Chitin Main AA CA activity Nucleation site Growth zone Texture Texture strength % twinning Angle betweena-axisand interior ofshell growth direction Cone complex crossed lamellar complex Cone 1967), cocculinids, most neritimorphs, and in in and 1967), most neritimorphs, cocculinids, (MacClintock patellogastropods the in occurs ture (1996), Hedegaard - and of Lindberg shell struc this (1985) Clark and sense expanded the of in Carter and 1996). Lindberg & sense Hedegaard traditional In the 1967; shell (MacClintock the Carter & Clark 1985; toward exterior apices of pointing the their with all resemble of cones, stacks closely regular spaced, which of lamellae order composed second are lamellae modification. someto environmental may heterogeneous subject be be and can structures shell lamellar crossed in morphology of crystallites suggestthe findings These nutrients. of increased Tridacna in structures shell lamellar of some crossed deterioration reported (1993) asingleeven Belda taxon. et al. within from and taxa, numerous from structures lamellar crossed orientations)ferent (crystallographic textures in 2010) (2000, al. dif described et Chateigner gins. of indication ori independent an is not necessarily it structures, lamellar of crossed property inherent 1495–1506, 2009;DatacompiledbyC.Hedegaard andDRL. Acta Palaeontol. ChemBioChem,10, Pol. J. Comp.Physiol.B,161,413–418,1991,8–Marie,B.et al., , 39,17–44,1994,7–Machado,J.et al., International Biomineralization Symposium Ago-chō, Japan, 1977 Tokai University Press, Tokyo, Japan,1980,6–Kulicki, C.andDoguzhaeva, L.A., Watabe,N., inM.Ōmori & molluscan shells,pp. 49–56, Report), Vol. 2, Texas MUniversity,A & Galveston, TX, 1970,4–Mutvei, H.,Zool.Scr., 7,287–296,1978,5–Mutvei, layerin H., The nacreous inE.Chin,ScientificResearch oftheSoutheast Scientific resultsoftheSoutheast Pacific Expedition.II,pp. 1–12, Pacific Expedition(A.Bruun K., 2000; Chateigner, D.et al., Mater. Sci.Eng., 528,37–51,2010,2–Grégoire, C.et al.,Annales del’Institutocéanographique , 31,1–36,1955;Iwata, J. Fac. Sci.,17,173–229,1975,3–Meenakshi, V.R. Ultrastructure,histochemistryandaminoacidcompositionoftheshellNeopilina: et al., 1 – Hedegaard, C. and Wenk, H.R., Sources 1 1 1 1,5,6 2,3 2,3 2,3 2,3 3,7 8 8 1,5 1,5 1,2,3 1,2,3 1,2,3 1,2,3 related to the availability availability the to related : Prismatic first order order first : Prismatic C-axis Aligned Weak/absent 1 Absent – Present – Absent – – Edge oflower tablet Entire surface Fibre – – – Monoplacophora J. Molluscan Stud., 64, 133–136, 1998; Chateigner, D. et al., The Mechanisms ofBiomineralization in Animals andPlants.Proceedings ofthe3rdThe Mechanisms - - Bivalvia C-axis Aligned Absent 1 Sparse Small, round Absent Absent Absent orpresent Gly,Glx Asx,Ala,Arg, Yes Edge oflower tablet Entire surface Double twin 49–>9999 (10) 12–67 (11) 90–95 (9) Helical of type Irregular complex crossed lamellar: This cal shell microstructure enable the construction of enable construction the shell microstructure cal Cavolinia pteropod of the shells of the species in repair with tion associated shell deposi secondary in transitions structure cal heli to dendritic reported and structure, lamellar crossed to similar which are structures, acicular were crossed derived from structures helical that Cavolinia Miocene the including was pteropods found other in structure columnella Cuvierina pteropod of the bivalves 1985). Clark (Carter & 1990), (Hedegaard arcid in and most neritimorphs in lepetelloidean Osteopeltidae, the patellogastropods, units’ (Carter & 1985, Clark p. 62). It is found some in structural order second aggregationsing of parallel interpenetrat shaped, of ‘irregularly comprised lae order lamel first the has structure lamellar crossed bivalves. autobranch (Hedegaard 1990). fissurellids It isalso in some found : First reported by Bé (1972) et al. reported : First shell the in (Bandel 1990). (Bandel Bandel (1977) suggested Gastropoda C-axis Unaligned – 1–20 Abundant Small, round Present Present Present Gly,Ser Asx,Ala, No Centre oflower tablet Margin Fiber 88–90 (2) – – Vaginella , and living living , and . The properties of heli . The properties J. Struct. Geol., 22, 1723–1735, Cephalopoda C-axis Aligned Prominent 3 Abundant Large, oval Present Present Present Gly,Glx Asx,Ala, No Centre oflower tablet Margin Double twin 51–333 (2) 50–92 (2) 75–100 (2) Diacria , this micro , this and and ------75 Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 for shell structure impressions Runnegar and Pojeta and (1985), impressions Runnegar for shell structure steinkerns Cambrian view. traditional examining this After seriously has luscs hypothesis no alternative challenged and Bivalvia.the except one another with in seldom and co-occur structures prismatic outer spherulitic most the likely derived from are ‘nacre.’ called ‘replacement’all these shell structures All and which some others were includingfoliated, fibrillar, tures have by- replaced several been shell struc structures lamellar layer.ous nacre aragonitic layer inner outer calcitic prismatic an an and 1990),Hall shell monoplacophorans, consists of the in while layersmatic, homogeneous, lamellar (Carter & crossed and outer calcitic homogeneous layer 1990a). (Carter covered sometimes lamellar, by crossed athin, aragonitic where it is predominantly more derived taxa, the with trasts bivalves pteriomorphian strongly and con gastropods early in The high diversity systematicas of characters. shell structures bivalves and ofgroups gastropods have extensively been used some in structures larly diverse well-studied. The shell and particu are bivalveOnly shell microstructures gastropod and 76 There is a general belief that nacre is plesiomorphicThere is mol nacre belief in ageneral that plesiomorphic crossed perspective, inner From ahistorical - consists pris of aragonitic Polyplacophoran shell structure Homogeneous the homogeneousthe layer. in embedded of sections those structure the describe (1996) Hedegaard to by used Lindberg & been has ‘relics term of…’ The of awell-defined structure. pattern the into arranged are homogeneous structure of the granules where the structure, more distinct (1985). Clark and enclose also of sections a It may of Carter banding accretion the with as organisation, homogeneous although neous layers may show some homoge it is called granules, minute than other no identifiable has elements when ashell structure 63). 1985, &Clark Thus, p. tion (Carter banding’ except for arrangement possible accre structural order first clear lacking crystallites shaped ularly ‘aggregations of irreg more or less equidimensional, for is used term axes. The crystallographic of the arrangement an retains it although still substructure, is no discernible there it as that implies unfortunate, ‘homogeneous’ is bivalves. shell structure The term and gastropods various in seen are shell structures Such pattern. showsthat ahomogeneous structural 1981). forces (Vermeij crushing to 1978,tance 1979; Paul resis- shell, it giving the greater strengthen varices Murex neogastropod of the varices the in layers lamellar crossed among structures helical water live Bandel column. the (1990)that in found et al. 2011), Zhang et al. 2006; for ideal organisms (Daraio impact to light shell resilience with a thin, : An aragonitic or calcitic structure or calcitic structure aragonitic : An . These . These ------expensive trade-off. which produce, to is another composition, of organic is energetically its because high nacre tension, under compression, or when although bent, structure compression. strongest the shell is generally Nacre than omorphian pinnids,andsomestylommatophoranlandsnails. material, asintheshellsofprotobranchSolemya,pteri- of crystals. lattice criss-crossing due the to restricted are cracks advantage that the has strong and is also structure lamellar weakest. Crossed 1990), the being homogeneous foliated with and structure 1988, (Currey shell having structures those other ger than stron not dwell are here. Shells nacre with built details on the so we need of shell microstructures properties mechanical the (1990) Currey of thickness. excellent provided an summary its and shape and shell of structure the properties mechanical 1972; Mutvei 1983; Bandel 1988; Dullo & 1990a). Carter Mutvei 1967; et al. Erben 1969; Taylor et al. 1969, 1973; Batten Mesozoic, 1930; (Bøggild Recent nacres and 1966; Grégoire Paleozoic, between differences no demonstrated are but there (seetaxa Chapter 18, Figure 18.6). some is only vetigastropod present in and patellogastropods is absent in nacre Figure 15.4). In gastropods, Chapter 15, shells except (seelamellar for some Anomalodesmata have Unionida), crossed primarily heterodonts whereas non-heterodont Pteriomorphia, in bivalves (Protobranchia, present primarily are structures Nacreous Cephalopoda. except taxa for conchiferan Monoplacophora all ent and in - pres layers also lamellar are Hyolitha, Crossed others. and shelled outgroup extinct, Polyplacophora, the in in and present being structures lamellar notably crossed with molluscs (see within of nacre distribution Figure 3.21),the conclusion. similar a (2011) Vendrasco also see et al. taxa, molluscan different for in structure plesiomorphic lamellar dently the aragonitic from evolved shell structures indepen lamellar crossed and nacre (2000), by Kouchinsky who considered it ported likely that sup was also This view state. one was closer ancestral the to tive itmolluscs, thus was whichand not possible determine to - puta earliest these present were in both structures nacre and by Wallerrepeated (1998), lamellar cone crossed that noted or by shell structure, thus falling into two main groups, groups, two into main falling thus or by shell structure, 1989).Mapes either by formed Shell pigments colours are & were developed evolution molluscan in early (Kobluk Paleozoic early in fossils showof such patterns patterns that colour) ultraviolet under light (e.g., 1974) Krueger traces and shells. Even (not fossil reveal shells colour can the patterns of molluscan notable many features are patterns Colours and s 3.2.8 Shells are more easily brokenShells by apart) are tension (pulling Flexibility isincreased byincorporatingmoreorganic by the of ashell is determined strength the general, In older in of sparse, fossils nacre are reports Regrettably the by is plesiomorphic nacre is not supported that The idea h ell C olour Biology and Evolution of the Mollusca of the Evolution and Biology , P a tterns , a nd P ig m ents - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 2002). In al. et outer shell layer (Brink transparent the in embedded aragonite of crystalline microstructure regular highly from In have to developed appears patellogastropods convergently. blue colouration (schemochromes)The structural two these in Helcion pruinosus pellucida Patella limpets patellogastropod including the some gastropods in seen colours are structural of of Examples nacre. (pearly) such iridescent appearance the from colouration by caused it differs pigments, and also shell of anormal that ration is from relatively differs and rare colou Such structural microstructure. surface modified from or diffraction by colouration caused interference iridescent (Fox 1953,pearls 1983). Some shells have of patches bright of shells nacre and layers the such in as of carbonate calcium thin very of interplay light through the from colours resulting pigments) (Fox 1966). include Schemochromes iridescent Shell, Body, and Muscles and Body, Shell, Laminaria 3.22 FIGURE colours. tones or up of made contrasting patterns or irregular regular colour, or or graded of exist auniform as They may matrix. organic the and periostracum the in shell, and/or down the in may laid be wavelengths absorb. of They cannot light they seawater. in absorption light of band minimal blue ofrange the the colour is within on which P.fronds pellucida Laminaria the inhabit colours also blue bright with warning two of species noxious because nudibranchs Batesian mimicry (2015b) et al. Li colouration may the indicate that speculated and waterily atseveral distance, visible the meters through 2015b). of P. stripes pellucida et al. (Li The blue provide for thus vividabsorb contrast light and the blue colour that of colloidal particles array by an underlain are lamellae layer. lamellar These irregular, transparent, a thin, underlies schemochromes Pigments (biochromes)Pigments show colour reflected of the the as . pruinosus H. in the intertidal. (Courtesy of Malcolm Storey.) of Malcolm (Courtesy intertidal. the in P. pellucida

Patella pellucida Patella (structural colours) (structural biochromes and , it is caused by interference or diffraction , it or diffraction by is caused interference which have or spots. blue bright streaks , the microstructure of calcite lamellae of lamellae calcite microstructure , the lives. Interestingly, spectral the – East Cornwall, England, on England, Cornwall, –East (Figure 3.22) and and (Figure 3.22) are read are (true (true - -

ther by Boettiger et al. (2009). Gong et al. (2012) (2009). by Gong et al. ther Boettiger et al. this used was developed later fur activity. by cells ing neural This (1986),et al. which involved control of the pigment secret light of aphysiological the in posed model of Ermentrout (1987) Klingler and computer model by Meinhardt was pro subsequent A for process. account to the mechanism cal adefinitive physiologi but not suggest did patterns, tation (1969) acomputer model for proposed pigmen simulating Waddington Cowe ofmation and pigmentation patterns. for have for account to the proposed some theories been ofcapacity most molluscs. or lack of, visual limited, of the because ration or patterning reason unlikely for coloushell an is recognition interspecific reasons, colour. same sediment the For these with correlated (1994) shell colour the of some of that species Oliva noted For example, even organisms. burrowing in Savazzioccurring isms. Nevertheless, colour selection may for be cryptic or fouling organ opaque by periostracum ration is hidden an shell colou or their sediment in livepossessing them buried species is even many because more enigmatic patterns their unknown. remain molluscs exist many in that diversity great of patterns the colours and (if any) reasons the for understood, shell colouration is readily selective polymorphic the and while advantage of cryptic production. Thus, cost of metabolic their assumed the ity and given complex accept to their molluscs, is difficult but this have to many in on function shells appear no apparent terns Bauchau (2001) pat pigment their that colours and observed unknown. any, remains if patterns, shell of colours and/or the molluscs utility, other many the in some although species, in may pigmentationdation, patterns explain colour the and/or selection apostatic (see in ing below) pre by visual reducing result such polymorphism, as mechanisms other and Crypsis (e.g.,tic 1991; Lindberg 2009). Sorensen & et al. Manríquez more cryp them byadvantage some to making individuals 1951a), aselective impart such also changes phenotypic can (e.g.,simply of waste disposal metabolic afunction Comfort are food-derived patterns these or not Whether gastropods. (e.g., Gibbs 1993; et al. 2009), Manríquez afew and veti other 1990; Sorensen & 1991), Lindberg caenogastropods predatory &Pearse several (Lindberg in patellogastropods onstrated 1976).Creese Such changes phenotypic have dem been also & &Underwood 1976;wave Underwood exposure (Creese to of which available to is related indirectly food and algal abundance and concentration the I, pigment uroporphyrin trochid intertidal the in colour patterns For example, striped variable changes. diet as changing latter the food, with or derived from (see below), by-products the of are metabolism others while genetically determined are patterns shell their pigments and layers. inner the Some in occur also pigments can although outer shell found layer, the is usually in edge and mantle the Although their reason for reason mysterious, existence is often their Although or selective of colours and functional utility The possible by pigmentation shells, is molluscan imparted the In most Austrocochlea porcata are mainly composed of the of composed the mainly are was was 77 ------Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 and and Umbonium trochoideans such the as pods gastro bivalves beach sandy toral such pectinids, many as 1962) and (Moment bivalves variabilis include beach sandy the Donax fresh-water and molluscs (Clarke 1978).marine Examples examples both many among colour numerous with morphs overviews are available there Besides are date. to snails, land 1987a), 1972;Parkin Goodhart no comprehensive although examples (e.g., snail land other numerous 1951b; Comfort (e.g., nemoralis Cepaea 1977), also Jones et al. are but there snail land a few European most the famous being the species, investigated phenomenon only been of has in this nature the 2013).et al. (Scheilferent have demonstrated colour morphs been also 2013a). et al. Cameron dif in responses immune Different (Cowiesnails 1992a; Cowie & Jones 1998; Cook et al. 1999; some long-term in on helicid studies demonstrated been has over colour morphs time, of frequencies particular the in 2013).genes al. (e.g., et Zheng Change, or lack see of it, by one only to afew determined colourknown, is usually 2013). et al. Zheng Where 2009; 2001; Evans et al. et al. 1988; &Castagna Winkler bivalves (e.g., Adamkewicz 1997), &Johannesson some and 1984, 1985b; Ekendahl (e.g., snails 2004), some Chiba marine Palmer Hayashi & 1976; Bogan Clarke 1984; 1999; Roth & Chiba Murray & 1966; King Owen 1969; 1950; Sheppard Cook & Cain & relativelyin (e.g., examples few snails some being land taxa, demonstrated only been has this although determined cally remains untested. mark theshellsurface. To ourknowledge, thishypothesis coloured ornon-pigmentedshellsused‘othersubstances’to thatuniformly regulate thegrowth oftheshell.He proposed shell edgewhichassistedthemantleneuralnetwork to posed thatthepigmentationpatternscreatedaheterogeneous generated donot explain whythey exist. Bauchau(2001)pro - noxious animals. coloured brightly or other nudibranchs with them confuse to shell which Savazzi (1998) suggested may cause predators patterned often coloured, brightly contrasting, markedly the it is withdrawn, exposescovers this shell may the be. When (Savazzi 1998), often that mantle of form colour the and the not cryptic are shell patterns the of shell. While thicknesses result of the different often are visible and mantle, patterns by overlapping the secreted shell having due the to been ture - struc in molluscs),other three-dimensional actually are they (as two-dimensional in be to appear these While species. (Cypraeidae), found most in are colour patterns In cowries 1976; Kunigelis 1984).(Saleuddin & Dillaman Saleuddin & on work planorbid done on mainly the Helisoma based being control is not strong, neuroendocrine networks and neural of species Conus in colour patterns network diversity remarkable model explain to the neural of 78 of the mangrove-saltmarsh species of species Littoraria mangrove-saltmarsh of the Some but molluscs colour exhibit polymorphism, distinct of molluscs many is probablyThe colour largely geneti models that explain how pigment patterns might be The Bankivia (Whiteley et al. 1997), al. sublit et (Whiteley cornea Donacilla (Clarke 1978; Ermentrout et al. 1986), al. some (Clarke 1978; et Ermentrout . The evidence for such . The evidence (Grüneberg 1980) (Grüneberg (e.g., Reid - - - -

Warwick 1983) Nerita and ofshore species Littorina oualaniensis and Batillaria1987), mudflat batillariids colour. For example, the effect of temperature in some snails colour. some snails in For example, effect of the temperature by determined including those polymorphism, maintaining in Non-biologicalpredation. important factors be may also may not only of and speculation is amatter aresult of be visual Absalão 2005). & &Ekendahl 2002;Rodrigues Cook 1998;Johannesson 1997; Mather 1986;Reid1987;Cain1988b; Whiteley et al. 1975; Joneset al. 1977;Heller1979;Palmer 1984;Hughes & &Sheppard 1950,1952,1954;Smith ronments (e.g.,Cain advantage of colour polymorphisms in heterogeneous envi- individuals suchenhancedcrypsisisanobvious selective ferences inspatialdistributions ofcolourmorphs.For some suggesting thatselective visualpredationcanmaintaindif- theirbackgroundweremorelikely tobetaken,did not match Sorensen and Lindberg (1991) showed that individuals that al.1987;Byers 1989).Crypsisisparticularlyimportant. et a formofcamouflageagainst predators(Giesel1970;Hockey in rocky shoremolluscs, suchaspatellogastropod limpets,is 2008). Drent shell (Luttikhuizen & visible the through be can floating juvenilesthis small in opaque shell, although of the interior the expressed only in are that colour morphs balthica bivalve tellinid the Macoma above. noted as In stracum, perio athick beneath hidden are shell patterns colourful 1989). &Mapes Similarly, some complex and Kobluk eyes were sufficiently well-developedthem see to (e.g., evolved colour past, patterns the 2008), in Drent before and shell of (e.g., the interior the 1988a; Cain Luttikhuizen & fortors, example, some bivalves in only visible are they in - preda from hidden colours oftion, are the some polymorphs - have preda studies selection visual to related demonstrated some not While develop morphs. the for image all asearch can predators the because predators advantage visual with evolved predation. visual through primarily were have to many, colour unlikely forms intergrading, often (1980) byduced Grüneberg cover to examples where there 1987a(see was intro Goodhart for term review). The latter pseudo-polymorphism and effects, coadaptation, area drift, genetic mating, effects, selection,assortative apostatic climatic disruptive and visual, crypsis, are latter effects. the Among including non-adaptive findings adaptiveand explainto the several with 2008) invoked &Drent concepts Luttikhuizen (e.g., 1987a; selection, biochemistry tional and Goodhart - direc frequency-dependent and genetic drift, inheritance, molluscs have involved of arange including approaches (e.g., 1978; Clarke Bunje 2007). colour polymorphism and exhibit also pattern water neritids (e.g.,tons Rodrigues &2005). Absalão Some of species fresh- Usually the nature of the selection of the on shell colour morphs nature Usually the Several workers have suggestedthatcolourpolymorphism is have thought to Colour polymorphism aselective investigatingStudies shelled in colour polymorphism Velacumantus , there are four, apparently genetically determined, four, genetically determined, are apparently , there (Grüneberg & Nugaliyadde 1976), (Grüneberg & some rocky (Ewers & Rose 1966), (Ewers & neritid the Biology and Evolution of the Mollusca of the Evolution and Biology (e.g., Reimchen 1979; Atkinson & (e.g., 1969), Safriel afew and chi (Miura et al. 2007) 2007) al. et (Miura Clithon Clithon - - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 11 porphyrins study (Comfort early 1950, an with known 1951a) showing that 2013). et al. 2010; Mariottini (e.g., species same of forms the distinct cally et al. Nakano morphologi genetically and/or representing as interpreted be (e.g., 2014), Joseph colour may et al. forms allopatric while taxa different be to appear species same of the morphs as 1999). colour regarded forms sympatric different Sometimes, (e.g., predation visual from 1962; Clarke 1988; Allen Chiba colour divergencein frequency-dependent selection through Ewers & Rose 1966; 2000). et al. McKillup invoking of aform morphs, selectionfavor (e.g., particular (e.g.,radiation Heller 1979). or parasitoids may Parasites also 1977) shells may UV offer darker from more and protection of dark-shelled Mytilus in observed morphs been (Burla & 1993). Gosteli grasslands alpine effects have Similar locations or in (Jones 1973; 2007) al. 1989; Stine et Miura light-coloured shells maywhile of warmer be advantage in maymore rapidly thus have and cold advantage in areas, an &Berger where 2000), heat dark-shelledSokolova morphs (e.g., 1975; Heath 1977; Jones et al. 1988b; Etter 1989; Stine ments in some shellsments in (Comfort 1951a). (Jones & Silver turbinids and 1979). trochids, otids, colourationbrown, (e.g., or red some colour hali in green the responsible are for and blue, green, porphyrins than common bivalves for references). (see 2006 et al. Hedegaard responsibleas pearl-producing for colour and of the some pearls 2017)shell colouration have (Williams identified and been also 1976). Creese brown, or purple red, produce compounds These & available on the chlorophylldepending (e.g., Underwood vary can ably food via and chlorophyll derived from obtained prob are They conchoporphyrin. Iand uroporphyrin being most common the with aring, form rings pyrrole the In these, Porphyrins 1976). (Fox blue, orange, green, violet,red, yellow, or brown colouration produce (bilins) and structures or linear (porphyrins) tures –cyclic- struc forms two main in occur shells.luscan They bile pigments. and including porphyrins tetrapyrroles, and follows (2017). review arecent by Williams below largely summary The 2006). al. et Hedegaard 2006; &Waal (Barnard common enes, are including carotenoids, have shown poly that microspectrometry Raman Resonance elusive. pigments remains latter usingthese Recent research 1951a), not (Comfort nates’ are they composition the and of acid-soluble,are ‘pulmo and caenogastropods but many in ‘opisthobranchs’, vetigastropods, and pods, shell pigments the Shell, Body, and Muscles and Body, Shell,

red in haemoglobin. in red heme–the is of which one pigments, includes of compounds This group ( methine and atom carbon their via connected subunits role pyr of four comprised compounds organic macrocyclic or Heterocyclic The chemical composition of poorly shell pigments is rather may species result two between sympatric Interactions Quinones Bilins Tetrapyrroles melanin, carotenoids, shell pigments are known The main , where the pyrrole rings form a chain, are much less are a chain, form rings pyrrole , where the 11 wr rsn.I lower bivalves, patellogastro were In present. may responsible be for non-acid-soluble the pig are the main acid-soluble main the mol pigments in are are the most common shell most pigments. common the are (Mitton + CH–). CH–). ------Velella Janthina blue-violet colouration pelagic of ‘violet the The striking snail’ pigments suggesting may widespread. these be spectra, Raman Waal using and (2006) by some Barnard neogastropods and 2014b) et al. Li 2006; have and found shells of in been pectinids al. sible for yellow the et colour (Hedegaard of some pearls 1981). Merlin (Dele-Dubois & respon be may also Carotenoids werein Strombus and identified 2006) et al. (Hedegaard for yellow the (Cypraeidae) of aspecies colouration cowry in responsible are Carotenoids taxa. as in someshell fied pigments have they shells, although in identi compounds been since these 1996;Vershinin 2001), Matsuno (1951a) Comfort not find did (e.g., tissues molluscan in 1972; Goodwin not uncommon are carotenoids Although taxa. pigment different adifferent to in for with, taxon pigment, colour example, due and being same the but was found no relationship clear colour, there between taxa, shell 13 gastropods, pigments in four bivalve and one cephalopod, polyenes identify to as microspectrometry Raman Resonance Nucella situation is more colour complex shell of in ground the the as 1936).(Moore Subsequent work, however, shown the has that diet is changed the colour change if in abrupt an food, with when brown Mytilus purple to and of barnacles lapillus ofThe shell Nucella (e.g., dramatically times Leighton 1961; 1980). Tajima et al. Haliotis food (e.g., the pigments in from 1951a). Comfort For example, novo derived de genetic are basis and colours have food the or whether the from a sequestered being investigated pigments are the whether to as not been Most have cases of cryptic. these them rendering substrata, their food and/or colouration their as or similar same the of haveto indigoids shells. subsequent in reports been do not appear indigoids there supposed and may pyrroles, be (Comfort 1949), (1951a) but Comfort suggested later these some shells,present in such be to as yellow, black brown, and thought colours. red, Indigoids are (Glass et al. 2012). probably are responsible Melanins for some 2014) sacs (Derby fossil in ink detected been also has and component ink of cephalopod important is an eumelanin Lymnaea 2017). shells of the from have reported Melanins been (Williams pheomelanin and two – eumelanin come forms in indigoids. and Melanins molluscs twoin melanins forms, in have investigated. not been found afew shells, but also in these gastropod ments are other Waal Blue 2006). pig (Barnard & structure chemical the ing alter may chemically be gastropod the suggesting that respects, responsible carotenoids some in the forthat colour differed the 12

 carbon double and single bonds. single and double carbon to carbon multiple from resulting state low energy their to due colored often are that compounds organic conjugated of polyunsaturated A group The shells (and often the animals) of (and molluscs many animals) The shells adopt the often Indoles found have pigments as are and abicyclic structure Polyenes . Analysis pigment of Velella the in (Spight 1981; Emery 1976a; Castle & Palmer 1984) fed on different algal foods change colour, fed algal on different some is like that of its that prey, is like siphonophores the and Mytilus and 12 include carotenoids include , but are presumably more widespread; , but are may be white or grey with a diet adiet may with white or grey be . Hedegaard et al. (2006) used used et al. (2006) . Hedegaard . Some are clearly. Some derived are and Janthina and Haliotis cracherodii Physalia is the main main is the showed showed shells shells and and 79 - - - - -

Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 nautiloids and belemnites having developed sculptural sculptural developed having belemnites and nautiloids itself some fossil presents with with picture cephalopods, A different shells lack sculpture. cephalopod and cophoran monopla extant - All or have sculpture. smooth ally radial gener developed are Scaphopods or granules some taxa. in or it ridges and/ either with is subdued, lack sculpture orans bivalves in polyplacoph is seen while - gastropods, ture and spines. or ules, - nod granules, in as or discontinuous ridges, frills, lines, in as some bivalves (Seilacher 1972). continuous be can Sculpture divergent,edly of sculpture for as example, divaricating the in elements mark be can sculptural the some taxa, ments. In ele radial often also are there growth, in some discontinuity 13 collabrally, arranged is usually sculpture long to While or heavy knobs. spines lines growth enhanced from ranging a wide of range ornament bear Shells can s 3.2.10 ancestry. shareacommon and itisunclearastowhetherornot they chiopods areallvery different (Reindl & Haszprunar1996b), Pteriomorphia) bivalves, vetigastropods, chitons,andbra- ture ofthecaecainsideporesinarcoid(andsomeother the pores in gastropods are less modified. struc- The detailed 14),but thecellularextensions thatenter ing (seeChapter called aesthetesandhave sensoryfunctionsincludingimag- thecaecaare caeca mayassistinsuchexchange. In chitons, mation betweentheorganism anditsenvironment, andthe the shelllimitsexchange ofmaterialsandsensoryinfor (e.g., line lial Waller 1980). however,Arcoidea, side pal of inner the on the dense are they juvenile the to shell (as Cyrenoidea) in (Waller 1998). In the restricted shell or are the through right do not penetrate and 1994, bivalves, 1996a). sparse Haszprunar are they In most shell layers formed the (Waller 1980; penetrating tle Reindl & In bivalves, man by formed the projections from are pores the soids), lack Chamidae], but them. and most cyrenoideans, taxa some bivalves [some limop (all and arcoids pteriomorphians 2010b), al. et afew(Sasaki neritoideans, glacidorbids], and [some some neomphaloideans fissurellids, gastropods both apatchy within distribution They have barnacles. and cods, - ostra bryozoans, some brachiopods, in occur structures Similar caeca. called extensions are entercellular them that the and pores, by minute penetrated shells are gastropod and plates,Chiton monoplacophoran some shells, bivalve and s 3.2.9 the fromby pigmentsderived food. modified be and 80

 margin in abivalve). in margin shell the or of agastropod aperture of the lip (the outer shell of the edge growing the to conform that lines growth or ornament – shell Collabral In extant molluscs most shells, sculp with elaborate the In extant The function ofmanyThe function ofthedifferent caecais uncertain – Haliotis h h ell (Liu et al. 2009) has a genetic basis, and this can can agenetic this et al. has 2009) basis, (Liu and ell P O ores rn am ent

a nd I ts F unction 13 which implies implies which ------array of sculpture in ammonoids. in of sculpture array bizarre sometimes, and, amazing elements an with and suture (Vermeijsuture 1993). is aprotruding but shell is smooth, there the others, in while side steep toward apex, the which the has sculpture ratchet develop also arranged gastropods Some spirally burrowing valves the (Checa & strengthen also Jiménez-Jiménez 2003). Such oblique ridges not only enable efficientthey burrowing, when burrowing. shell rotates the as sediment the grip they ones, so posterior the to angles atright ridges are anterior of edges; oblique dorsal the steep ridges with This consists Divaricella example, lucinid the in haveseen as for sculpture, version – amodified divaricating found several in bivalve (Vermeij families 1993) some and is of sculpture type This page foot when the is extruded. movement,resists backward by assisting slip thus reducing opposite face on side the asteep while sediment the through slip that of burrowing edge toward direction rounded the a ridges with has bivalve live It sand. that burrowers in (e.g., Seilacher1985;Savazzi 2005). bore usingmechanicalmeans(e.g.,pholadidsandteredinids) ture seenintheanteriorpartofshellbivalves which 1993; Seilacher1985;Savazzi 1989)andthefile-like sculp- gastropods andbivalves (e.g.,Stanley 1981;Signor1982a, bly theso-calledratchetsculpture(Signor1982a)insome sculptural elementsincludeassistingwithburrowing, nota- tion onsoftsubstrata.Otheradaptive functionsforcertain adaptive rolessuchasproviding camouflageorforstabilisa- tion defenses,ithasalsobeensuggestedthatspineshave other to antipreda- sculpture, especially inthetropics. In addition important selective agents intheevolution ofmolluscanshell Palmer (1979)concluded thatshell-crushingfishhave been follow-up work, down ifdetachedfromthesubstratum.In lisation andincreasingtheprobabilitythatitlandsaperture Ceratostoma foliatuminproviding hydrodynamic destabi - tally demonstrated the role of the shell varices in the muricid (Willmanwas not reduced 2007).Palmer (1977)experimen- artificial spines on Rollins2002),experiments using courage borers(Beatty & While evidence suggeststhatspinesonbivalves maydis- were not effective against predationbystarfish(Stone1998). cids andstarfish.Spinesdeterredpredationbymuricids, but tested theeffectiveness ofspinesagainst predationbymuri- attempts totestthis.Experimentswithepifaunal bivalves in deterringpredators,but therehave been relatively few ing crypsis.Ribsandspinesonshellsshouldlogicallyaid for sedimentandfoulingbiotatolodgethusfacilitat- Some sculptureroughensthesurface, increasingtheability or have whorl reduced overlap (Vermeij 1973b, 1977b). Vetigastropods glaze cover to tend athick with any sculpture 1972; Signor 1982b), recycling enabling calcium. of the is dissolved (e.g., sculpture by mantle the truding Carriker whorl pro the preceding of the part over sculptured the ammonoids), (many and shell grows gastropods ture the as In coiled molluscs develop that In coiled sculp projecting elaborate The ‘ratchet sculpture’ is common in shallow-water ‘ratchet in sculpture’ is common The isusuallyassumedthatshellsculpturefunctional. It Mytilus foundthat predation by Biology and Evolution of the Mollusca of the Evolution and Biology and the tellinid Strigilla tellinid the and Nucella - - - .

Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 of this process have not been investigated. been Similarly, the have process of not this details the although by mantle, the is presumably secreted and pholadid Martesia wood-boring of the individuals mature in gape covers pedal callum, the pholadid the bivalves. A plate, shell plates in accessory of formation the the in occurs also 1959; 1969). Grahame Subdivision presumably mantle of the left valve the to (Kawaguti attached shell remaining larval the left shell ‘valves’ and right divides produce to atsettlement with In bivalved sacoglossans (the ‘bivalved gastropods’), mantle the (e.g., substratum the to plate attached 1991, Knudsen 1993). calcareous sole abasal the foot of the secretes of hipponicids edge, and by mantle the long form vermetids secreted tubes structure thantrueshellsecretedbythemantleedge. detail). The shell materialcomprisingthesetubesissimplerin 15formore al.2011;seeChapter 1984, 2006c;Mortonet secreted byglandsonthesiphon(e.g., Savazzi 1982;Morton loidea), shipworms (Teredinidae), andGastrochaenidae,are Adventitious tubesformed bywatering potshells(Clavagel- s 3.2.12 subfamily Fraginae. dows arealsofoundinsomeothermembersofthecardiid Schneider 1997).Similar,(Carter & but lessdeveloped, win- may help to focus light on the zooxanthellae bearing tissues mainly fromtheouterprismaticshelllayer, andtheirshape Signor 1986;Seilacher1990). These ‘windows’ areformed through theshellinaway analogoustofibreoptics(Watson & of theshellforming‘shellwindows’ thatfunnellight Corculum cardissa whichhasanteriorandposteriorpatches known example isthecardiid thesising symbionts. The best fied todirectlightontothetissuescontainingphotosyn- symbiotic zooxanthellaewheretheshellstructureismodi- apomorphic ‘shellwindows’ arefoundinafew bivalves with Kellogg 1975; Lindberg & tion (Lindberg et al. 1982). More on the anterior part of the shell which lack further modifica- strated thatitrespondedtolightthroughtranslucentpatches patellogastropod limpetwas investigated, anditwas demon- tal studiesoncoiledgastropods, but asimilarsituationin awarethis partoftheshell. ofany experimenWe- arenot of theshellbehindaperture. The eyes canbeseenthrough shell have atransparentpatchinthelastpartofwhorl or semitransparentshells,but someofthosewithanopaque Many speciesofsmallcoiledgastropods have transparent s 3.2.11 cockles. bivalves and some scallops than other well as most as cephalopods, extant and chitons, scaphopods, 2010).(Örstan elements absent in are sculptural Such internal pneumostomeprevent blocking the from foot the snail of the shell. ellobiid In the Pedipes the or strengthen to predators to barriers as serve thought to 1991) (Paul structures often other ridges, and are of that teeth, developments elaborate may contain shell. The aperture the Shell, Body, and Muscles and Body, Shell, In gastropods, gastropods, In of the outer part to is not confined gastropods in Sculpture h econd ell W a Magilus indows ry S h ell (Muricidae, Coralliophilinae) and and Coralliophilinae) (Muricidae, S , it has been suggested these teeth teeth suggested, it these been has tructures

and otherparticlestotheperiostracum(Sartoriet al.2006). mucoid substanceswhich enable the attachment of sand grains gins ofseveral otheranomalodesmatan bivalves. These secrete Multicellular arenophilicglandsarefoundonthemantlemar onal glandshasagglutinatedsandgrains(e.g.,Morton1984). shells (Clavagellidae), theadventitious shellproducedbysiph- watering pot and shellformationatthemantleedge.In some shells (e.g.,etc. their to 2007). Allgaier lichens fragments, leaf dirt, attach shells. Some snails land Granicorum (Scaliolidae) venerid Scaliola bivalve the gastropod and dean cerithioi the examples shells. are Other of their outer surface shells, stones dead etc. the to Xenophoridae which attach most of some famous examples members the are The shells. on the agglutinated objects are other sometimes and few grains sand bivalve taxa, gastropod and In a predation. shell against provideandprotection hence the camouflage on growing shelled molluscs, many organisms epizootic In 3.2.13 not known. again, are, siphonal tissue, details but the by the secreted Teredinidae are in siphonal pallets calcareous reflexed and spreads dorsally after metamorphosis, but it does metamorphosis, after reflexed dorsally and spreads Page In developing 2007). fold mantle the nudibranchs, is also development, shell during enclosing larval the it (LaForge & foldshow mantle the extends that back over outside the of Developmental shelled Berthella pleurobranch on the studies shell. have often shell internal and areduced larval the retain sister pleurobranchs, group, the their although shelled adult, no ‘nudibranch’ extant example, a are with there taxa For 1984; 1985, Gosliner 1991; 20). 1989) Tillier (see Chapter Ghiselin 1963; (Morton of groups many typical Gosliner & No shell loss patellogastropods. in is known shells. Velutinidae, the caenogastropods, internal have thin Enteroxenos Entocolax parasites the caenogastropods, in (the slug-like neritimorphs in loss occurred has (e.g.,include some trochids most Vetigastropod it groups in is rare. and pods, examples the gastro through ofExamples scattered adult shell loss are Teredinidae), complete shell loss bivalves in is unknown. afew in bivalvesoccurred (a and few galeommatoideans extreme shell although reduction has and cephalopods, and gastropods only in Adult occurs shell loss conchiferans in s 3.2.15 features. these Volume in chapters possessing the groups with 2dealing in shell chambers) discussed cephalopod ligament; and are (e.g., shell structures taxon-specific Special bivalvehinges o 3.2.14 Objects aretypicallycementedlargely throughperiostracal In heterobranch gastropods, shell reduction and loss shell reduction and is gastropods, heterobranch In A h gglutin t which attach sand grains to the exterior of their exterior of the to their grains sand which attach (Eulimidae) (Lützen 1968). (Lützen (Eulimidae) of slug-like A group ell h er R S eduction h a ell tion S tructures Gena

a nd ), some fissurellids. Shelland L oss , Entoconcha Titiscania ) and, , and , and 81 - - -

Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 xedd hs process, called ‘limacisation’, extended. This ceral masstobelengthened and flattenedthefoottobe els in many soils. Adopting a slug-like body allows the vis- requirements forshellconstructionandthelow calciumlev - terrestrial gastropods mustcontendwithgreaterenergy also expends considerableenergy (Palmer 1992).Shelled the energy tocarrytheshell(Palmer 1992).Shellformation doubling thesizeofNucellalamellosarequiredthreetimes shell sizecanmarkedly increaseshell weight.For example, their energy needs(e.g.,Hausdorf2001). increasein A small of the mollusc, and moving it contributes significantly to shellcomprisesmuchoftheweight into smallspaces. The and enhancingmanoeuvrabilitytheabilitytosqueeze tion inweightandmusculaturehenceenergy savings, advantages ofshellreductionorlossincludeareduc- The 3.2.15.1 dorsal integument differs, being either pedalinoriginor pallial. eventually belostinthe adult,but thederivation ofthenew tissue is pedal or pallial, the shell becomes reduced and may chitons suchasCryptochiton . Whether theshellenclosing bivalves suchasPhlyctaenachlamys andDevonia andafew shell valves bythemantleoccursinsomegaleommatoidean 14 (e.g., (e.g., some fissurellids(e.g.,Scutus), Cypraeidae and Velutinidae (e.g., naticidsor partly orcompletelyabsorbedbyeitherlateralfoldsofthefoot gastropods, theshelliscovered andeventually enclosedand restrial ‘semi-slugs’,andTestacella In some (seeChapter 20). (see Chapter 15), some‘opisthobranchs’(seeChapter 20), ter the rest of theanimal–as in teredinidand clavagellid bivalves shell remainsexternal, but ismuchreducedinsizerelative to taxa,the having minimalornocalcareousmaterial.In some branch gastropods, they arechitinous(Furuhashiet al. 2009a), reduced andeven disappear, but insquidandafew hetero- by tissueandthenreduced. These internalshellsmaybemuch (octopus). mantle adult (gastropods) by or subsumed atmetamorphosis the shed then development early in produced shell, which is still and larval coleoids, adult and shell is lost, the not the gastropods In both shellsome may taxa. present in be arudimentary although squid) or and completely lost some octopods, in octopods, cuttlefish, coleoids (belemnoids, in internalised and reduced been shell has shell reduction or loss nautiloids, external in the have to no been appears there coleoid While cephalopods. (G. Nov. Barker, comm. pers. 2014). 1943) (Fretter onchidiids in vaginulids occurs and shell also 1976). (Thompson larval the which is discarded Discarding 20.67), 20, Figure shell (see enclose larval Chapter the not 82

 slug-like. slug Limax genus the from derived This term, In most casesof shell reduction, the shell is first surrounded the in predominant also Shell shell loss reduction and are Philine, Lamellaria), andvarious shelled‘opisthobranchs’

Consequences and Opportunities ). A similar enclosure of the similar enclosure of the Pleurobranchus). A Akera ) or the mantleencloses the shellasin , is the process of becoming of becoming process the , is 14 involves the - susceptibility to desiccation. to susceptibility increased markedly in it results also taxa intertidal and trial of disadvantages shell loss,- predation-related forfrom terres or, sacoglossans, of many plastids in (see Apart Chapter 20). of zooxanthellae, photosynthetic sequestration the to led has shell reduction few or lossChapter 20). In a taxa, nudibranch duction of slugs defensive (see some mucus terrestrial in as 1998, Ghiselin 1999) or by pro the coloursing (Cimino & ‘opisthobranchs’other warn with where it associated is often defence and nudibranchs many chemical with, in correlated (notum)mantle Shell (see loss to, led has or is Chapter 20). spicules their produced in have acochlidians) and secondarily cavity. mantle the Some shell-less slugs (some nudibranchs by reduction or loss of accompanied is often and surface tory - provide respira can additional of skin area much-increased the swimming, and burrowing ing, both which may facilitate Besides streamlin opportunities. open losing shell can the would beimpossiblewithanexternal shell(seeChapter 17). an innovationcular mantle wall (see Section 3.12.3.8.2), that development ofrapidjetlocomotionusingacontractilemus- pods, shell reduction and loss are thought to be related to the cephalo- Örstan2006).In coleoid terrestrial slugs(Pearce & other advantages have ledtoabouttenindependentoriginsof grow morequicklybecausethey lacked ashell. These and to findshelter(bysqueezingintotiny crevices) andcould showed thatslugsweremoremobileandflexible, betterable Experiments withsemi-slugsandslugsbyHausdorf(2001) organs ofthevisceralmassdescendingintobodycavity. many gastropod lineages. Varix formation has appeared appeared Varix has formation lineages. gastropod many in have ancestors that growth evolved indeterminate from characteristics growth, possible determinate became with aperture throughouttheirlife (Vermeij & Signor 1992). with indeterminategrowth withathin-edged,undifferentiated otherwise modifiedatmaturity, inmarked contrasttothose ous inmany gastropods wheretheapertureisthickened or lar stageintheirlifecycle. This indeterminate growth , whileothersstopgrowing ataparticu- growth continuesthroughtheirentirelife,thisbeingtermed taxa, by way ofmaterialaddedtoitsinner surface. In some edge oftheirshell,andtheshellalsothickens asitgrows Molluscs grow incrementally by adding shell material to the 3.2.16.1 ments for fishery. the measure by adoption of the standardised facilitated been also of coleoid (squid, cephalopods cuttlefish,octopus) has which species on commercial studies exception growth many is the such for molluscs.size as organisms notable soft-bodied One body of measurements accurate itto obtain as is difficult haveMost on growth molluscan studies shell focused on the g 3.2.16 Despite theoretically increasing vulnerability to predation, predation, to vulnerability increasing Despite theoretically The elaborations of the last whorl and apertural margin margin last whorl of apertural the and The elaborations Shell Growth and Its Record Its and Growth Shell rowt h Biology and Evolution of the Mollusca of the Evolution and Biology determinate growth isobvi- - - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, in growth ratesbetweenindividuals canbeconsiderable than othermethods.Somestudies show thatthevariation is amoreaccurate and detailedmeasureofgrowth rate technique &Crisp1984). This gastropods (e.g., Ekaratne ies ofintertidalbivalves (seereferencesabove) andsome form witheachtidalcycle have beenusedmainlyinstud - 2011).Richardson show (Ridgway & and senescence no growth over 400 years bivalvethe Arctica islandica shell of the in increments growth derived from usingSea data Irish chronology the in climate marine a489 year reported (2010) al. 1980; example, al. Butler Jones et 1985). For et (e.g., alesserto extent gastropods in 1976; Lutz Richardson shell havethe extensively been some bivalves in studied and (e.g., lines growth 1976; Lutz Jones 1980). Such in records macroscopic as growth seasonal and lines growth microscopic shell as the in seasonally. is recorded also growth Daily (e.g., scales time short very in occurs tidally, diurnally), but ‘growth in ous, resulting lines’. not only growth This periodic (Savazzi them reassembling and ward, 1996). sides shell moving the pieces, of into out the them breaking whorl of the by area cross-sectional shellof the slit the and width the increases it periodically because gastropods among Siliquaria in occurs also growth Episodic increase. also spurts growth the increases, regularly of varices pair gap each between the because and awhorl, around interval same atabout the formed are taxa Varices formed. most is being in varix apertural the while subsequently and thickened spurt growth the in formed quickly shell are thin and The periostracum varices. between rapid very being varices, intermittent with gastropods in spines). continuous (e.g., be can ribs) (e.g., or discontinuous granules, elements. sculptures it, spiral to These producing pendicular (bivalves)concentric or per (gastropods) sculpture, or axial (collabral), margin growing the to producing parallel be can some sculpture and lines Growth margin. mantle at the which reflect changes intervals elements atregular sculptural Cancellariidae). (e.g., some families in Strombidae, internal Potamididae, externally, thickened mainly usually but are are varices The evolved has feature this ing several in independently lineages. indicat varices, etc.),few Eulimidae, apertural possess also (e.g., a some Rissoidae, Epitoniidae, and Rissoinidae many ‘asiphonate’ certain caenogastropods and cerithioideans, caenogastropod basal near Many ofstylommatophorans. the neogastropods) and well as ans, some ellobioideans as and (notablytropods stromboide tonnoideans, cerithioideans, caenogas- higher many in occurring adult, the in structure Vermeij 2017), varix-like or atleast aterminal varices, with evolution gastropod during (Webster & 40 times more than Microscopic growth lines(microgrowth bands)that continu is not Even shell scale, growth time on a daily growth) episodic as (known bursts in proceeds Growth shell grows, the As bivalves many produce gastropods and (Siliquariidae), which is unique unique is which (Siliquariidae), , individuals of live which, individuals can for - - - - - other elements as outlined below elementsother outlined (see as Section 3.2.18). shell involve analysis of the oxygen and isotopes carbon and saxatilis reversed (relating shell to shape) astudy on Littorina in 1984), Bertness (Kemp & result was this although aperture more slowly higher-spired shells asmaller had with and food grew limited with those while aperture, alarge with developedample food faster grew and low-spired shells littorea Littorina littorinid the shell but shape. rate, in For example, also growth not only winter. supply Food may or not in influence little and mer 1993). sum grow cold in Thus, water typically species (Vermeij temperature increasing with increase to tends cification (Graus 1974), and shell ornamentation elaborate cal Warm increasing to lead conditions growth. also nate determi with taxa slower those in ceases life, and in later more rapid when is usually young Growth individual. and food(temperature, availability, etc.) age of the the and conditions by environmental is modified and Chapter 2 in Section 3.2.19). found insomeunionoideans(e.g., Anthony et al. 2001)(see may complicategrowth ratestudiesusinggrowth lines,as &Crisp1984).Resorptionoftheshell (e.g., Ekaratne alliophiline cor the caecids, vermetids, tube-like including the tropods (see 13gastropods 19) Chapters and afew- gas and modern some fossil in seen enigmatic also are septa, shell, termed of close the interior that off the partitions calcareous Internal i 3.2.17 et al. 2001).et al. for as spaces, example, some oysters in Spondylus and bivalve by foliated shells layers as water-filled separated some 1967). in formed also are formations et al. Septa-like (Knutson of flyinfection parasitic because formed are septa Melongenidae (Vermeij & Raven 2009). snails, some land In Gundlachianorbid limpet doslit septa. not produce and live sponges that in those have and not cemented, along shell mostly are siliquariids, the of group gastropods, unrelated allows much it body. become to longer the but than A similar, shell the in septa of internal The production substratum. the above high extend shell aperture can the and substrata hard removed shell of are the by wear.parts protoconch is lost older the or as the shell is sealed where the conchiferans many in occurs commonly formation septa to by asiphuncleconnected (see process Chapter 17). A similar them between chambers the and more regular being in ing differ cephalopods in those with analogues, are septa pod (Bieler cephalo and some architectonicids 2009). Gastropod Other ways of studying the environmental record in the the in ways record Other environmental of the studying discussed control as hormonal is under Shell growth Septa-like formations are found in the fresh-water found the pla in - are formations Septa-like to cemented shells of most are vermetids The worm-like (Saura 2012). et al. ntern Magilus a l S , some turritellids (Andrews 1974),, some turritellids and ept a (Basch 1959a) (Basch afew in and , individuals supplied with , individuals (Healy (Healy 83 ------Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 results in lower in results temperature in increase an For example, palaeotemperature. and palaeosalinity estimating in useful shell, of are ate the Putative ‘molluscan’ shell ( isotopes change. global climate of unprecedented time this in data tal of palaeoenvironmen sources luscs, have important become (e.g., Jones 1985). fossil derived from often mol data, These eventsand hydrography such productivity and changes in as salinities and palaeotemperatures estimating ous papers Canyon (CD). Diablo meteorite for and sulphur, it air is atmospheric is the standard gen the Water Ocean (or Mean Standard V-SMOW), for while nitro example, oxygen the is Vienna hydrogen and standard For of depletions). because now standards (ordards secondary V-PDBthe PDB). (Vienna have isotopes Other stan other is called standard the Austria, Vienna, was in recalibration the performed that laboratory Since the specimen. original the against anew reference calibrated sample be to required which studies calibration were depleted during standard the USA. Samples South of Carolina, Formation, Dee Pee the americana fossil, Belemnitella cephalopod Cretaceous calibrate C calibrate to used The standard compared. whichto sample are results different to elements.taxa different of affinities including considered, the be to factors need many although (see below), factors such temperature as environmental and fossils from conditions about of the depositioninformation obtain to elements used be can trace various of and calcium relative inclusions abundance accidental (Jones 1985). The or by matrix, organic the into incorporation byplanes, their lattice or between surface, crystal on the absorption cium, where replace they cal lattice crystal the into assimilation used. commonly of Isotopes nitrogen, hydrogen, also tion type. are sulphur and vegeta and of- productivity, burial, estimates carbon organic 18 ( stable of ratios of isotopes the carbon 2013).Dehairs The & Ivany 2008; 2012; &Gillikin Gillikin (McConnaughey 9) 3and or oxygenby using carbon (see isotopes Chapters was down laid shell when material existed conditions the that environmental about provide the also shell data itself can the of 3), properties chemical but the (see rate growth Chapter determining in have increments useful been growth often 2010; et al. Stott 2011). Richardson Ridgway & Traditionally 2010; al. biological and habitats, (Butler et processes ture, - on tempera stamp’ providing data date and ‘time historical shell provides a carbonate calcium of formation the tionary accre The taxa. molluscan Many isotopic feature studies s 3.2.18 84 and to reconstruct the carbonate content of Cambrian seas. seas. content of Cambrian carbonate the reconstruct to and 2012) al. explosion’ ‘Cambrian the during et (Kouchinsky events of sequence biomineralisation the document to used 13 O relative to C/ Studies ofStudies shell molluscan have isotopes numer to led Each isotopic comparison requires a calibrated standard standard acalibrated requires isotopicEach comparison shells by in incorporated Various elements also are trace 12 C) and oxygenC) and ( 13 t ab was a mollusc – the Pee Dee Belemnite (PDB), Belemnite was a mollusc Pee Dee – the a le 16 I 18 O, while the O, the while O/ sotopes 16 O ratios and salinity tends to increase increase to tends salinity and O ratios 18 O/

16 a O), carbon calcium found the in nd T 13 C/ r a 12 ce C relationship provides E 13 le C) have been also m ents

in S h ells , from , from ------Holocene snails. Although C Holocene Although snails. early and glacial for late of both carbon source main the as shell carbon isotopes ( isotopes shell carbon (2013) al. have example, analysed Colonese et 2013). For al. palaeovegetation proxies (Yanes important as serve et food preferences thereby and and rainfall) and temperature physical conditions (mainly determining in important are 2010; 2010). Demopoulos et al. isotopes habitats In terrestrial al. Becker et Soto 2008; 2009; al. 1997;Giere et Naraoka preferences chemosynthetic nutrition (e.g., and Windoffer & from Greece and were and able C identify to Greece from figulina line studies coupled studies stable ( with analyses isotope line et al. growth 2009). Alaska, Islands, In theHallmann Aleutian (e.g., increments study of growth the with try Jones 1983a; drought. to adapted communities woody shrub Mediterranean extant in living snails to shells werevalues the similar from and and (e.g., communities seep white Calyptogena clam giant the well Western of studies the as Pacific Pool. Warm of events Niño El frequency and conditions, different as under strength for use in factors assessing complicate variation their yield relatively (e.g., series time short et al. 2005b). Carré These application they as their in somewhat limited 2009). They are Black 2006; et al. 2005b; Lazareth 2005a, events et al. (Carré ENSO reconstructing 2009), in and et al. (Radermacher ture aquacul in used taxa in 2017), traits history life reconstructing et al. Fiebig Gilbert 2009; 2005; Schöne & (Chauvaud et al. reconstruction have for useful data palaeoclimatic series been available. Molluscan isotopic sclerochronological and time skeletons coral locations are where and only altered periods for they may climate provide of tropical past robust estimates skeletons, coral diagenesis to more resistant than generally 2011). al. conditions (Welsh climate shells are Since the et Oscillation) mean variability, Southern Niño and ENSO (El and yield to tial reliable of seasonality changes past in records were studies conducted. where no pre-impact systems drainage in management policies assessed could be of how water it impact demonstrated the because interest ular bivalves- Colorado the River in is of This study estuary. partic have of two rates of species veneridAmerica growth changed Colorado waters management of of the the and River North in isotopic with howcombined document to studies diversion (2003) analysis al. increment growth used Schönescale, et lowest the with seasons the to time amore recent tides. On not correspond did and autumn early through spring early the from were cockles collected the that ablealso determine to 2012). today (Koike found et al. cockles there was The study larger, were (170–400 years past and BP) older the the in than faster, grew nuttallii have Clinocardium cockle shown the that living taxa provides isotopic taxa living evidence ( shells, besides tissue of the using and, isotopes studied been have taxa also and communities molluscan Chemosynthetic tiful water and high CO high water and tiful plen temperature, and sunlight moderate with habitats with Many archaeology studies have studies Many archaeology - shell chemis combined Dense monospecific populations monospecific of Dense bivalvescoldin Shells fossil of and living Tridacna gigas Bathymodiolus mussels) because of significance are Biology and Evolution of the Mollusca of the Evolution and Biology 13 Helix Helix Pleistocene living C) from and 2 concentrations (200 ppm), the the (200 ppm), concentrations 3 plants are typically associated associated typically are plants 13 C and C and have poten the 15 N) of dietary of dietary N) 18 3 vegetation vegetation O and O and 13 13 C) C - - -

Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 resorb the internal shell whorls. internal the resorb (e.g., 1955a). Morton never Stylommatophorans completely whorls, resorption ellobiids while have internal partial their have all of complete resorption Proserpinidae Ceresidae, and whorlsnal (Solem 1983); Helicinidae, taxa neritimorph the inter resorb also taxa Some terrestrial shell material. internal ofSpecies Conus (Vermeij possessing elongate these 1977b). apertures all with Mnestia cephalaspidean the heterobranchs sensory cells which, sometimes, have which, cells sometimes, sensory evolved sense into by muscleated andcontains fibres. with nerves supplied It is overlyingon a basement membrane connective tissue perme is asingle layer (Figure 3.23) cells of The epidermis external foot of locomotion the sole tenacity.epidermis and facilitates the osmoregulation, while and input, sensory tion, respiration, - including protec functions many performs and body entire world. external It covers the with the interacts and interfaces and (or animal The epidermis or the integument) protects skin t 3.3.1 (see shape more compact body Chapters 1, 5, 8). and developmentthe and flexure) tubes in life blind enabling of a aU-shape (ano-pedal bent into gut the is and extended, axis dorsoventral the In others, anus. aposterior end and anterior elongate,some molluscs Some authors. primitive are an with collectively, ‘soft quaintly, by the rather parts’ and called The body of viscera – amollusc foot, and consists head, of the 3.3 such as examples other include and afew timorphs, neogastropods notably most gastropods, neri of only afewteristic marine 2001).et al. 1993; Downing Anthony some (Downing & in tion recorded shell- with reduc shell to growth rate ata similar shell occurs Section 3.2.10). fresh-water mussels of the resorption In some it as grows wall (see parietal the across spreads aperture the of lip elements remove to inner when the sculptural sary these - is neces resorption as or knobs, spines with such those as taxa sculptured highly in necessary shell particularly grows. This is the as side aperture of adjacent inner the the to surface rior exte remove the from gastropods coiled some shell material down. laid it Most been has after shell material some internal capable shelled molluscsProbably of are all resorbing at least s 3.2.19 1992; et al. 1992). Callender of fluidPowell signatures taphonomic venting (Callender & additional ofpost-mortem shells accumulations may contain al. 1992), while et (Rio isotopic and fingerprints cal includes record chemi 1980). &Lutz This (Rhoads tats habi unique these in fluctuations of environmental record adetailed preserves of mode growth accretionary their Shell, Body, and Muscles and Body, Shell, - shell of is acharac the parts internal ofResorption the

THE BODY Bullia h h e E ell pider , R Conus can remove up to around a quarter of the of the remove can aquarter up around to esorption m is , Conorbis , and , and Olivella and ellobiids, ellobiids, and , and in the the in , and ------gastropods and cephalopods. and gastropods However, layer cuticular a true region mouth is found the of in &Rieger 1976; Rieger 1984). acuticle as to (see Rieger wrongly referred is sometimes placemucoid and in secretions layer ofcomposed amicrovillous which retaining assists in is surface external Their or glandular. non-ciliated, ciliated, be can and shape in columnar typically are cells Epidermal of (see pinocytosis Chapter 5). by way (DOM) dissolved matter uptake organic also can and (see damage Chapter 2) after heal can The epidermis organs. and Scaphopoda, but is absent in Monoplacophora, Gastropoda, but Monoplacophora, is absent Scaphopoda, in Gastropoda, and Polyplacophora, the is present in Solenogastres, Caudofoveata, is probably rootlet plesiomorphic it as This short rootlet. ciliary molluscs. double, in If it consists ofstructure a long short and bycell body. a‘foot’ or basal The root may asingle be or adouble the ‘root’ in which the as is anchored cell the which into passes axoneme, the of microtubules, aring has cilium each Internally involved and or motile moving in water, mucus, locomotion. or in sensory, and may immobile be that cilia bear often cells Epidermal 3.3.1.1 also importantindispersingmucusover thebodysurface. sparser onthegeneralbodysurface andoutermantle,they are flow, particle sorting and rejection, and locomotion. Although labial palpsofbivalves wherethey assistinmaintainingwater gastropods, themouth,gills,andfootofmostmolluscs, cavity ofaquatic snailsandthepneumostomeof‘pulmonate’ 2012). Ciliatedcellsareabundant inareassuchasthemantle are alsofoundintheepidermisofsomeslugs(Wondrak 1969, 1968; al.2000).Non-glandularpigmentcells Yamaguchi et buds fromtheirsurface duringapocrinesecretion(Wondrak (see Chapter 17). rapidly to changealopods colourdisplays forand camouflage pigment (chromatophores) cells epidermal which enable- ceph of somemantle shell-less ‘opisthobranchs’, specialised and found defence, the in glands predator notably repugnatorial involved also are cells anti- with epidermal specialised (see light receptors and Chapter 7), chemoreceptors ceptors, asimple derived from epithelium. are cephalopods of beaks jaws the the and contrast, of gastropods many In or radula. operculum, an byssus produce to proteins threads, sue quinone-tanned complex form to may secrete that glands assist locomotion. with and help surface cells body the cleanse desiccation. epithelial against With mucus, ciliated protecting it assists in gastropods terrestrial locomotion, in in and dermis Section 3.3.2). Mucus plays epi often the arole protecting in of which is mucus (see most important the cells, gland dermal by epi produced also are Various secretions and chemicals operculum. an gastropods, many in of ashellsecretion and, epithelium. mantle regions body, of the epidermal outer oneral the but smaller Microvilli are usually well-developed usually exposed are gen the in Microvilli much interest. attracted has The histology epidermis of the In some terrestrial slugs, the epidermal cells produce small terrestrialslugs,theepidermalcellsproducesmall In some such mechanore organs sense as epidermal to In addition folded may- connective become tis the into The epidermis its by protective the function may perform The epidermis Cilia 85 - - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 up toover 20%ofthewetweightamollusc. The inorganic compriselessthan1%to weight andinorganic salts.It may plus aprotein-polysaccharide complex ofhighmolecular tions. Mucus is a viscous colloidal solution of mostly water gland cellswhichcover theoutersurfaces withmucoid secre- epitheliumtypicallycontainsmucus-secreting The molluscan 3.3.2 1982; 1995b). et al. Beninger Ehlers Davis1978; Matera & (Ehlers & artefacts fixation be 1982; 1985a, 1987b), Haszprunar now thought but to are they (e.g., function aproof of be to this presence Davis Matera & their and chemoreceptive considered as been structures also even it, and forthrough applying They have byssus threads. for locomotory as either moving water or moving interpreted have variously been They taxa. molluscs other in and cilia (1985a) Haszprunar dia. of paddle reviewed occurrence the - osphra and gills such the as molluscs on structures larval and 2001b, 2001c; 2009). et al. Lundin 1999, Schander 2001a, (Lundin & resent rootlet asplit vertical autobranch bivalves probably but these cephalopods, rep and however, There are, Bivalvia, in rootlets Cephalopoda. and twin 1 Mollusca Invertebrates. of F. J., A. Anatomy Kohn, W. Microscopic Harrison & . Function and Form (excludingskin K.,cephalopods), Molluscan pp. 11–35, from Simkiss, R., M. modified Clarke, not shown. and R. E. in Redrawn Trueman & FIGURE 3.23 86 Flattened ‘paddle cilia’ have been reported from many adult many from ‘paddle cilia’ haveFlattened reported been M ucus

Three basic types of epithelial cells (epidermal, ciliated, and mucous) found in molluscan epidermis. Sensory cells are are cells Sensory mucous) epidermis. and molluscan found in ciliated, (epidermal, cells of epithelial basic types Three endoplasmic desmosome endoplasmic reticulum smooth The Mollusca reticulum apparatus junc septate nucleus rough Golg microvilli tion i , Vol. 11, New York, Press, Academic 1988 Voltzow,pp. 111–252, and Prosobranchia, J., in Gastropoda: epidermal cell cilial root cilia ciliated cell - of gland cells (Denny 1983; (Denny cells of gland 1998; Hawkins Davies & Smith by must avariety produced be mucus ofties turn which the in physical different proper necessitates biochemical often and (see of functions range different below) The appreciated. slugs, is rarely of terrestrial slime legendary the particular Cook 1987). & combine toproduceaspecifictypeofmucus(Shirbhate vated, secretions from several different types ofgland cell may are presumablyderived fromdifferent glandcellsbeingacti- While different kindsofmucusproduced,notablybythefoot, gland cellsthatproducetheminmolluscs(seeSection 3.3.3). phyla. other molluscs in different and in edly composition and mark polymers of differ the The structure complexesentangled gels (Smith slippery form to 2010). large make polymers that containing secretions generally 1978; Diet al.2012). &Clamp rides orproteoglycans)andglycoproteins(Reid glycosaminoglycans (GAGs; oftencalledmucopolysaccha- polysaccharide complexes have usuallybeenrecognised – the & Walker 1980). Two groupsofprotein- mucus (Grenon salts compriseabout3%ofthewetweightPatella pedal The variety and complexity and of mucus, in molluscan variety and The The wide range of secretions is reflected in the diversity of ‘mucus’, called mucoid the all gels are While are they , Vol. 5, Wiley-Liss, New York, 1994. mucous cell Biology and Evolution of the Mollusca of the Evolution and Biology basal lamina mitochondrion intercellular pigment secretor lysosome granule vacuole space y - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, ens when dry and prevents aestivation. and loss moisture during whenens dry - hard The epiphragm whole the across sheet aperture. like operculum- an or forms surface ahard to aperture the seals alayer epiphragm, of an either mucus that secrete snails ran 1998 Hawkins Davies & for review). Some stylommatopho (see limpets and snails shown some been intertidal in has as help stress, heat also reduce can substratum foot the from of layer a thick secretion the of separates mucus that The or overhangingdesiccation. reduce to vertical rocks to attach mucus use to can snails land and such littorinids as snails example, intertidal For taxa. terrestrial shoreupper and some in seen as stiffness, and its strength increase markedly gland(s). by hypobranchial quantities, the large layers in epithelial often by general the and, is secreted cavities mantle waste of clean to the most molluscs, where it moving in ticles. (aided It is critical by also cilia) binding and of food mucus par trap or strings sheets some gastropods, in and, mouth the to palps labial the via gills of the food from In autobranch bivalves, for transportation the mucus is crucial suspension-feeders. in importance Chapter 5) is of and critical Connor 1986). &Quinn1984; and diatomsonthesubstratum(Connor foot secretionsalsotrapandstimulatethegrowth ofalgae Lithophaginae (Morton & Scott1980).In patellogastropods, spondyloideum (Yonge 1967),andthecoral-boringmytilid 20), the coral living scallop nudibranchs (Chapter mucus caninhibitthedischarge ofnematocysts asinsome those taxa associated with cnidarians, Hawkins 1998). In to protectfrompollutants,andeven extreme cold(Davies & the surface tooslipperytograsp.Mucushasalsobeenshown production ofcopiousgelatinoussecretions,orbymaking and 20), the distasteful or toxic compounds (see Chapters 9 and canalsoprotectagainst predatorsbytheadditionof 1992) antimicrobial properties(e.g.,Otsuka-Fuchinoet al. ionic regulation (Hillman 1969). Some molluscan mucus has al.1986)andpossiblyfacilitating (Grimm-Jørgensen et surrounding environment, actingasabarriertodiffusion insulates themolluscfrom motion andadhesion.It also reproduction,andloco- is vitalinfeeding(seeChapter 5), restrial molluscs are overviewed by Denny (1983). Mucus by Davies andHawkins (1998),anditsmany rolesinter of mucusinmarinemolluscsweresummarisedareview many functions 3.3.2.1). The in locomotion(seeSection property enables its use when the stress is released. This becomes aliquid,but returnstoaneffectively solidstate stance isaviscoelasticsolidwhich,whenstressincreases, adhesivelubricant, anadhesive, sub- oreven arope. This its infancy. in mucus is still 2010) (see Chapter 10), also much work of the on molluscan applications (e.g., practical potential of their 2006, Smith of some adhesive gels, structure biochemical largely because 2010) (see the to paid being Despite attention Section 3.3.3). Once secreted, subsequent dehydration mucus of secreted, can the Once Mucus plays (see gut molluscan role the in avital Mucus isdynamicandversatile, functioningasaslippery Pedum - - - tion (Wolcott 1973). avoid to barrier desicca- epiphragm-like an secrete also pets gel lim (Pawlicki et al.littorinid 2004). Some intertidal high have in shownwhen been extracted, cause stiffening to also which, proteins three comprises epiphragm up the making 1983). material organic the (Barnhart Aboutpiration half 1961)Campion isallow sufficiently and porousto some- res some (e.g., of calcium and mucoprotein consists mainly It 1989). mucus in slow to is bound and dispersionpredators (Denny 1988).(Packard (see Coleoid ink Chapter 17) deter to is used mucus complex consisting of a protein-polysaccharide secrete that cells is supplied gland with skin lopods. Their (seecapture Chapter 16). filaments feeding (captaculae) are employed which in food adhesive the of by club-shaped mucus the heads the produced is interest particular Of scaphopods. in foot mantle the and (seerole feeding in Chapter 5). its and by gills mucus the produced the with ies concerned out by mucus bivalves in roles carried varied most with - stud Hawkins 1998forreferences). some stylommatophoransandaloliginidsquid(seeDavies & have alsobeenreportedfromthemucusof (see Chapter 2) being alarge partoftheirenergy budget (Horn1986).Lectins very few concernedwith chitonmucus,despiteitsproduction (Höglund & Rahemtulla1977). This latter reportisoneofthe bivalves andgastropods, andtwo typeswerefoundinachiton 3.3.2.1).Sulphated AMPS have beenfoundin (see Section tates cross-linkage(Smith2002)andaffinitytocertainmetals charge facili- Schauer1972). The negative lium (Faillard & readilyhydrated orseparatedfromtheepithe- they arenot component of the mucus and are good lubricants because areanimportant sourced fromotherglandcells. The AMPS gels, but onlyafteraddingspecificproteinsand/ormetalions mucopolysaccharides (AMPS)oftenformsticky adhesive mucopolysaccharides and can be neutral or acidic. Acidic (Denny 1983). These polysaccharidesareusuallycalled also composed of different protein-polysaccharide complexes although structurallyandbiochemicallydiverse, mucusis molluscs, polysaccharide complexes thattangletogether. In slime. their well slugs, being for known latter the including terrestrial 3.3.2.1) (see Section of gastropods epithelia pedal the in 1998; 2010 Smith for case reviews). the particularly This is (see cells of Hawkins gland Davies & kinds different from secretions of mucin-like amixture from is formed secretion volume. in Usually a mucous dramatically increase water and absorb which membrane, immediately by athin rounded packages sur in cells secretory mucus from isthe released molluscs, slugs afew and marine butterrestrial in stood, The mechanisms in marine molluscs are not well under not well molluscs are marine in The mechanisms There are few details available few about are - mucus cepha details in There by mucus secreted the regarding known are Few details (1990)Prezant evolution the discussed and many of the Vertebrate mucinsareformedfromlarge protein- 87 - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 but becomes very sticky after several acouple to seconds after sticky very but becomes slime, aviscous as secreted mucus is initially dorsal The 1986). &Deyrup-Olsen weightbody slug of the (Martin over be can secretion 5 total 2002), the Port and & foot, defensive is probably the and mainly (e.g., Mair Arion In patellids. and lottiids both (Smith 1992; 1993). Worms et al. investigated Those include change can gel properties glue, pedal and the suggesting that suction adhesive between using an gel,tum alternate but can those onlyfromintertidalandterrestrialhabitats. major groupsofgastropods beinginvestigated indetailand ited selectionofgastropod diversity withonlythreeofthefive mainly onareview bySmith(2010). a They reflect very lim- main taxainvestigated are describedbriefly below, based tigated indetailthatgeneralisationsarepremature. The three sumably reflectsphylogeny, but sofew taxahave beeninves - 2012). (Byern et al. polysaccharides non-adhesive epithelium of Nautilus the mucopolysaccharides. in cells Gland of neutral mainly amucoid produce adhesive that glue composed papillae 88 is renowned for its quantity and stickiness. In is renowned stickiness. for and its quantity Some slug(Werneke 2007). stylommatophoran et al. mucus ions involved metal substantial cross-linkages in contains it and also proteins, consisting of small mainly ponents Arion subfuscus aspersum Pawlicki 2004). et al. 2002; &Morin (Smith carbohydrates the by cross-linking gel presumably in stiffening, gel implicated whichtory are not found proteins locomo glue short the has the in and rides, large, complex are carbohydrates polysaccha- The protein. of but carbohydrate, amount much same less about the has for used locomotion that while amounts, approximately equal in carbohydrate and adhesive protein mucus contains The 1972b). (Bingham sole foot edgesaperture of of the the the to is done by foot movements gel the transfer from that This substratum. the to wetting,to shell glue they aperture the when not subjected 2002). shore upper littorinids, many Like adhesive and locomotory gels both (Smith &produces Morin rata (Pawlickiecules 2004). et al. gel the mol may cross-link protein 2002). stiffening This gel Morin 1999; Walker 1980; Smith & (Grenon & et al. Smith complexes large very of the carbohydrate and of protein molecules of composed instead protein component is mainly non-water the molluscs of that those other gels in from differ clamping using locomotion last two suction. in in and These mucus used the absent from aprotein contains This glue-gel relatively contains (Smith 1999).that carbohydrate et al. little bygates way of non-covalent adhesive an form to bonds gel aggre large into relatively cross-link that tains proteins short - substra strongly the to adhere Patellogastropod limpets Some ofthebiochemicaldiversity ingastropod mucuspre- Nautilus Cornu Cornu snail of the two stylommatophorans, The mucus irro Littoraria periwinkle’ ‘marsh caenogastropod The (Littorinidae) (as Littorina (as (Littorinidae) , the mucus is extruded from both the dorsal surface surface dorsal the both from mucus is, the extruded Helix aspersa Helix (as tentacles lack suckers or hooks and instead have tentacles lack instead suckers and or hooks (Pawlicki et al. 2004) has non-water has 2004) com (Pawlicki et al. in most slug literature), in the and Lottia in much in literature) of the , the pedal mucus con pedal , the produce acidic muco Ariolimax % of the and and ------the pseudofaeces inbivalves islosttotheanimal. being assimilatedduringfeeding,althoughthemucusbinding suspension-feeding molluscs,withmuchofthemucusutilised binds faecal materialislost.Mucusplaysanimportantrolein much ofthemucusgeneratedingutisreutilised,somethat 70% tion, involves aconsiderablecosttotheanimal,utilisingup 2007;et al. 2013). Smith copper) and magnesium, (Werneke iron, zinc, manganese, (calcium, slugs metals in is rich by someproduced terrestrial (Pawlicki et al.stiffening 2004). The defensive mucus sticky gel trigger that proteins short additional glue contains the glycoprotein complexes butcontain proteins, smaller and foot of the part by foot dorsal the soleproduced the and et al. 1983) (see Section 3.3.2.1). mucous secretions the Both slugs mucusviscous these locomotion in use (Deyrup-Olsen and slippery the with contrasts This markedly of minutes. 15 the chemicalcompositionof the pedalmucusofchitonsand WalkerMarsh 1978; Grenon & 1981). Little is known about patellid limpets ranging from 1.03 to 5.18 kg/cm mucus can be very efficient, with theforce required to remove adhesive propertiesofthe with low mucoussecretion. The properties ofthepedalmucus.Increasedtenacityisassociated the footisacombinationofareaattachmentand the poweror climbclamponsteepsurfaces. of The adhesive foot enablestheanimaltoeffectively clamptothesubstratum increepingmolluscs,the muscular locomotion.In addition, (see bysometimes predators Chapter 9). followedof be mucus often which can by or conspecifics moves, it adhesive. and/or leavesanchor animal the As atrail an as act also it and propulsive can which the in beat, cilia provides liquid the several has roles. substratum It the and 2012). et al. of foot mucusShirtcliffe the between This layer (10–20 thin a with by them coating surfaces many to adhere to pods mucus enable of gastro pedal properties remarkable The roleluscs, the of but we here mucus locomotion. in examine above, mol noted As in mucus for is used purposes many 3.3.2.1 2002).Holmes et al. (e.g., organisms marine ofsettlement various 1986; Connor composition and film microbial may crawling affect and been or chitons have where gastropods for on surfaces some time of nitrogen by 29 remineralisation of was rate found the accelerate to sediment mucus the pod in gastro remineralisation, matter organic study of sedimentary recent a & Hawkins1998). In (Davies significant could be but unknown, ecosystems is virtually role shallow marine in

Particulate organic material. organic Particulate The contribution of contribution mucus molluscan POM to The Mucus production,andparticularlythatinvolved inlocomo- Pedal mucusisextremely importantinbothcilialand persist trails slime by bacteria, degraded readily Although of all consumed energy (Davies & Hawkins 1998). While and Adhesion in Gastropods Adhesion and in Locomotion The Role of Mucus Pedal µ m) layer of 1980a, mucus (Denny 1980b, 1981; Biology and Evolution of the Mollusca of the Evolution and Biology (Hannides & Aller 2016). Aller % (Hannides & 2 (Branch & (Branch & 15 and its and - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, 2 adhesive the gel of form and the proteins, contains small some relatively and of carbohydrates molecules large in rich 95 more than being yet despite strong adhesion wet to produce it can surfaces, 2004), and al. (Pawlicki et proteins of and polysaccharides fluid foot rest of mucus. the the due this to wave sole of is the the that move part can to That respect with 1980a). (Denny direction desired moving the in facilitating aratchet-like material as mucus in acting results rapid and fluid tofrom is gel transition states very wave.of the This edge back its to more solid gel trailing transforms atthe phase then The mucus fluid. mucus causing become to the area that wavepedal (see Section 3.10.3) in pressure reduced in results 3.31). generation of the adhesive and thick (see Figure The sole of the where it is parts stationary wave the beneath than much more fluid thus the not adhesive)moving (and beneath sole mucus foot, fluidity. changes the of in agastropod It is good informationaboutgastropods (e.g., Trueman 1983). nothing aboutthatofmonoplacophorans,but thereissome produced mucus mucus produced columbianus slug Ariolimax terrestrial the tion. However, foot on of the sole mucocyte a single of kind for locomo required properties viscoelastic necessary the mucus produce to with required of be may mucins usually littorea Littorina (Grenon & Walker 1978), but only five the caenogastropod in logastropod patel the from have of mucocyte reported types been Nine gastropods. of marine taxa different in differed of mucocyte those resultingfromadjustmentstodifferences inhabits. taxa sothetaxon-specificcomponentscanbeseparatedfrom separate histories.It will beofinteresttotestawiderrange also a significant evolutionary component, given theirlong in thehabitsandhabitatsofthesetaxa,but thereispresumably tural modifications,have beenin part derived from variations between 6%and27. These differences, togetherwithstruc- al. (2004)theoptimalproteincomponentwas Pawlicki et stylommatophoranslugandsnailinvestigatedLottia. In a by and carbohydrate, with two of the proteins being absent from adhesive formhasapproximately thesameamountsofprotein and adhesive gels, while in the caenogastropod six timesmoreproteinthancarbohydrate inboththetrail example, inthepatellogastropod Lottia,thereisabout For nificant differences in gastropods from different major groups. of few specieshave beenexamined indetail,theremaybesig- (Werneke 2007). et al. cross-linking by apparently catalysing the 2006), (Smithof 2002, metals involvement the with cross-linked gel the The polymers are in gel on act the to glue. form to for proteins the necessary are which copper and including iron, zinc, metals transition are important 2004). al. Also gelthe it stiffen to (Pawlicki et component polymers in glueprobably of and the cross-link essential an thus are 2002). proteins Morin These Smith & % Pedal mucus gel is up adilute ofPedal made acomplex mixture wave pedal (see amuscular As below) moves the across Davies (1998) Hawkins and of number types the that noted While theformationandcompositionofmucoussecretions –3 more protein than the dilute gel (Smith et al. 1999; gel dilute (Smith the et al. than % more protein Patella vulgata Patella (hrht &Cook 1987). Multiple types (Shirbhate % water. composed mucus Trail is mainly Lottia testudinalis testudinalis Lottia from six and Littorina the - -

probable source oftheadhesive gel(Smith 2010). Walker 1978, 1980). The subepithelial glandsof the soleare magnesium and calcium produced in the secretions (Grenon & proteins, andsulphatednon-sulphated sugars with some 3.3.2.1), acidic orneutralmucopolysaccharides (seeSection Several1978) (Figure 3.24). different gland cells produce either in thesole,andsomeofthoseare subepithelial(Grenon & Walker in thefootofEuropeanlimpetPatella vulgata,sixarefound reviewed bySmith(2010).Oftheninekindsofglandcellsfound mainly basedoninformationfromgastropod studies. cytes associatedwiththegills.Consequently, thetext below is those onbivalves beingmainlyconcernedwiththemuco- 2010). Mostdetailedstudieshave focused ongastropods, with ucts ofmorethanonetypeglandcellmixed together(Smith contribute to mucusproductionandmostgelsaretheprod- Studies aredifficultbecauseseveral typesofglandularcells specific glandcellsarelimitedtoasmallnumberofspecies. different materials,but detailsabouttheproductssecretedby thelia containvarious kindsofsecretoryglandsthatproduce diversity ofglandcellsthat producethem.Mostmolluscanepi- oles byway ofexocytosis, andthecellcontinuestofunction. tions arereleasedfromthecellsmall cytoplasmic vacu- cell membranerupturing,destroying thecell.Merocrinesecre- secretions areformedinthecellcytoplasm andreleasedbythe merocrine dependingontheirmethodofsecretion.Holocrine the body).Glandcellscanalsobecategorised asholocrineand crine glandswhosesecretionsaresuppliedtotheinteriorof rior ofthebodyarecalledexocrine glands(asopposedtoendo- do occur. The gland cellsthatsecrete substancesontotheexte- cells areusuallyunicellular, but multicellularepithelialglands Veronicella, andSiphonaria(Smith2010). The epithelial gland for example, the pedal epithelium of the gastropods clusters, andinthelattercase,mayhave acommonductasin, subepithelial (orextraepithelial ) cellsmaybeunicellularorin extends throughtheepithelial cellstoreachthesurface. These epithelium (intraepithelial ) orsunkbeneathitwithaductthat Gland cellsassociatedwiththeepitheliumcanbelodgedin e 3.3.3 scraping the rock with its radula (see its rock with radula the scraping Chapter 9). 1983). by limpet the home deepened depressions be These can &Dwyer on which rest they (e.g.,rock surfaces Lindberg on the scars produce can edges of limpets patellogastropod 1992). 1991, (Smith active suction when and is used are they offor time, aperiod when adhesion is used immobile glue-like atleast, limpets in 1974a).ity they have (Miller when stationary because, This is foot of the 2012). (Wondrak margin ‘protein glands’ anterior the on the from added be to appear mucus glue-like the form to generally, necessary proteins the 1981), slugs and snails more stylommatophoran in although, Gosline (Denny & change its properties viscoelastic can that h diversity ofpedalglands insomegastropods was The The diversity oftypesmucoidsecretionsisrelatedtothe AMPS (and carbonic anhydrase) from the foot and mantle foot (and mantle anhydrase) the and from carbonic AMPS - tenac of have crawling, the When gastropods about athird pit h eli a l

a nd S u b epit h eli a l G l a nd C ells Littorina, 89 Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 mucosubstances. the foot.Dorsally, threetypesofgland cellproducevarious restricted to a transverse band halfway down the sole of that producescarboxylated mucopolysaccharidethatis alsoanothercelltypesecrete AMPS andprotein. There is tein, whilethefootsolehas two typesofglandcellthat pedal glandproducesneutral andweaklyacidicmucopro- Bithynia tentaculata,thesinglecelltypeofanterior desiccation. reducing in aid that facesecretions foot ofproducing five the has types cell sur mucopolysaccharide. asulphated The dorsal and neutral a produce where two types cell furrow except amedian in sole the foot cells species, of gland the lacks terrestrial In this mucopolysaccharide. sulphated and protein, mucoprotein, Pomatias elegans littorinoidean terrestrial of the a mucoprotein. surface ofthefootsecreteasulphatedmucopolysaccharideand mucopolysaccharide andamucoprotein.Glandsonthedorsal on thesoleoffootproducesulphatedandcarboxylated typesofsubepithelialglandcells polysaccharides. The three different neutral mucoprotein, and one also has neutral muco- groove ontheanterioredgeoffoot.Eachtypesecretesa comprise muchoftheanteriorpedalglandthatopensintoa &Cook1987). Two types cells, allsubepithelial(Shirbhate intertidal footofthe pod snailsfrommarkedly different habitats. The of thepedalandopercularglandcellsthreecaenogastro - Wiley-Liss, New York, 1994. 1 Mollusca Invertebrates. of J.,A. Anatomy Microscopic pp. 111–252, Prosobranchia, Gastropoda: F. in W. Kohn, Harrison & from Voltzow, modified and foot sole. Redrawn gastropod J., FIGURE 3.24 90 n thefresh-water truncatelloideancaenogastropod In gland pedal anterior up the make types cell gland Three Shirbhate andCook(1987)examined thehistochemistry Littorina littorea hasfive typesofmucus-secreting

Epithelial and subepithelial gland cells in a marine amarine in cells gland subepithelial and Epithelial cilia sole muscle fibres dorsoventral subepidermal gland cell membrane basement mucocyte epithelial cell epithelial ciliated columnar and produce produce and o. 5, , Vol. - nel cellsdependson­ for mucussecretionandbody cleansing. The activity ofchan- levels following hyperhydration and,­ cells assistinrestoringthevolume ofbodyfluidtonormal channel &Martin1982). The Wilbur 1977;Deyrup-Olsen ing haemocyanin, topassthroughthecellwalls (Simkiss & tated bylarge poresthatallow thebigmolecules,includ- with permeability greater than normal cells – a function facili- (see Figure 3.25). They achieve thisbyhaving cellmembranes and macromoleculestobepasseddirectlytheenvironment in regulating thebodyfluidbyallowing water, large particles, These cellshave(see Chapter 6). acentralchanneland assist 1984), thus differing from pore cells exterior (Luchtel et al. stylommatophoran slugs and snails where they open to the specialised mmlong) the large moleculesarereleasedvialarge (~0.5 (Burton 1965;Deyrup-Olsen & Martin1982). This water and ucts derived directlyby way ofultrafiltrationfromtheblood from glandcells,large proteinmolecules,and watery prod- ran snailsandslugsare a combinationof mucous secretion the skin. Thus thesecretionsofskinstylommatopho- high molecularweightproteinstoolarge todiffuse through alsocontains clear watery fluidcontaininglittlemucus.It from densemucusproducedbyvesicular mucouscellsto adaptations. structural physiological, including body various the and behavioural, havenates developed prevent to mechanisms water loss via faeces) and (urine ucts (see eupulmo Terrestrial Chapter 6). locomotion (mucus),- waste prod when discharging also and evaporation skin, the via through occurs water loss. This challenge is preventing main butfresh-water their snails, slugs and snails suffer osmotic lessTerrestrial than stress 3.3.4 nates’, (see Chapter 20). trimusculids and notably siphonariids ‘pulmo including marine severalbranchs and nudibranchs slug-likethe velutinids (see 19) 9and Chapters hetero and including afewsome gastropods notably caenogastropods, some burrowing andboringbivalves (seeChapter 15). Specialised mantleglandsarefoundinthepedalaperturesof ylate groups abundant in the acidic material (Park et al. 2012). the pedalmucouscellscontainedmainly AMPS withcarbox- venerid,phate andcarboxylategroups.In another Gomphina, gland cellscontainingacidglycosaminoglycansrichinsul- A study ofthevenerid Mercenaria (Eble2001)reportedpedal al. 2012). secretory cells reported in otherbivalves (Lee et which areallunicellularandmerocrine,beingtypicalofmost cells were found in the foot of the arcid the mantleedgeandfootofbivalves. Three typesofsecretory 16

 epinephrine (Luchtel et al. 1994). et al. (Luchtel epinephrine nor by inhibited is this and cell, channel the through particles and fluid movement of both the stimulates vasotocin arginine The neurohormone h composition oftheslimeterrestrialslugsranges The defensive found in are mantle Specialised on the glands Mucus-secreting cellsarealsopresentintheepitheliaof M odific channel cells that penetrate the skin in terrestrial a tions neural and/orendocrine Biology and Evolution of the Mollusca of the Evolution and Biology

for T errestri possibly, providing fluid a l L Tegillarca granosa, ife 16 controlofboth - - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 and channelcells (i.e.,nocalciumcells)are thephilomycid 3.3.2). Examplesofslugswith onlymucous (see Section be thecatalystforrendering mucusadhesive (Smith 2010) slugs whichlackcalciumcells, suggestingthatcalciummay sive mucus(Martin &Deyrup-Olsen 1986). 1984), withthemucousandcalcium cellssecretingtheadhe- mucous cells,calciumandchannelcells(Luchtelet al. of glandcellsinthedorsalsurface – types main three are In stylommatophorans. other et al. 1984;Smith2010). tain protein,andthesemayactuallybechannelcells(Luchtel on thecollarare‘proteinglands’whosewatery contentscon- cal granules ina protein matrix (Campion 1961). Also present tral partofthemantlecollarandcontainrod-shapedorspheri - on the foot sole. Calcium glands are also common on the ven- secretes AMPS has granular contents and islike cells found late. Another, lesscommon,typeofmucouscellwhichalso polysaccharide andtheglandcontentsappeartobereticu- gland whichsecretesanacidic,probablysulphated,muco- epithelial andlarge, oneofthemostcommonbeingamucous areallsub- 3.3.2). They (Campion 1961)(seealsoSection on thecollar(mantleedge)appeartosecreteepiphragm skin ofCornuaspersum (Smith2010).Ofthese,threetypes cells (Martin &Deyrup-Olsen 1982;Luchtelet al.1984). haemocoelic 2001. UK, Wallingford, Publishing, Molluscs Terrestrial of 178, Biology G. M. Barker, The in pp. 147– function, and Form I., wall: Body Deyrup-Olsen, D.L. and slug Ariolimax terrestrial 3.25 FIGURE Shell, Body, and Muscles and Body, Shell, Less sticky watery mucus is found on the dorsal surface of The skinofslugs(Figure 3.26) hasbeenbetterstudiedthan Eight typesofglandcelloccurindifferent regions ofthe vacuol centra

­pressure and the permeability of the channel Channel cell from the dorsal integument of the of the integument dorsal the from cell Channel e l nucleus . Redrawn and modified from Luchtel, from modified and . Redrawn membrane basement tubule there there columbianus Ariolimax microvillous epithelialcells passage ofhaemolymph processes thatmodifythe ion e composition ofthe uid ultraltrate intoand through thevacuole xc in thevacuole hange &transpo , CABI rt

cells (Lane1964). hasthreetypesofgland ated withthemouth(seeChapter 7), tentacles (e.g., Wondrak 1981)andSemper’s organ, associ- also oftenassociatedwithchemoreceptive epitheliaonthe 1998). Hawkins tral mucopolysaccharideandaprotein(Davies & suprapedal glandwhichproducesaweaklyacidicandneu- alsoaverymucopolysaccharides andprotein. small There is on transverse ridges on the sole, is, as usual, a mixture of mucus,secreted byglandcells 1998; Smith2010). The foot &Hawkins gland ductswhentheslugisirritated(Davies secretion releasedonthesurface fromtheinflatedcommon bination ofthesetwo secretionsthatresultsintheadhesive presumably the com- second cell type secretes protein. It is non-sulphated carboxylatedmucopolysaccharideswhilethe dant typeofglandcellsecretesneutralandweaklyacidic, into acommonductthatopenstothesurface. The most abun- slugs mentionedabove, thesubepithelialglandcellssecrete the surface appearstobedry. Unlike thestylommatophoran are two typesofglandcells(Cook1987),but atothertimes duces avery sticky mucusonitsdorsalsurface, wherethere gland cellinitsskinandalso,responsetoirritation,pro- cells (Wondrak 2012). glandcomprisesidenticalmucus-secreting gland. The whole teriorly alongthedorsalsideoffootasatubular suprapedal mucous gland found in all stylommatophorans. It extends pos- rior gland. The suprapedal glandisagreatlyenlarged anterior gland ductopens,oneamediangland,andtheotheraninfe- the foot,oneondorsalanterioredgewheresuprapedal three distinctgroupsofsecretorycellsontheanterioredge of glandcells(Cook & Shirbhate1983).In addition, thereare in theslugLimacusecarinatusatleast,consistofthreetypes surrounds thefootandisrichlysuppliedwithglandswhich, stylommatophorans,theperipodialgroove (Smith 2010).In their narrow necksextending betweentheepithelialcells secreted protein. All these gland cells are subepithelial, with 13, oneofwhichsecreted AMPS andanunusualtypethat kinds ofsecretoryglands(otherthanchannelcells)out limacid, found inthedorsalepitheliumofbodysurface ofanother contrast,CookandShirbhate (1983) eri) (Arcadi1967).In 2000) andthelimacidLehmanniavalentiana(asL.poiri- Meghimatium (= Adese a.19) h epithelium incontactwithfree al. 1999). The (Andrews et secretion of hydrochloric acid by mammalian oxyntic cells appears tobethesameinall thesecasesandsimilartothe secretorymechanism 5). The robranchoideans (seeChapter 1986), andinthesalivary glands oftonnoideansandpleu- (Thompson 1969), in the acid glands of and cypraeoideans (Edmunds 1968b) (see also Chapter 20), such asseenintheskinglandsofsome‘opisthobranchs’ Some molluscscanproducestrongsulphuricacidsecretions 3.3.5 In stylommatophorans, clusters of small gland cells are systellommatophoran The A Limacus ecarinatus(asLimaxpseudoflavus),two cid - S ecreting Incilaria) T issues (aauh t al. fruhstorferi (Yamaguchi et Veronicella has11typesof Philine (Thompson 91 Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 hydraulic skeleton comprisingtheblood inthehaemocoelic by antagonistic muscle elongation and contraction against a Most movements madebymolluscsinvolve forcesgenerated 3.4 the acidcontactingcellsurface (Andrews et al.1999). devices andacoatingofmucus,orcirri,ciliathatprevent acid secretionisprotectedbyvarious possiblymolecular from Newell, modified and P.F.,Redrawn Malacologia FIGURE 3.26 92

MUSCULAR HYDROSTATMUSCULAR

Arion and Deroceras and onArion slugs (based (sole) ventral of and terrestrial dorsal the epidermis through sections Diagrammatic ex haemoc Dorsal sur Ve tracellula pore cell glycogen nucleus coat ntral sur muscle (Sole) yanin r fac fac e e septate junc , 16, 183–195, 1977. tion por e oeuuulfaue n iiain RselHne & some unusual features andlimitations(Russell-Hunter with aconstant bloodvolume inthehaemocoel,results in distance fromtheorgan concernedandthisfeature, together blood flow isreliantonantagonists thatareoftenatsome antagonists areoftenlacking (Russell-Hunter1968). Thus, In many molluscanstructuresthereareretractors,but obvious tion orwithdrawal canberapid ifitinvolves retractormuscles. this way istypicallyafairly slow process,althoughcontrac- andcontraction ofpartsthebodyin spaces. The dilation -secretin mucus cell g Biology and Evolution of the Mollusca of the Evolution and Biology Golg mitochondrion cilia microvill basal lamina sensor muscle i zone y cell i ). ). Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, from Tompa,from Watabe, N., A.S. and J. Morphol. FIGURE 3.27 naticids (seein Section 3.8.2), hydraulic resulting where the water-sinus is the mechanism system different very Another 1962). & Grant &Newell 1956; Russell-Hunter Chapman shell of adductoronist muscles the (Russell-Hunter 1949; antag skeleton. is the siphonal musculature the In these cases, hydrostatic siphons accessory cavities and an as mantle of the sealed temporarily the in edges seawater use mantle contained some molluscs.in Bivalves siphons large very with fused and (Goldingcaenogastropods 2009b). et al. (e.g., 1995) of introverts higher proboscis Chapman the and systems occur, for example,Similar some bivalve in siphons (see muscle wall lar mantle system Section 3.12.3.8.2). the in circu main muscles the against act radial where the alopods efficiently. includecoleoid of Examples mantle the wall ceph- more muscles used be antagonistic can the haemocoel, of the rest the is isolated from structure blood aparticular in the If compartments. into haemocoel by the dividing part, at least in shell, butbe the inefficiencies into withdrawn overcome, can when animal the in contained be which can that to is limited tures, resultinginotherpartsofthebodybecomingflaccid. large proportion of its blood to expand the male genital struc- ple, acopulatingstylommatophoranlandsnaildisplaces of structuresthatcanbeextended atany given time.For exam- Russell-Hunter 1968). Examplesincludelimitstothenumber Mechanisms that sidestep these basic limitations are found are basic sidestep limitations that these Mechanisms volume bivalves and ofThe total blood most gastropods in

Diagrammatic section through the attachment zone of the columellar muscle of a gastropod snail. Redrawn and modified modified and Redrawn snail. muscle of agastropod columellar of the zone attachment the through section Diagrammatic , 149, 339–352, 1976. - - 1976; Watabe 1988) More Song recently et al. (Figure 3.27). Bevelander 1970;Nakahara & Plesch 1976; Tompa & Watabe literature) (Hubendick 1958; earlier in border Mutvei 1964; shell of (often the abrush surface called inner don the to cells ten the epithelial of microvilli the fibresfrom organic extends extensivemuscle shell. An the and network of extracellular epithelium (tendon an and cells) matrix the between lie lular bivalves, and a collagenous intercel shell. In gastropods the muscle of the to attachment was no direct there that was seen it microscope, electron closely using atransmission examined way adhesive of an epithelium (Hubendick 1958), but when the mantlealsodirectlyattachtoshell(Smith1983). heterodont bivalves (Unionidaand Trigoniida), smallpatchesof which provides a stable anchor point. Unusually, in the palaeo- head andgillmuscles,etc.arealsotypicallyattachedtotheshell lial line in bivalves). Other muscles such as the buccal retractors, muscles), andmantlemuscleswhichattachtotheshell(e.g.,pal- opods, monoplacophorans,Nautilus,andgastropods (columellar are mainlythefootorpedalmusclesofchitons,bivalves, scaph- bodyisattachedtotheshellbymuscles. These The molluscan 3.5 (Russell-Hunter & Russell-Hunter 1968). shell of capacity the the four to times skeleton three be can It was thought that the muscles attached to the shell by the to muscles the was attached thought that It my Shel septate desmosome apical hemidesmosome Co cell Epithelial tendon microvillus oftendoncell muscle hemidesmosome macula adherens micro lament desmosome basal hemi- organic bril fibril tendon sheath ATTACHMENT OFTHE BODY TO THE SHELL otendon spac lumellar muscle l tendon cells epithelial s e shell 93 - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 2012). Pigment-containing chromatophores under nervous 2010;Mäthger et al. 2010) andinoctopuses(Huffard et al. sematism insomenudibranchs (Edmunds1991;Haberet al. the external bodytissuesarealsoconsideredimportant inapo- probably reducesthethreatof visualpredators.Pigmentsin dark pigmentationofexposed bodyregions ofgastropods the aforementioned For example, ration (see Section 3.2.8). with crypsis and perhaps aposematism, as with shell colou- gastropod taxa. of sides head many edge, on foot, the and of mantle the involved seen black brown and pigment dark patterns the in probably are Eumelanins taxa. muricoidean other and of Stramonita haemastoma gland hypobranchial the from dyefamous Phoenician Tyrian which was purple, produced 1976), (Branden oid cephalopods indoles include and the of cole chromatophores found the in are Ommochromes of some coleoid ink the cephalopods. which comprises tein brownbrown, black, to and respectively, melanopro and yellow to red from range that and diverse melanins nins, brown. and red, green, yellow, between colours varying with ofucts porphyrins Section 3.2.8). (or Bilichromes - prod metabolic bilins) are shell pigments as (see important being also porphyrins with 2006), pigments as (Bandaranayake secondarily, and, role oxidation in play aprimary They porphyrins. and Heras et al.2007). sues includingtheovary andeggs ofsomemolluscs(e.g., green, purple, and red and have been found in various tis- Carotenoproteins producemany colours,includingblue, in most­ arepresent responsible foryellow toredcolours. They (2006) arecarotenoidsderived fromplantsandare overviewmore recent (2006). of Bandaranayake reviews of Fox (1966), (1972), Goodwin Fox (1983), the and of ­ treatments (2016). Section 3.2.8 shells, Williams see in and types Useful some explanation of the tissues. molluscan For in pigments ­ main the we section, brieflyIn this outline 3.6 2003). (Price mella of neogastropods not always for shell –as on the example, colu marked on the of ismuscles mantle attachment and the shell, although the of interior on the line pallial the as is indicated ment scar (Bubel - tonofilaments the attach contain 1984).In bivalves, mussel the Mytilus in adductor muscle outer layer calcite the to muscle of the scar (2013) the aglue as act binding might proteins suggested that 94 Pigments intheexternal bodyobtainedfromfoodcanassist eumela- and pigments include pheomelanins Other the Tetrapyrroles include haemoglobins, the haematins, pigmentclassesrecognisedby BandaranayakeThe main shell by the to that tendon cells adheres also The mantle

PIGMENTS IN TISSUES IN PIGMENTS molluscs (e.g.,Kantha1989; Vershinin 1996). pigments in molluscan tissues include the earlier include tissues molluscan pigments earlier in the . identified identified ­pigment - - -

lages are described in Chapter 5. in described lages are (e.g., invertebrates other in 1977). carti Odontophoral Kryvi seen cartilage the or in cartilages odontophoral in not found Person 1970) are that (Philpott & extensions matrix the into have cells long cartilage cytoplasmic squid head and cells, the of number vesicles and size the in differences in ple, are there For exam some differences. are it, possess there that tebrates inver all in similar is rather of cartilage structure cellular the general in Although of cephalopods. brain the encapsulating bivalves, than classes other it found and is all also in cartilages or odontophoral buccal the in occurs cartilage In molluscs, 2007). Schmidt-Rhaesa 2004; &Hall (Cole Brachiopoda and Annelida, Mollusca, Chelicerata, including the than other several groups in invertebrate tissue occurs Cartilage c 3.7.2 of aeolidioidnudibranchs(seeChapter 20). and insideepithelialcellsliningthebodypartsofgut various molluscanstructuresincludingtheradulaeandjaws, in the cell walls of fungi, the exoskeleton of arthropods, and in N-acetylglucosamine, whichisderived fromglucose,isfound Chitin, along-chainpolymerofthemonosaccharide c 3.7.1 3.7 in coleoidcephalopods(seeChapter 17). and muscular control are responsible for rapid colour changes external environment. external the with contact direct in are edge, that mantle along the with Scaphopoda, andGastropoda. conditionoccursinCephalopoda, shell muscle(s). This Buccal musclescarsareabsentexcept thoseintegrated with attachedtotheshell. tion iswhentheheadregion isnot Polyplacophora, andBivalvia. The isseeninMonoplacophora, rior oftheshell. This condition shell, andbuccal musclescarsareoftenpresentontheinte- dition is where the head region is attached dorsally to the tionship oftheheadwithshell. The We introducetwo new termstorecognisethedifferent rela- but closely linked, structures–hencethetermhead-foot. and gastropods –theheadandfootaredistinctlyseparate, threegroups –scaphopods,cephalopods, 12).In Chapter often sharesdorsoventral muscleswiththehead(seealso footisimmediatelyposteriortotheheadregion and The with themouth,comprisingheadregion ofthemollusc. sues andsensoryorgans attheanteriorofanimal,along undergone cephalisationwithaconcentrationofnervous tis- Like mostbilaterallysymmetricalorganisms, molluscshave 3.8 In shelled taxa (bivalves taxa excepted),In shelled foot, and it head is the NON-CALCAREOUS STRUCTURAL STRUCTURAL NON-CALCAREOUS HEAD-FOOT ELEMENTS IN THE BODY h a itin rtil –A S a ge –S tructur Biology and Evolution of the Mollusca of the Evolution and Biology tructure a l

P a nd olys H a apocephalic condi- o cc m ligocephalic con- ha ology ride - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, one of the cephalic tentacles is modified as a penis, but, in but, penis, as a tentacles is modified one cephalic of the few of groups gastropods eyes. small located In a laterally tropods), of tentacles (cephalic apair tentacles), of apair and jawsthe mouth(a just distal of inside the synapomorphy - gas tentacles of resemble gastropods. cephalic also they the that (2002a) concluded Haszprunar Wanninger and and lopod arms, - cepha to Dreyer and Steiner captaculae (2003) the compared (see scaphopods to is unique and 16). head Chapters 5 the from of long, tentacles (captaculae) hair-like emerge that laterally jaw. the to it anterior is formed because gastropods A series homologous snouta ‘proboscis’) in the with seen is not that organs. sense cephalic development the with correlated of additional appears and shell, the into withdrawal facilitates musculature, ents head exoskeleton adorsal from head of the reori The detachment well-developed. especially being cephalopods and tropods of those - gas heads, have detached –all distinct, Cephalopoda Chapters 7 and15. detailsonthesensoryequipmentofbivalves see For further Eyes are also developed on the ends of siphons in a few taxa. 2017)(seeChapter 7). guanine crystalmirrors(Palmer et al. lops) there are eyes, some of which have double retinas and mantle edgeand/orsiphons,andinafew taxa(e.g.,many scal- mation. Many have sensory papillae or tentacles along the bivalves mainly utilise the mantle edge to gain sensory infor sensory structures with which to assess the external world, (autobranchs). Becauseofthelackaheadandassociated either directly (protobranchs) orindirectlyviathe ctenidia ciliated tractswhichassistinsortingfoodparticlescaptured region arethemouth and itsassociatedlabialpalps,with onlyremainingvestiges ofthehead tinct headregion. The ‘velum’ fold. mantle anterior the and tentacle the between preoral asmall and appendages post-oral of haveMonoplacophorans tentaculate also pair aposterior 1959). &Wingstrand found monoplacophorans (Lemche in ‘velum’ the to similar structure disc oral the surrounding Placiphorella may have (e.g., extended or lappets lips chiton carnivorous the and mouth the surrounds disc oral simple chitons. An in erally is gen mouth. The head ventral the carry to aprotrusion than which foot, it from more the to is little anterior situated and shell. It is the to eyeless, by small, its attachments constrained with fooddetection,but isalsoinvolved inburrowing. motile. Caudofoveates have asensoryoralshieldthatmayassist moving, theheadregion isheldabove thesubstratumandis sory vestibule locatedanterodorsallytothemouthand,when with aterminalorsubterminalmouth.Solenogasters have asen- Aplacophorans have apoorlydifferentiated, eyeless headregion t 3.8.1 The gastropod head bears a short to elongate to ashort snout bears with head The gastropod consists of head ‘snout’ alarge The scaphopod (often called and Gastropoda, –Scaphopoda, taxa three The remaining Bivalves are the only molluscan group which lacks a dis- region head monoplacophorans, is chitonsthe and In both h e H ). In e a d Lepidopleurus R egion there is a dorso-lateral hood hood is adorso-lateral there - - - groove ­ by amantle it groups is surrounded both In surfaces. sole creeping capable abroad, has of clampinghard to (Ivanov 1996; Scheltema 1996). is secondary foot groups aplacophoran reduction or loss the in groove. There is end pedal of evidence the the anterior that the eversible at pit lies bymucus that aciliated, produced pedal on Movement mucous with plied glands. creeping is by ciliary of fold anon-muscular sup richly and or folds is ciliated and specimens) groove preserved which in consists pedal ventral Solenogastres the have foot within (retracted narrow avery Caudofoveata aplacophoran lack afoot the while The t 3.8.2 hectocotylus)structure. copulatory as a is modified 17. and Chapters 8 (the coleoid one arm In male cephalopods, in more detail in 2008), al. discussed as foot (Shigeno et the from be to appears arms of the suckers. The derivation tentacles. Nautilus retractile as fied modi are apair ten, are there if suckers and, or hooks bear Nautilus in 90 ‘arms’ (up by of tentaculate aseries to ismouth surrounded (introvert) proboscis aretractile form to (see Chapter 5). snout the is inverted gastropods, 18–20. higher and In some Chapters 7 in more detail in discussed are found gastropods in of tentacles types edge. foot The various mantle the and with tentacles associated additional sometimes There are present. usually are structures penial other taxa fertilising internally 98 usl-utr pe 98 usl-utr & & Apley 1968;Russell-Hunter 1968; Russell-Hunter sinus systemtoexpand thefoot(Morris1950; Bernard by takingupexternal seawater intoanextensive pedalwater- thisisachieved tropods, bemarkedly expanded. In naticids, sides andtopofthefoot(seeChapters 911). squamiferum hasdeveloped iron-mineralisedscalesonthe hydrothermal vent snailChrysomallon ‘fin’. The keel-like tropod group, the heteropods, have the foot modified as a othercompletelypelagic gas- are modifiedparapodia. The wingsofthepelagic pteropods and Gastropteridae. The Hydatinidae, Akeridae, Aplysiidae, as Atyidae, such branchs of thefootformparapodiaseveral groupsofeuopistho- opercular lobe is sometimes also present. Lateral extensions gastropods, othertentaclesareassociatedwiththefoot,andan and epipodial sense organs (see Chapters 7 and 18). In caeno- is presentinmany vetigastropods andtypicallybearstentacles lum (seeSection 3.8.3). fringe,theepipodial A lateral there isusuallyanopercularlobewhichsecretestheopercu- an anterior propodium and a larger metapodium. Dorsally, mobile, usually flexible and,inorthogastropods, divided into monoplacophorans. inthe shell and byin chitons afleshyexternally girdle In polyplacophorans and monoplacophorans the foot monoplacophorans the polyplacophorans and In eyes, have of the lateral large Cephalopods and apair h footcan,particularlyin someburrowing caenogas- The footingastropods isparticularlywell-developed, The containing the gills, and the groove the is covered and gills, the containing h e F oot or 8–10 coleoids, may coleoids). these in In ‘tentacles’ or cirri lack ‘tentacles’ or cirri 95 - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 (see Chapter 15). molluscs ofthose other or even bivalves within (Waller 1998) afewin bivalves, probably are not homologous but these with tion (see Section 3.3.2.1). found also are glands pedal Anterior locomo sole mucus lubricate the to during secrete gastropods foot chitons, of aplacophorans, monoplacophorans, and the in end anterior the near Besides sole glands epithelial glands, 3.8.2.1 Chapter 17 for details). cavity, mantle muscular the jet propulsion notably (see during of water expelled from astream directs funnel The muscular 17). and Chapters 8 see information (for 2008) further et al. foot the (Shigeno derived from are arms shown the that such, developmental as although have recognised studies be papillae. with foot of fringed the disc is often terminal the Gadilida, In the sediment. foot the the in anchor that ventrally and laterally foot well-developed has conical the lobes epipodial smooth former, In the Gadilida. and Dentaliida groups, two main the most bivalve cementing foot the is reduced. species in foot, of while the part posterior ventrally, the in especially present is sole-like flattening asmall sometimes and rounded autobranch bivalves, foot hatchet-shaped the is or often In sediment. the in anchor an as act to laterally expanded be can most The keels species. in papillae with keelsventral fringed bivalves,tobranch foot two form to the ventrally is divided for crawling, or even reduced or very lost (in adults). In pro (modifiedcompressed digging), for rarely laterally expanded bivalve laterally foot large, typically is often muscles. The retractor pedal posterior and anterior byspaces enlarged haemocoelic through using generated hydrostatic pressure capable being sediment in of in digging gastropods and rans, of chitons, monoplacopho typical surface creeping broad the expelled toenablethebody ofthewhelktofitwithinshell. foot is fullyretracted into the shell, blood and water are both the kidney) beforereturningtothegillandmantle. When the bloodisreconcentrated (presumably by ing theblood. The and that blood and water mix freely in the foot, greatly dilut- the footinBusyconcaricaisexpanded byseawater uptake, (1978)showedalso occur(Brown that 1964).Mangumet al. to haemocoelicpressure,but someminorwater uptake may foot ofthesurfbeachnassariidBulliaisexpanded largely due pods (Russell-Hunter & Russell-Hunter 1968). The very large the infoldedpedalmucousglandsofsomeothercaenogastro - could bederived fromepidermalinvaginations suchasseenin sible thatthisuniquewater-sinus systeminthe footofnaticids pos- Russell-Hunter1968).It is seconds (Russell-Hunter & taking several minutes,althoughretraction takes onlyafew naticids ondrysurfaces, andeven inwater expansion isslow, those ofthepropodium. Thus, pedalexpansion cannotoccurin water mustbepumpedfromthemesopodialwater-sinuses to system are in themesopodium so thatduring expansion, sea- pores of the water-sinus Russell-Hunter 1968). The external 96 In cephalopods, the foot is so highly modified it cannot footit cannot modified the is so highly cephalopods, In in differs and glands foot pedal the lacks In scaphopods, bivalves, many and scaphopods from foot the differs In Pedal Glands Pedal - - - can be situated internally, marginally, or terminally. Spiral Spiral internally, or terminally. marginally, situated be can its nucleus and is not spiral, type This latter concentric. and nucleus, (oligogyrous)a central paucispiral few with spirals, (polygyrous) multispiral and ognised: spirals numerous with reduced operculumembedded inafleshy pocket. like neritimorphs (e.g.,PhenacolepasandSeptaria)have a neritimorphs (ProserpinidaeandCeresidae),whilelimpet- pod families. isalsoabsentinsometerrestrial The operculum and sometaxainanumberofvetigastropod andcaenogastro- pod, cocculinoidandlepetelloidlimpets,mosteuthyneurans, absentinadultpatellogastro- some basaleuthyneurans. It is tropods and caenogastropods, in lower heterobranchs, and gastropods, anoperculumispresentinmostvetigas- In adult tophorans andvaginulids (G.Barker pers.comm.Nov. 2014). oping embryosofsomegastropods, includingstylomma- (Gibson 2003). An operculumisalsoabsentindirect-devel- most nudibranchlarvae, althoughitislostatmetamorphosis stage; itisabsentinthelarvae ofpleurobranchs,but presentin usuallyfirstappears inthelarval morphy ofthegroup.It shows mantle, not the itepidermis, is not a homologue. valve second production supposed but of the the by foot the bivalvethe shell (see 1962, review p. 76), Fretter & Graham in shell valve asecond operculum equivalenttropod and with Someearly calcified. - the gas workersconsidered sometimes of and foot of is composed conchiolin the and surface dorsal Chapter 17).see on the is generated operculum The gastropod (also chamber body withdraws the into animal when the ture which closes shell aper the structure hood form a leathery Nautilus withdrew. In living animal the (the shell of when the aptychi), which closed aperture the of horny, lower apair calcified, had sometimes and jaw plates ammonites cephalopods, ently derived. independently In the appar all Gastropoda, the in –and ammonites nautiloids and – Cephalopoda in occur Mollusca, opercula the 2009). In Wanninger even phyla within (e.g.,structure, Brinkmann & multiple represent to protective derivations appear ofand this Mollusca, Hyolitha, in Annelida, occur Bryozoa, and Opercula 3.8.3 Section 3.12.3.4). Chapter 15).and autobranch bivalve (for Section 3.11.1 see larvae more details footfound the of adult in autobranch bivalves many all in and sole. or slit the in ture aper an via opens (or that gland pedal metapodial) posterior alarge in concentrated are some these in metapodium, of the foot. of the part muscular the and viscera the between runs that gland – gland along tubular it stylommatophorans, is developed suprapedal the as In foot. some the extends into in deep and gastropods many in - rec usually are opercula of gastropod basic types Three gastropod operculum is areadilyidentifiedsynapo- The below foot of the is described (see musculature The is the gland, byssal gland, pedal posterior modified A sole the to have opening gastropods cells gland all While well-developed is particularly gland pedal anterior The O perculu m Biology and Evolution of the Mollusca of the Evolution and Biology , two modified cirri cirri , two modified - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, Jiménez 1998 references). and for more details (see operculum of Jiménez- the bottom Checa & at the added each disc, opercular of the surface the posteriorly from added layers opercula, are disc. In concentric edge opercular of the opercula),concentric byposterior the aflap it on is secreted (including butothers in groove, some trochids, in as opercular the behind by groove immediately lies asecond that secreted disc. Varnish may be edge opercular of atthe the cells by tall layer hyaline below (when thin the present) is secreted and layer lies operculum of the The main edge aperture. of the groove inner coincides the with opercular the is retracted, foot the When periostracum. the to similarities bears secretes it material the and axis, body main the across runs and disc edge opercular of the anterior at the lies structure foot, this groove. extended the opercular On foot, of the the structure layer hyaline (when aslit-like present) in is secreted The (calciticcareous or aragonitic) layers added. are one or more cal taxa, In some opercula. found concentric in nucleus adventitious edge, and labral on the layers only are the with opercula layer concentric and line is found spiral in layers always are varnish ahya and present, - main the While &Jiménez-Jiménez 1998). (shiny)varnish layers (Checa layer,hyaline layer, main adventitious athicker the and and outer side –athin outer inner to –from typically which are levels higher has layers other of the 1976). (Hunt glycine than varnish the acid content, although glycine aspartic high and a with acids of amino pattern show asimilar examined cula oper All by tanning. quinone geneous scleroprotein hardened (Shirbhate & Cook 1987). proteins staining atleast two mucopolysaccharide and differently secrete erally gen groove disc and opercular the in cells Secretory surface. whole under not the operculum, of the only to part attached disc. It is opercular the foot, of called the surface dorsal the have apaucispiraloperculum(Yochelson & Linsley 1972). the MiddleOrdovician, while Macluritesfromthesameperiod Typical multispiralcalcifiedoperculaareknown asearly & Wise 1972). opercula(Yochelson shells areprobablynot Ceratopea Bridge1957),but (Yochelson & thesecap-shaped as calcifiedoperculaaretheEarlyOrdovician fossilsnamed gastropod evolution. fossils sometimes interpreted The earliest opercula. paucispiral and multispiral between distinction clear how is and not a tightly so there of coil they number spirals considerablethe in is also variation There bithyniids. in as concentric, become to pattern spiral initially an change from clear-cutnot as For example, thought. often as some opercula are distinctions neat seemingly but these operculum, of the periphery of the or part along all is added ently – new material grow differ opercula Concentric taxa. clockwise sinistral in is always rotation counter the and clockwise dextral tern, in it as grows. pat outside rotates onoperculum the Based spiral (see disc below), edge opercular of the internal the the and at secreted (whetheropercula are or paucispiral) multispiral The different layers are produced in different ways. different in layers different produced are The 3.28), consists of operculum several layers (Figure The ahomo The operculum of mainly is composed conchiolin, on epithelium, a disc-like to is attached operculum The Calcification oftheoperculumhasoccurredmultipletimesin ------match the aperture in shape ( shape in aperture the match closely that –those opercula of spiral kinds two main nised Jiménez-Jiménez and (1998) Checa years, recent recog (Checa & Jiménez-Jiménez 1998). operculum aconcentric result in will a canal with aperture elongated an while more spirals, with circular becoming cula oper oval result in often paucispiral shell morphology will ral planispi or near planispiral to depression leading spire of the example, the by shell morphologies.changes imposed For aphylogenetic has gastropods by in is modified basis, this Retusa and Rissoellidae in opercula centric (Checa & Jiménez-Jiménez 1998), exceptions with con being lower few the euthyneurans and operculate heterobranchs found all nearly in are opercula Rigiclaudent spiral tropods. found neogas- in only kind is the this and opercula, centric mostly caenogastropods have Higher opercula. con spiral have afew although gastropods, cerithioideans flexiclaudent lower in type caeno usual the is also this and operculum, have arigiclaudent Neritimorphs predominant. former the vetigastropods, with present in types the generally are ral layers closely are calcareous and packed together. (e.g., calcareous are Pomatiidae), Bithyniidae, where organic Jiménez-Jiménez(Checa & 1998). opercula Some concentric operculum (ascalcium corneous aragonite) otherwise onto the foot, deposits the not the margin, mantle labial the opercula, calcareous with naticids. In naticids and some neritoideans in occur opercula spiral of calcified types Other foot is retracted. exposed when operculum the the and ing, but it is retracted is crawlcompletely covers animal when operculum the the or fold whenThe precipitation this partially of occurs calcium foot groove is extended) (Figure 3.28). edge opercular of the by afold (when anterior atthe of lies epithelium the that is achieved This operculum. paucispiral face of acorneous layer outer sur on the calcareous is added athick turbinids example, in but is achievedopercula, several in ways. For above.described formation and structure, form, in distinctions the between situations intermediate many are there noted, already As it (i.e.,or may as grows). not be spiral rotating operculum the may growth this and aperture, is held operculum the in the grow when margins, outermost tion, except attheir perhaps which do not flex two- types other extended.retrac The upon the when isfoot secreted is flexiclaudenttype spiral The in size. unless reduced it is the aperture fits typically also plate when (3) growing, and rigiclaudent which concentric, atem as is used more usually, aperture paucispiral), the and or,mayand be multispiral (fittingthe aperture dent spiral but fitsaperture, rigiclau the (2) by into flexing aperture, the of shape which not fit the does operculum, multispiral) (1) types: main three flexiclaudent tinguished spiral (mostly - dis authors These outward. by edges bending the aperture the fits operculum Trochidae where the and Pleurotomariidae do not ( In the only detailed investigation in only detailed operculum of the the In While the distribution of the different kinds of opercula kinds different of the distribution the While rigiclaudentand (mostly A flexiclaudent spimultispiral) rigiclaudentin only occur can calcification Opercular flexiclaudent ), as in opercula of vetigastropods like of), opercula vetigastropods like in as rigiclaudent . ) and those that that those ) and 97 ------Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 A.G. and Jiménez-Jiménez, A.P.,A.G. Jiménez-Jiménez, and Paleobiology Tiere der Okologie und Morphologie fur Zeitschrift E., Kessel, Ecology and Anatomy Functional Their Molluscs: Prosobranch British A.L., Fretter, from Graham, and modified V. and lowerand redrawn right A.P., A.G. and Jiménez-Jiménez, Checa, from Paleobiology modified and redrawn section Uppermost disc. FIGURE 3.28 98 groove opercular secreting varnish groove , Ray Society, London, UK, 1962;, Ray générale Society, et UK, onHoussay, London, based F., expérimentale zoologie de Archives

oper

The structure of various types of gastropod opercula, as seen in cross-section, and its relationship to the foot and opercular opercular foot and the to its relationship and cross-section, in seen as opercula, of gastropod types of various The structure

c ular dis ular calcium laye paucispiral rigiclaudentwith ex

multispiral exiclauden c ternal calcareouslayer r f oot epipodial e varnish laye secretes calciumlaye , 24, 109–132,, 24, 1998. t xt r ension which Sections throughopercul concentric withterminalnucleus concentric withinternalnucleus r , 38, 197–250, 1942; three of lower four redrawn and modified from Checa, Checa, from , 38, 197–250, modified of and 1942; lower redrawn four three paucispiral rigiclauden multispiral exiclauden nucleus nucleus a nucleus t t concentric withe paucispiral rigiclauden direc Biology and Evolution of the Mollusca of the Evolution and Biology operculum asitgrows tion ofrotation adventitious laye conchiolin (main)laye xt , 24, 109–132,, 24, 1998; next three ernal nucleus t nucleus , 2, 171–288,, 2, 1884 and r r opercular lobe Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 the mantle and the shell (i.e., that part lying beneath the shell) the shell lying (i.e., beneath the and mantle part the that fluidbetween extrapallial shell.of the with It is the contact in surface body.the inner molluscs, the it In shelled against lies layer epithelial (‘skin’) of The thin part covering visceral the d 3.9.1 terminology outlinedbelow forthepartsofmantle. material tothicken orrepairtheshell from theinside. We usethe mantle edge. The mantle underlyingtheshellsecretesadditional ostracum andthegrowing edgeoftheshellaresecretedby the together with,ifthey arepresent,theprotrudingedges. The peri- dorsal covering ofamolluscbody(except fortheheadandfoot) Here wetreatthemantleasepitheliumthatformsentire also usethetermfordorsalepitheliumcovering theviscera. Graham1962) of theshell,whilemany others(e.g.,Fretter & some (e.g.,Hyman1967)restrictthemantletolastwhorl ated withthemantle,anditsextent –forexample, ingastropods issomeconfusionastotheterminologyassoci- body. There been reducedorlost,thepartthatliesover thesurface ofthe lies beneaththeshell,orinthosemolluscswhereshellhas cavity groove. or mantle mantle or exiting the entering ble water for currents regulating responsialso It is surface. respiratory asignificant often and information, of spicules,shell reception sensory and/or the of formation out the cavity, –the several functions carries and body, dorsal the of mantle molluscs. including the It covers is one hallmark pallium, the called sometimes The mantle, environment. that with animal of the interactions role the in plays thus and environment asignificant external the with tact con direct edge has mantle foot, the and head Along the with 3.9 of possibleshapes(Checa &Jiménez-Jiménez1998). the evolution oftheconcentricoperculumanditswiderange a siphonalcanal)becamepossibleandgreatlyincreasedwith cification. rangeofaperturalmodifications(suchas A greater The evolution ofrigiclaudentoperculaalsoprecededtheircal- pendent evolution oftherigiclaudenttypeinseveral lineages. aperture shape, but this was rectified by the subsequent inde- the modified periostracal)groove. Theseoperculadonot fit from theperiostracalstripproducedbyopercular(i.e., lar disc,theflexiclaudent spiraloperculumcouldbeformed form of the operculum. With thedevelopment of theopercu- foot providing thenecessaryorganic materialtoformanearly independent from the rest of the mantle and migrated on to the parietal segment ofthemantleperiostracalgroove became appears to be the most primitive type. They argued that inthe the morphologyofflexiclaudent spiraloperculum,which ing model’toaccountfortheoriginofoperculumbasedon and Jiménez-Jiménez(1998)proposeda‘periostracumshav- This substance ischemicallylike theperiostracumandCheca ability tosecretetheconchiolinwhichformsoperculum. operculum onthesurface ofthefoot,andhow itobtainedthe Shell, Body, and Muscles and Body, Shell, The mantle consists of two main parts: the part that typically consistsoftwoThe mantle mainparts:thepartthattypically Various theorieshave beenproposedtoaccountforthe

THE MANTLE THE ors a l M a ntle - - flaps from the from flapsfoot Section 3.2.15).(see edge or parapodial mantle areflected from face is formed perinotum the called (or angulation agroove) sometimes by asharp notum the from demarcated This is surface. creeping ventral of the part forms foot, along slugs, the with hyponotum, tellommatophoran the hyponotum the edges is called protruding the beneath homologous mantle), dorsal surface ventral the with the and dorsum (plus extending edges) surface the the as to referred is often shell-less 3.2.19). slugs, sea dorsal the (seemal Section In available calcium ani the the to dissolved,shell are making of the chambers inner the ellobiid gastropods, as neritid and dissolve such shell. some taxa, For example, the or in taxa in overlying the thicken to shell, shell material secrete can and Chapter 14). nervous tissue (see from formed shell are the penetrate that (seeshell pores Section 3.2.9), aesthetes chitons, the in while bivalve and some shell extend gastropod forming the into taxa in mantle dorsal the from projections.elaborate The tubules some shell-lessin (slugs), gastropods into produced be it can bly plesiomorphic for Mollusca (see Scheltema 1993), while possi which aplacophorans are chitons and in papillae mal ys nac hsfnto seCatr 7),particularlyin eyes, enhance thisfunction(seeChapter in many molluscs. Many elaborations,includingtentacles and surface andprovides amajor partofthesensoryequipment external environment, themantleedgeisanimportantsensory fordetails).Becauseitisincontactwith the (see Chapter 15 much ofthemantleedgeconfines anddirectsthe water flow bivalves,with folds,flaps,orsiphons. In some theclosureof the mantlecavity byway ofcontrollingthesizeapertures sible forthecontrolofwater currents enteringandleaving edge isalsorespon- growing edgeoftheshell. The mantle the periostracumandinitialshellmaterialdepositedat the Parts ofthemantleedgeareresponsibleforsecretion lower epithelial layer is in contact with the external medium. ing somemuscle,connective tissue,andbloodspaces,the consists oftwo layersofepitheliaseparated byaspacecontain- edge expanded tocover someoralloftheshell. The mantle which maybeartentacles,and,insometaxa,onelobe be prise themantle edge . It usually hastwo orthree lobes, oneof edgeofthemantleskirtandany protrusionscom- The free 3.9.3 mantle. the of fieldsridges or is or ciliated not part Chapter 4), (see and/ glands suchas hypobranchial as structures modified which is often layer epithelial skirt, mantle of the The inner or, dorsum. of slugs, nudibranch the in as overhanging the part cavity roof mantle of the external the forms that mantle of the part cape-like body, that of the part particularly visceral the extend that beyond mantle of the for parts is used This term the 3.9.2 Other modifications of the dorsal mantle include mantle epider the dorsal of modifications Other or notum or M M a a ntle ntle S E (which, on its derivation, depending may be kirt dge . In some shell-less taxa the dorsal sur dorsal shell-less the taxa . In some . In sys- 99 - - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 the shell edge. In many limpet-like orthogastropods, thereis the shelledge. In many the shell,and the periostracalgroove issituatedadjacentto gastropods, themantle edgeformsasinglelobethatsecretes includingpatello- In most, of themantleedge(Figure 3.30). have, with a few exceptions, a relatively uniform arrangement but fromthemantleedge. of coleoidcephalopodsisnot derived fromthedorsalmantle, extension ofthemantlerim. Thus, theexposed dorsalsurface coleoids,themantlehascovered thebodybyan 2005). In dle lobeorfold. There is alsoaninnerfold(Westermann et al. ated betweentheouterlobe(thatsecretesshell)andamid - like the situation in bivalves, with the periostracal groove situ- in cephalopodscanbeseenNautiluswhereitistrilobed, more details). form siphons tionsand closeto (see mantle the Chapter 15 for bivalves In other surface. combina- folds various these in fuse lobe over is expanded middle the outer shellmatoideans, the (Stasek & McWilliams 1973) galeom (Figure 3.30). In some Schaefer 1997).fold (Haszprunar & is less distinct fold, ventral middle the inner hence shell) while an edge and (and mantle inside the groove some ventrally distance situated (seenarios Chapter 12). 1981),Haas it is only one of several possible evolutionary sce forconsidered primitive molluscs (e.g., Salvini-Plawen 1980a; condition been has this edges. Although mantle no distinct with body aworm-like surrounding spicule-producing mantle the conchiferanoutermantlefold(Haas1972;Stasek1972). properiostracal groove andtheshelledgeishomologouswith the mantleedgeinchitonsbetweenproximalwall ofthe beensuggestedthatthepartof contains mucousglands.It has ponent isalow ridgeontheundersideofmantleedgethat girdle andsecretesthespicules,hairs,orscales. The third com- by theperiostracalgroove. The main mantlerimcomprisesthe secretes the shell and is separatedfrom the main mantle rim foldontheproximaluppersurface of threeregions. A small dle aroundthelateraledgesofeightvalves. composed It is (1973). McWilliams (1967) Trueman and by Beedham and Stasek outlined as and major of 3.29), the groups molluscs in differently (Figure rated (see Chapter 20). chemicals are sometimes concentrated on themantleedge in othergastropods, andnotablynudibranchs, where noxious alsoexamples tise potentialpredators(Rice1985). There are those fromtherepugnatorialglandsofTrimusculus anesthe- Branch1980)and deter predatorsandcompetitors(Branch & tasteful secretionsofthemantleedgeinlimpetCellana example, assumed dis- structures that deterpredators.For molluscs and,insome,hasdeveloped repugnatorial secretory functions includingbeingasourceofmucussecretioninmany bivalves hasothersecretory becausethey lackahead.It also 100 Despite thesizeanddiversity ofthegroup,gastropods An indication of the plesiomorphic state of the mantle edge folds bivalves, of three edge is comprised In all mantle the aperiostracal edge has monoplacophoran mantle The molluscs having other a in unlike are Aplacophorans themantleskirtandedgeformagir In polyplacophorans, one or more edge folds has elabo which are The mantle - - - - the singlemantle lobethatisextended (Figure3.30). tropods withthe mantleenveloping partoralloftheshell,itis ventral foldformsafleshy curtainbelow the shell.In other gas- developed middle fold envelops part of the shell, and a larger species,awell- the mantleedgeisdistinctlytrilobed. In some from thenormalgastropod patternisseeninfissurellids,where a prominentinnerfoldorswelling, but the largest deviation Anz G., Zool. Schaefer, Haszprunar, from and K. Veliger and McWilliams, C.R. W.R., from Stasek, modified and Redrawn gastropod. bivalve a typical of and edge a typical mantle of the 3.29 FIGURE , 16, 1–19, modified and 1973. redrawn Monoplacophoran P Monoplac Aplacophor olyplacophor

Gastropoda C Scaphopoda Bivalvi ephalopoda A diagrammatic comparison of the morphology morphology of the comparison diagrammatic A a ophor Biology and Evolution of the Mollusca of the Evolution and Biology a a a ., 236, 13–23, 1997. Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 1917; Jones & 1970; Trueman 2014). et al. Kuroda pods (e.g.,pods Patella vetigastro and patellogastropods both in reported been has it Backward was locomotion duration. slow of limited and when present and rare, be to locomotionward gastropods in Boyle 1977; 2014). et al. Kuroda (1974b) Miller found back 1–19, 1973. 1–19, (e.g., (e.g., Backward locomotionpod. polyplacophorans is fastest in would that difficult for be a single-shelled gastro surfaces move and adhere to chitons allow over them irregular highly shell independent plates ofmove foot. along The eight the or wavesby waves) cilia (pedal activity of muscular that slugs and slowly snails, creep locomotion. limpets, Chitons, ably monoplacophorans), provides for adhesion and both 2011).Moroz (Four Fs) of Aplysia ible system of behaviours. four For example, basic the drives of of locomotion, which on acomplex depend all flex and roles of the breadth the describe travelled do not adequately (e.g., Donax bivalves of some rates energetic the burrowing and cephalopods, of rapid many jetting the shell-less pteropods, and heteropods of some swimming the of responses some limpets, territorial leaping movementsthe ­ of the strombid gastropods, faster movements somethis, molluscs, in such do occur as in is some truth there action. While of muscular antagonism and amplification the skeleton, limiting thus internal a hard, slow movements largely lack of due are the to of gastropods “at asnail’s pace”’. famously the that (2002) Chase argued movementsexamples for “sluggishness” time-consuming and (2012), Haase and Kappes provide proverbial ‘The Mollusca of organ locomotion. expressed deftly As foot by main is the crawl that the those or burrow, swim, some that in and In Molluscs move by crawling, or swimming. burrowing, 3.10 groove adjacent shell lies edge. the to The periostracal closing assists in edge that aperture. mantle off the anterior FIGURE 3.30 Muscles and Body, Shell, The broad, creeping foot of chitons, limpets (and foot ofThe broad, creeping presum chitons, limpets haveScaphopods a large, fleshy extensiontheir lobe-like to LOCOMOTION Chiton ,

Ischnochiton Mantle edge morphology in molluscs redrawn and modified from Stasek, C.R. and McWilliams, and McWilliams, C.R. W.R., Veliger from Stasek, modified and redrawn molluscs in morphology edge Mantle , Lottia all include 1996; locomotion all (Dickinson ). values Simple of distance rate-based epithelium , Fissurella , Cryptochiton shell Bivalv , Monodonta e ) (Parker 1914;) (Parker periostracum inner f old ) (Olmsted (Olmsted ) aggressive middle f old outer f old - - - - - ment and the strength of adhesion to the substratum. of adhesion the to strength the ment and of move speed the mode, affect locomotory in differences small shape, foot and and that size and caenogastropods, the within diversity occur modes locomotory greatest in the that (other Heterobranchia).gastropods than Her work showed of 52 marine in foot species and of form families 300 nearly b), who investigated tenacity, of modes locomotion, speed, 1974a, (Miller locomotion Miller pod by conducted Susanne review of studies gastro below detailed the is derived from 1917;Olmsted 1974b) Miller 3.4). (see Table Much of the which were subsequentlytropods by others modified (e.g., of modes for locomotion different - gas the in terminology study by early (1907) Vlés An provided aclassificationand c 3.10.1 strata). A longer cilium has a faster tip speed, so those with with so those afaster speed, tip has cilium strata). A longer factors (e.g., on environmental and subbeating temperature, (Jones species 1975). small to restricted be to alone appears locomotion using gastropod habitats, cilia terrestrial tion. In of locomo means this use to species larger enabling habitats, aquatic in by foot the is reduced weight the although carried locomotion is relatively species, larger ineffective, in especially branchs’. propulsion muscular to (see Compared below), ciliary fresh-water and ‘pulmonates,’ land tropods, ‘opistho many and e.g., some taxa, large in some naticids, in neogas- occurs also but of most locomotion gastropods, tiny in is seen type This 2011), rapid gliding. and uniform, asmooth, produce they and control (e.g., neurosecretory nervous and/or under be to Jékely thought and coordinated highly which are cilia, action of pedal (Salvini-Plawen 1968b; Scheltema & Jebb 1994). amonorail to likened been which has mucusa thick strand, action along moves by ciliary animal the Section 3.8.2) and Solenogasters have along, narrow, foot (see reduced c 3.10.2 The speed of locomotion depends on the rate of ciliary of of ciliary rate locomotion on the speed depends The entirely due be the to can some gastropods in Locomotion U Gast I ncluding ili shell ili sing ropod a a ry ry A C

a a nd nd L reeping M A e a rr ping uscul h yt mantle F periostraca ri hm oot a m groove r L ic S oco L ole oco l m otion m otion

, , 16, 16, , 101 - - - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 II. Ciliary I. Muscular (Miller 1974b). locomotion non-ciliary with most buccinoideans than area shell). For example, have amuch foot Nassariidae larger the below) having a broader,in longer foot the (longer than waves muscular use that those (see from differ means is necessary. speed greater waves muscular uses some neogastropods, (see below) when ilr S.L., Miller, Sources: could transport weights of 4 g/cm could transport of(1922) Polinices duplicata cilia pedal the that calculated example, 1974b). Copeland (Miller foot unit area per For locomotion have weight foot large a very the sole spreads that employing gastropods large ciliary other and species This tuberosa long heavy Cassis and 30 cm nearly power such the as tory some gastropods large in locomo molluscssized (and main animals), it the other is also (Jones cilia 1975). shorter with those than move (as taxa) will cilia aquatic many faster in long pedal Gastropoda and in Polyplacophora Modes Locomotory Muscular and Higher and Classification Occurrences Taxon of Ciliary 3.4 TABLE 102 b. Arrhythmic c. Leaping a. Rhythmic Non-heterobranch gastropods that move that Non-heterobranch gastropods by ciliary While ciliary locomotion is employed ciliary by small- many While iii. Composite ii. Indistinct ii. Ditaxic i. Distinct TerminatingDistinct i. Waves i. Monotaxic 3. Discontinuous Type 2 2. Discontinuous Type I 1. Continuous 2. Discontinuous Type 2 2. Direct 1. Retrograde 2. Direct 1. Retrograde l. Continuous Royal Soc.Interface,11,20140205,2014. al.,J. Plawen, L.v. Sarsia , 31,105–126,1968a;Kuroda, S.et b. Diagonal b. Diagonal a. Transverse a. Transverse J. MolluscanStud.,41,233–261,1974b;Salvini- (Cassididae) 1974b). (Miller Solenogastres, Caenogastropoda, Caenogastropoda Caenogastropoda Caenogastropoda Caenogastropoda Caenogastropoda Caenogastropoda Caenogastropoda Caenogastropoda Patellogastropoda (backward), Caenogastropoda Patellogastropoda (forward), Caenogastropoda, Heterobranchia Caenogastropoda, Heterobranchia Polyplacophora, Vetigastropoda, 2 Heterobranchia Vetigastropoda, Caenogastropoda Vetigastropoda, Caenogastropoda Neritimorpha , although this species, like like species, this , although - by pedal wavesby pedal (see below). Many ­ move gastropods some primitive chitons and that ­interesting thus alone. action moved first they It is likely that cilial with predators. below) Xenophoridae –see Stromboidea and in avoid to a leaping movement way a seen different in (but that from foot effecting their thrash can Nassariidae, caenogastropod 17 (mostly Conidae). considerably vary within Foot can shape have foot broad some can although short, a long, foot narrow havea wide of range shapes; foot and mainly they a sizes below. foot, described as the with ofmode locomotion involves snout of use the the together waves 1974a). pedal specialised (Miller rhythmic A similar, locomotion less efficient is usually than pedal ing, arrhythmic 1974a).shell or even forward (Miller backward Besides leap provide to leverage the substratum the the vigorously to thrust into a lever is thrust operculum foot the when the and twists, 1958c).Xenophoridae (Morton as is modified The operculum 1972, 1974; Field (Crump 1968), 1977), and Struthiolariidae Strombidae (Berg families caenogastropod ofmembers the in of locomotion occurs discontinuous and type latter of this movement form forward is aspecialised shell. of Leaping the for front next at in a point the or anchored attached and ward foot the is brought then for and forward, shell is thrust the muscles. by columellar ward second, of contraction the In the for shell is pulled the as or anchored foot attached the is then and substratum foot onshell the rests the is extended while 1974a, (Miller b):the types two first, main the in There are ment (see above) gait. some adistinctive with pedal in and move indistinct with species in occur can and discontinuous below.Figure 3.35 further is discussed and in is distinguished type leaping behaviour.facilitates This Xenophoroidea Stromboideais found and the only in and 2’locomotion of (the Miller) type discontinuous ‘indistinct waves(as retrograde below). in –see of arrhythmic type One sole where the epithelium elongatessole, areas being these on the anywhere waves terminate and begin can arrhythmic 3.35. These movement cilial with Figure in grouped are waves below, pedal form described that undulations they and regular movements the from pattern-less greatly tinct differ 2locomotion (Table type 1and ous 3.4). type - indis These continuous subdivided or into discontinu was further type waves. waves indistinct with those and The latter terminating 1974a,(Miller b) distinct which with was those into divided footthe sole locomotion arrhythmic –aphenomenon called movements muscular unpredictable of rather show irregular, ably developed independently. these movers Some cilial may movement cilial to alternative have methods motory presum 1997). (Ponder & Lindberg origin paedomorphic assumed of aconsequence their being perhaps action, this by cilial

+ Heterobranchia. Caenogastropoda ftefrtmluc eesal(e hpe 12), it is molluscs first the Chapter were small If (see locomotion, the in such those as Some ciliary with species Species with either type of arrhythmic locomotion have of arrhythmic either with Species type waves movement when the occur sole ofArrhythmic the is of loco types various with of apogastropods The groups Biology and Evolution of the Mollusca of the Evolution and Biology apogastropods 17 move move ------

Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, The Locomotion of Soft-Bodied Animals Soft-Bodied of E.R., The Locomotion from Trueman, wave. modified and Redrawn pedal Patella FIGURE 3.31 adhesive as known locomotion 1980a, method (Denny tory waves mucus conjunction in pedal with –alocomopedal of their properties special the use gastropods and Chitons movement foot ofthe the (see Figure 3.31). parts of other (see Section 3.3.2.1), provides which also anchorage during waves together adhesion with used sole creeping are on the locomotory taxa, many 3.4). In (Table gastropods among locomotion muscular is distributed broadly Rhythmic r 3.10.3 1974b). (Miller viduals movementsindi their ing muchmature in less efficientthan Strombus gigassuch immature as of it over. shell tipping modifications, without these Animals possibilitythe vides awide, flat, stable reduces base which (e.g., Strombidae, Xenophoridae, Distorsio foot a small shell of alarge, broad and with species acteristic Type locomotion, including leaping, is char 2 discontinuous bly Terebridae) 1974a). effective very are (Miller burrowers 1974a). (Miller species other in than shell the strombidsing have than narrower and afoot smaller 1. type The leap with species foot, shell but than abroader had waves) terminating short a broad, locomotion and (arrhythmic nid tively (1974a) foot. broad Miller and short ­ movement) pedal have- have arrhythmic acompara indistinct locomotion. ditaxic retrograde with most taxa be to diverse tends those size to in (wheretropods is seen), most variation relative foot the area preference (seesubstratum Section 3.10.6). also - In caenogas not entirely with are differences correlated these and Conidae, ‘Turridae’ have of do members the foot a shorter, broader than locomotion, of species Terebridae and arrhythmic indistinct have Conoidea example, examined all although clades. For Some species with type 1 discontinuous locomotion 1discontinuous (notaSome type with - species locomotion 1discontinuous (most type with species Those Distorsio anus Distorsio . Note the compression of the haemocoelic spaces and the mucus changing from viscous to fluid state under the raised part of the the of part raised the under fluid to state viscous from mucus changing the and spaces haemocoelic of compression the the . Note a nd h

yt A A diagrammatic representation of the employment of muscles in the formation of a retrograde wave in the patellogastropod wave patellogastropod the in of a retrograde employment formation of of the the muscles in representation A diagrammatic hm d which non- had h ic contrac esion M viscous mucus uscul zone of ting muscles a r L ­leaping type 2 , are unstable on sand, mak on unstable sand, , are oco m otion examined the perso the examined .Te shell pro ). The

discontinuous ­discontinuous pedal muscles dorso-ventral uid mucus ------with thesolemaximallyextended. regions attheirshortest length,andforward movement occurs is shortened. With retrogradewaves, thefootisanchoredby and forward movement occurswhentheremainderoffoot sole beingattachedtothesubstratumatmaximumextension, Thus withdirectwaves, movement isachieved bypartsofthe compression’ (Lissmann1945;Miller1974a; Trueman 1983). ‘waves ofelongation’ anddirectwaves areknown as‘waves of reasons,retrogradewavesthe wave. areknown as For these mencing posteriorlyandcontractionattheanterioredgeof directwaves, theoppositeoccurs,withwave com- In ing andthosebehindstretchingbackward (seeFigure 3.32). foot bytheanteriormuscleswhichformwave contract- end ofthefoot,andwave thenmoves backward alongthe nation ofmusclesactinginconcertwithbloodspaces. either solelybydifferential contractionofmusclesoracombi- alternate oneithersideofthefoot). These waves canbeformed ing horizontallyacrossthefoot)orditaxic(intwo serieswhich maybemonotaxic(wavesas theanimal). extend- The waves direction totheanimal)ordirect (moving inthesamedirection leaping of most the strombids famous being the (see below). assist to ­ is used locomotory operculum the cases, more agile. In a and few foot the is narrow others foot,broad in of movement type the and employed. on a some creep While is aconsiderable of foot there shape variety but gastropods in (e.g., 2005; et al. Iwamoto 2014). Chan et al. modelled mathematically be of locomotion can means that waves muscular the with combined effective avery produces of mucus properties biomechanical 3.3.2.1). The Section relaxed is more fluidpressure that and when pressure (see layer more solid under becomes ofthin mucus. This mucus by a substratum the to footalong the which is connected is achieved by asuccession waves of muscular It moving expensivegetically 1980b; (Denny Tyrakowski 2012). et al. of locomotionThis method effective, is very ener but is also 2005). al. 1981; &Gosline 1980b, 1981; et Chan Denny Retrograde waves begin withtheextension oftheanterior Pedal waves mayberetrograde (moving intheopposite haveChitons foot move abroad and waves, using muscular substratu pedal muscles transverse m

, Edward Arnold, London, UK 1975. UK London, Arnold, , Edward haemocoelic space relaxing muscles zone of

movements, 103 - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 pedal waves. Those gastropods withdirect waves appear to waves hadgreateradherence against shear forcesthanlarge rapidly. ExperimentsbyMiller(1974a)showed these small quickly becausethewaves canbevery smallandcantravel can maintainhightenacityeven whentheanimalismoving (for hightenacity)orlongand narrow. Compression waves smaller andtherangeoffoot shape isrestricted,usuallybroad direct waves (andotherwaves ofcompression)areoftenmuch and these waves are at least one third as long as the foot, while form isassociatedwithalarge rangeoffootsizesandshapes, producing analmostbipedalgait. The retrograde ditaxicwave - the footremainsanchoredwhileothermoves forward – caenogastropod landsnailPomatiaspods. In the , onesideof logastropods, somevetigastropods, andmany caenogastro- (Table 3.4). Retrograde ditaxic pedal waves are seen inpatel- waves while inafew othergastropods thewaves aredirect Stud. S.L., J. Molluscan Miller, from and modified waves rograde Redrawn (wavesin vetigastropods. acceleration of oftwo elongation). methods figures show The lower FIGURE 3.32 104 1 3 DIRECT WAVE 4 2 5 NORMAL SPEED-onewaveoccursonsideoff Chitons andsomegastropods have retrogrademonotaxic

The upper figures show the two main pedal wave patterns in gastropods, direct wavesdirect (wavesin gastropods, compression),of ret waveand pedal patterns twomain the figures show The upper Wa Wa Wa ve travelslengthoffootin10sec ve for at onetime ve isonequar ms in2sec , 41, 233–261, 1974b. contracting ter lengthoff 5mm -2sec wave oot elongating oot Direc tion ofmovemen ger than the shell. the ger than some (e.g., and footlarge area, some trochids) have a foot lon 1974a).shell (Miller waves ditaxic Taxa have direct with a footof the is variable, but none have afoot longer the than (Miller 1974a). then it is unnecessary to increase the speed of contraction so theenergetic costisgreater. Ifthe wavelength isincreased, speed ofcontractionthesolemusculaturemustincrease, thefirstinstance, ing wave velocity orwavelength. In despite reducingtenacity. Speedcanbeincreasedbyincreas- substratum at any one time. Large waves do have advantages, ing asonlyasmallpartofthefootsoleisreleasedfrom the many stylommatophoransandmaybeimportantwhenclimb- (Miller 1974a).Smalldirectwaves are,forexample, seen in can thusachieve greatergrippingpower withasmallerfoot generate waves smallerthanthosewithretrogradewaves and In species with retrograde ditaxic waves shape ditaxic and size the retrograde In species with 4 3 2 5 1 RETROGRADE WAVE RAPID SPEED-onewaveatatimetwiceasfast contracting Method 1 Method 2 elongating t wave Nochangeinwave Nochangeinwavefrequenc Wa Wa elongating Biology and Evolution of the Mollusca of the Evolution and Biology ve frequenc ve -length doubles

y doubles

2 sec 2 - 10mm -length 5mm -1sec y - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 of locomotionforescape,reversing, orclimbing,but fornormal modify the normalpattern.Somespecies use a different pattern tern forforward movement, but, foranincreaseinspeed,itcan Figure 3.35) andhabits.In addition, aspeciesmayuseonepat- (Figure 3.34).monotaxic wave the separate is wave remain they if whereas is ditaxic, (Figure 3.33). waves ditaxic direct with species to whenshapes compared Taxa composite with foot wave and have sizes similar patterns substratum. the to of sole amount out the attached reducing complex,- easily with move to them enabling turn quickly and compositeconsidered the waves most the of cypraeoideans (1974a), by Miller gastropods in observed patterns cular she 1974a, (Miller b). mus- the 14 kinds all Of tion, recognised study her of in ‘prosobranch’ Miller and locomo recognised, be can types these basic Modifications of directions. various few waves such where cowries the as gastropods move can in page. of top the the towardis moving row,top the animal the figures in In the of movement animal. of the show direction the arrows red large the moving, and waves are pedal the that show direction the arrows red (Cypraeoidea). cowries The small waves Composite in found only are gastropods. in Miller, S.L., from modified and row redrawn is bottom the 1 Part M., K. Wilbur, Physiology, and pp. 155–198, A.S.M. lusks, Salauddin, in FIGURE 3.33 Shell, Body, and Muscles and Body, Shell, h typeoflocomotionreflects bothphylogeny (see The shell muscles locomotory foot the the cross, in main the If So-called Direc

waves are less common and seen in a waves in seen and lesscomposite common are The main kinds of pedal wave seen in the gastropod foot. Redrawn and modified from Trueman, E.R., Locomotion in mol Locomotion E.R., from Trueman, modified and foot. Redrawn gastropod wave the in seen of pedal kinds The main t monotaxic Direc t ditaxic J. Exp. Mar. Biol. Ecol. Mar.J. Biol. Exp. C omposite wave - waves. monotaxic have all direct stylommatophorans and diids, waves ‘pulmonates’,monotaxic basal larger the and onchi cilia. use primarily but groups many of wave a variety use neogastropods types, Other gastropods. waves but only ditaxic found some diagonal neo in are types, 1974a). (Miller substratum the to attached firmly usually are and wave stationary at any moment remain a locomotionward sole of is low, the not within parts all and for waves normal rhythmic of during the amplitude The one end foot other. of from the the to bands parallel regular waves pedal only use rhythmic neritimorphs 1974a). Miller 1922; 1919, (Copeland waves speed Olividae, monotaxic use or increase burrow to employed, asisthenumberandsizeofmuscularwaves. forward movement, a single pattern of locomotion is usually Small-sized ‘pulmonates’ use either ciliary movement ‘pulmonates’ orSmall-sized either use ciliary Lower have caenogastropods awide diversity of wave Polyplacophorans, vetigastropods, and patellogastropods, notably Naticidae and gastropods, Some burrowing Retrograde monotaxic s . The Mollusca , 14, 99–156, 1974a. Figure 3.35 distribution See for their , Vol. 4., New York, Press, Academic 1983, Retrograde ditaxic which move in 105 - - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Tübingen, Germany, 1992. Germany, Tübingen, increases itsadhesive capabilities. most surfaces, andthe thinlayerofadhesive pedalgelgreatly sible becausethefootsolecan closelyconformtotheshapeof thin layer of liquidbetween them. Adhesion is generally pos - force holdingtogethertwo closelyappliedsurfaces witha ate anegative pressurewhenpullisexerted. Adhesion isthe 3.26.1). With suction,aspaceisformed under thefoottocre- and tenacity –suctionandadhesion(seealsoSections 3.26 to discourage predators. Two mechanisms are involved in onto rocksaretowithstandwave actionandcurrents Tenacity is important ifchitons,snails,orlimpetsclamping 3.10.4 1974) (Figure 3.36). involve may sometimes that snout the 1974; (Berg Solem of mode progression asimilar Some practise strombids also 1962; Graham Davis 1967). (Fretter & gression (Figure 3.36) a looping foot of mode along the pro practise to with used end snout of of mode the is progression, anterior the In this Pomatiopsidae. and some Assimineidae in and Truncatellidae, 1974a). themselvesrighting (Miller sole of the when any part attach readily can patellogastropods some vetigastropods (e.g.,In contrast, Haliotis foot rest of subsequently.ment applied the the being with - reattach initiate to is used gland) pedal anterior associated 1989 –2September 27 August Tübingen, Congress, Malacological International 10th the of Proceedings Meier-Brook, C. in 83–84, pp. function, from structure and ­ from function Predicting architecture: pedal Gastropod ­ the foot ­ the through sections transverse are right onthe those waves sole, onthe show pedal left the Figures on ditaxic. or taxic mono waves be will pedal the whether determine interactions FIGURE 3.34 Monotaxic pedalwa 106 Ditaxic pedalwave Looping using the foot and snout is seen in species of foot snout species using the in and Looping is seen (with propodium the its caenogastropods, detached In musculature (blue). Redrawn and modified from from (blue).Voltzow, modified and musculature Redrawn J., A d h esion A diagrammatic representation of how ­ shell representation A diagrammatic s ve pedal wave sole of s f muscles oot

pedal a nd T en a city F issurellid andsiphonarii Pa , University of T tellogastropod , Trochus structure structure u showing d bingen, bingen, muscle ) and ) and - - a large proportion of foot area atonce) of foot proportion area a large less probably require waves long adhesion.good In contrast, rhythmic (which move enabling attached, sole muchthe firmly while of it remains waves the because waves move optimal pedal are quickly over rhythmic needed, are tenacity and speed where both Thus, closer and together. smaller typically are they tion because waves ditaxic of retrograde elongahave than tenacity - greater tenacity. wavesand waves Direct other and of compression efficiency, energy speed, between is acompromise pattern of movement method or the tern do not change. forces wave if shearing pat against tenacity without affecting increase can speed narrow-footed taxa, rather those least in pods pods vetigastro trochoidean the with stationary, but experiments is achieved is usually animal only tenacity when the imum role. play presumably also important glands an tion of pedal distribu and nature the and factors such musculature as Other adhesion. for maximum substratum the tightly against clamped be shell can shell of so the length the the slightlyand less than foot is for broad tenacity high feet. The optimal narrow with those feet broad have with to tend species than higher tenacity motion (including leaping) have low very tenacity. Similarly, loco action or discontinuous ciliary with tionary, those while locomotionmuscular have tenacity, high when- sta especially continuous pedal with Those patterns. locomotory the and foot include of size the the taxa between Differences texture. (4)ual; how long and it (5) type is applied; and substratum the (3)moving or stationary; force- the is whether sudden or grad (1) force; dislodging of is the (2) direction animal the whether include: These or limpet. of tenacity asnail the determining atlow was than tide. tide less tenacity athigh mean although low adhesion during tides, used percentage same about the while suction, used limpets of the about tide three-quarters high During height. on tidal depending suction adhesion attachment and Pacific between switched eastern the in limpets found lottiid that 1978). Marsh (Branch & for limpets (1992) other Smith recorded . kg/cm 2.8 (1974a) by Miller recorded tenacity stationary was The highest muscles of the shell. of the to attachment strength exceed the can limpets patellogastropod adhesion in of pedal The strength stationary. remains limpet the that time the with but increases atfirst, is poor tenacity for reattached, Once several minutes. less thanwhencrawling. 3.26.1), thetotalfootareaincontactwithsubstratumis 3.26and in thenatureofsecretedmucus(seeSections although tenacityisgreatlyenhancedbecauseofachange caenogastropods usuallyhave thepropodiumretractedand, clamps itsshelltightlyagainst thesubstratum. Stationary sion is usually attained when an animal stops moving and an active processinvolving muscularaction.Maximumadhe- to 4.8 kg/cm to Patella vulgata Patella The experiments of Miller showed that the optimal wave showed optimal of the Miller that The experiments The requirements for speed and tenacity conflict, and max and conflict, tenacity and for speed The requirements (1974a)Miller investigated factors the experimentally Some patellogastropods, once dislodged, will not reattach reattach not Some once dislodged, will patellogastropods, Tenacity passive adhesion,but is ingastropods isnot just Calliostoma 2 Lottia pelta Lottia for 2 , but figures of as much as 5.2 kg/cm , but figures of with a foot area of 2.9 cm afoot with area and Tegula and Biology and Evolution of the Mollusca of the Evolution and Biology , while Aubin, while (1892) found a that by Miller (1974a) by Miller at imply that, 2 resisted pulls of up of up pulls resisted 2 have been been have - - - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 restricted to species of small or large size. The experiments size. or large The experiments of species to small restricted power, mechanical in but of no locomotion one major is type employed, differ to mechanism expected the be might they is muchtenacity reduced. rapid but waves small, speed, same than energy achieving the FIGURE 3.35 Shell, Body, and Muscles and Body, Shell, 14, +Truncatelloidea. 99–156, =Rissooidea 1974a. Note: Rissooidea Figure 3.33 for See types. key locomotor to Because the modes of modes locomotion considerably the Because differ in

Pedal wave patterns in polyplacophorans and gastropods based mainly on data from Miller, S.L., Miller, from on data mainly based gastropods and polyplacophorans in wavePedal patterns

PA POL H Sacoglossa Siphonarioidea Pyramidelloidea Cephalaspide Aplysiida Acteonoidea Valvatoidea Cancellarioidea Conoidea Pseudolivoidea Olivoidea M Buccinoidea Tonnoidea Haliotoide Trochoidea Systellommatophora Stylommatophora Stromboide N Littorinoide Triphoroidea Epitonioidea Eulimoide Rissooide Cerithioidea Architaenioglosssa Fissurelloide NERITIMORPHA Ellobiida Calyptraeoidea Xenophoroidea Nudipleura Cypraeoide Velutinoidea aticoidea exceeds shell size, tenacity is much reduced. Limpets have Limpets exceeds is much shell size, tenacity reduced. or to but foot if is equal size foot to area, mately proportional due two to be to factors. Tenacity is approxi This appeared of about 1.5 of width foot1.1 between and length/foot 1.5. and wereform for tenacity of length ratios high shell length/foot (1974a) foot byconducted Miller optimal the that determined ygrophila uricoidea TELL YPLA OGASTROPOD C a OPHOR a a a a a a a A A

HETEROBRANCHIA CAENOGASTROPODA VETIGASTROPODA CILIAR CILIAR Y J. Exp. Mar. Biol. Ecol. Mar.J. Biol. Exp. LEAPING Y 107 - , Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 and some (vermetidsand hipponicids) permanently and are Some haveably move to taxa. need between little much locomotion (for below) see alternatives consider differs jet propulsion below (see Section 3.10.9.1). under discussed fastest molluscs the are and are Cephalopods s 3.10.5 submerged whether air. or in surfaces vertical have climbing no difficulty animals, mostTeflon other coated along, with those with flexibletopography compared foot. disadvantageless on complex flexiblemore marked and ata of foot for ideal type clamping is the that experimentally (1974a)Miller moved rapidly clung and tightly. showed Miller by exposed studied habitats most in Thus, species similar. for are both optimal shape foot and the size because degree ahigh to maximised pletely be can compatible, attributes both tion employed tenacity, high not com and for are speed high substratum. the against pulled shell be to allowingthe aperture, the foot than the is smaller by shell (or the pull columellar) if muscles exerted only be can The maximum gastropods. by intertidal limpet-shape many adoption of explain the a part in This may limpets. itto in as not vertical substratum, the to would parallel pull of be the muscles outer edges foot, of much the the must reach to curve shell shell (i.e., muscles. short snails, the in as If, columellar) (1974a)Miller by may increased tenacity be suggested that of adhesion when stationary, strength and greatest by the far New York, 1974. 1962; UK, London, Ecology and Anatomy Functional Their Molluscs: Prosobranch British A.L., Fretter, from Graham, and modified V. and FIGURE 3.36 108 In gastropods, the speed of movement speed In gastropods, pedal the normal with (1974a)Miller unlike gastropods, many that demonstrated of locomo type the shape, foot and and size optimal While T Strombus runc peed Operculum embedded,shelland operculum

atella head-f Looping and utilisation of the snout in locomotion in the caenogastropods Truncatella caenogastropods the in locomotion snout in of the utilisation and Looping

of Snout star Strombus L oot thrustfo oco m ting toex f otion redrawn and modified from from Solem,A.C., modified and redrawn oot rw ards tend snout f oot P osterior f operculum re Snout thrustfo and grippingsubstratum oot dragged Snout ex - - - - embedded. tended (Miller 1974a).(Miller waves pedal rhythmic with of gastropods may typical be 1924).(Crozier & speed of increasing Pilz method this Thus, 11–19has waves monotaxic sole on the direct atany one time than waves, foot whose was steps larger took length greater, mean Calliostoma species, both in speed with linearly of sizes increased steps the steps.of While the of waves frequency and number size the by the and increasing 1.4 mm/sec 1.2 and 2.9 mm/sec, to respectively). They did this about (from astarfish 0.8bled with to contact when made they (1974a) by Miller vetigastropods studied two trochoidean dou of For example, speed the pattern. the without altering speed increase can of others size while wavesthe speeds, atgreater 1974a).(Miller ‘step’ (including discontinuous with leaping) locomotion above), or, afew, in whole the employed be foot can a in waves muscular (see pedal of the frequency and size of the employing is afunction locomotion, taxa speed muscular in (Copeland activity 1919), of ciliary rate the with lated but, avoid predators. quickly for shelter, reach to feeding, toor mates, find to move to need rather Others substratum. ahard to cemented Similar changes occur in a terrestrial slug ( aterrestrial in changes occur Similar waves. of spacing by the the achange in velocity, not and wave in increase of an because mainly probably increases waves. retrograde with those in Waveespecially frequency gastropods, in is common speed in increase an with length Tegula rw fo ards Many species with rhythmic pedal waves pedal merely increase rhythmic with Many species is corre locomotion, speed ciliary with gastropods In rw The Shell Makers. IntroducingThe Shell Mollusks ards and Tegula had a greater wave a greater had wave in frequency. increase An

snout (with direct ditaxic waves) (with ditaxic direct while atany speed, operculum Biology and Evolution of the Mollusca of the Evolution and Biology contac F fo Snout contra and f oot andsnoutmake rw and Strombus and ard toitsbas t withsubstratum oot brought with retrograde ditaxic ditaxic retrograde with ct ed e , John Wiley & Sons, Sons, Wiley & , John . Truncatella Limax , Ray Society, ), which ), which redrawn - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, 37.2 mm/sec ( mm/sec 37.2 Source ofdata: Given also Size Mode and Size. Shell Values and Median Mode Locomotory for by Parsed Speeds Gastropod ofHeat Maximum Map 3.5 TABLE sistently showed higher speeds (Miller 1974a). This is true is true 1974a).sistently showed (Miller speeds higher This waves ditaxic more con direct with those and of speeds, wavesTaxa ditaxic awide exhibited range retrograde with size. of similar for animals attained speeds maximum the continuous locomotion (Table 3.5). of- dis locomotion either type and arrhythmic indistinct than better waves performing generally terminating arrhythmic locomotionmuscular (other leaping), than was slow, with arrhythmic In contrast, 80 mm. exceeded size unless pattern acomposite with well those did as sizes, atlarger performed also ditaxic, wave especially patterns, sizes. Rhythmic all locomotion. ciliary with size similar movers ditaxic ( sized slower leaping use be locomotion, small- that and those than waves ditaxic with of may locomotion. taxa Larger type of the regardless taxa of exceeds other that tenacity their and speeds, waves capable ditaxic with of are fairly taxa high In general, waves. pedal muscular with that than much greater potentially travelled asingle is with contraction distance step, the and musclemellar complex (dorsal-ventral) involved are each in power head-foot the colu because entire and of the dynamic leaping locomotion is Overall, was fastest. Leaping by the far Monotaxi Ditaxi Discontinuous Arrh Le Size median Ciliar Loco Retro Direct Retro Ty Ty I Terminating waves Composite Direct ndistinct apin Miller (1974a)Miller 0.1 from ranging to speeds recorded Direct and retrograde ditaxic patterns were close in patterns ditaxic retrograde and Direct movement consistently wellCiliary was performed over pe pe yt mo y c hmic gr gr 2 1 g tory Mode ad ad c e e s Miller, S.L.,J. MolluscanStud.,41,233–261,1974b. Strombus <15mm Slow < 15 mm) are also slower also of those are 15 mm) than 15–40 mm ihngsrpd Tbe 3.5). (Table gastropods ) within 41–80 mm >80 mm Fast Medians Mode - - posite pattern. which employed waves of compression, acom so had they waves monotaxic direct with found species regularly in also waves. retrograde with those Relativelythan were speeds high waves direct with those movedsize, and significantly faster of species similar in Muricidae Trochidae and the in occur –for example,even taxa types related both distantly between away from predatory starfish (Morton (Morton Ansell 1964; 1967b; starfish away predatory from les long (Cardiidae) foot actively to muscular their use leap Some cock sediment. move the by ploughing through laterally laterally, some shallow-burrowing and bivalves readily can move butrow cannot downward efficiently sediment, the into (Boyle 10 cm/min 1977). around speeds idly move awayand at rock is light when overturned from the live move undersidesthat of can on rocks the relatively rap Some of species Ischnochiton limpet. agastropod like rather (see Chapter 14). slow generally are Chitons crawlers, moving sediment soft in food or burrow either crawl cnidarian on their slow-moving very are Aplacophorans speed. locomotory and not always) (but is often shell and the broad. most foot rapid the moversaction, the in long is atleast as as rely that on ciliary yetlength, locomotion is rapid. In those Strombus –in different locomotion discontinuous with Species (leaping) are reduced. is speed or when foot exceeds maximum shell length length, shell the than foot shorter the becomes As speeds. highest the had shell to length locomotion, afoot with equal those length pedal continuous muscular with species large to medium in 1917; crawlinglocomotion (Parker faster than 1989). Pearce Aplysia hare sea the in galloping from It thus differs gliding. regular faster than edly of progression is not mark ent This method at any one time. 3.37).- may pres be one arch More than of (Figure contact moved new is then body rest of point the the this to forward and It touches but alow behind is formed substratum, arch the forward. thrust and substratum the from is lifted head the of 1989). slug locomotion, method of (Pearce arionid In this atleast one species and snails land some stylommatophoran in moved wavelengths. faster even shorter had many though (1974a) Miller muricids, waves direct with found species that some and trochids among Thus, not equal. usually are tors wave each as would step, forward cause alarger but such fac- longer with waves animal an should move equal, all faster are sole unit per area traction of contraction speed the if In theory, length. 1/3 foot 1/5 to normal the more than wavelengththe not increase did ditaxic, direct with species in foot while the length, half than wavesditaxic awavelength had usually or to greater equal below. discussed of whichboth are its relationship and shell shape foot with size, and and size were wavelength These crawling speed. determining in tant Several factors were Miller identified by (1974a)impor as Scaphopods and many burrowing bivalves burrowing many quickly and Scaphopods bur can is relatively for ‘minor’ classes on the data little There size – shell with relationship its and shape Foot size and intermittently (sometimes galloping)Loping occurs called Wavelength – rapidly moving species with retrograde –rapidly moving retrograde with species which is a distinct type of retrograde of retrograde type which is adistinct the narrow foot is shell 1/2 1/3 to narrow the the + the successive between time waves + con 109 ------

Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 changes experienced by an animal can present problems can for animal bychanges experienced an and variable often topography are and type Substratum t 3.10.6 (e.g., predator the some evenand attacking 1979). Branch away (e.g., 1975), Phillips (e.g., twisting others Bullock 1953), have some well with moving predators been studied other (see scallops Section 3.10.9swimming Chapter 2). and foot morphology.similar bivalves The fastest-moving the are possible be to Neotrigonia in (Ansell 1969), including Gari movements have several bivalve in other observed been taxa 3.38). leaping Similar 1976) &Thompson (Figure Yonge Yonge, and K.M. Wilbur, in pp. 383–423, M., C. Physiology of Mollusca FIGURE 3.38 1979. CA, Molluscs Opisthobranch of Study Comparative the to A Contribution Aplysia: of Biology Behavioral 37–50, 1945 (figures on left),Gray, NewE.R., and York,, Norton, Kandel, in Locomotion 1968J.,right) Animal (figuresreproduced on as FIGURE 3.37 110 The responses of patellogastropod limpets to starfish and starfish to of limpets patellogastropod The responses on h negative stimulus

e

E t h Different modes of locomotion in a terrestrial helicid snail. Redrawn and modified from Lissmann, H. Biol Lissmann, from W. J. Exp. modified and Redrawn snail. helicid aterrestrial in of locomotion modes Different Leaping movement of the cardiid bivalve movement Laevicardium crassum. cardiid ofLeaping the ffect e L oco

of m S otion u bstr (Ansell 1967a), assumed are and (e.g., 1969) Ansell of because

a of tu Creeping gait G m

a a stropods nd T opogr a p h y

ous locomotion and poor tenacity (Miller 1974a). (Miller tenacity ous locomotion poor and To climb discontinu with species are as surfaces, cient hard on smooth leaping movement their with although ineffi strombids are surfaces, hard onciently horizontal and on soft substrata leaping, locomotion ciliary, with or discontinuous move effi waves. Species live arrhythmic use to tend that on both Those waves. pedal rhythmic use waves substrata on hard those and discontinuous locomotion or arrhythmic ciliary use to tend (1974a) on substrata soft living showed conducted taxa that and locomotion. their form influenced (1974a)Miller investigated topography and how substratum plex movements turning. such and climbing as complexity com necessitate can topographical and surfaces provide softsubstrata different very locomotion. and Hard , Vol. 1, New York, Press, Academic 1964. . The experiments that Miller Miller . The experiments that substratum the in Differences by gastropods out on marine work carried Experimental Redrawn and modified from Morton, J.E., Locomotion, Locomotion, J.E., from Morton, modified and Redrawn Galloping gait Biology and Evolution of the Mollusca of the Evolution and Biology , W. Co., Francisco, Freeman & H. San ., 22, - - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Dendronotus iris mud-living the Dendronotus foot nudibranch in is seen (Gonor even 1965).and transport of enlargement the A similar massive the that foot of prey some capture in Naticidae is used suggested It has been on loose for substratum. and/or stability burrowing for foot functions, instance, other serves enlarged for effective necessary propulsion. the This suggests that than locomotion have amuchcies ciliary foot with larger area for not essential effectiveare movement. Similarly, most spe movers, or discontinuous yet foot these shapes ciliary in seen movement pedal have that foot, alarge like arrhythmic tinct exclusively.sediments - Some continuous of indis with those or soft habitats movement substratum mixed inhabit to tend pedal waves arrhythmic continuous indistinct and terminating have both and lowsubstrata tenacity. Taxa arrhythmic with soft with associated caenogastropods and vetigastropods in habitats. sand/rock mixed or sand in locomotion occurred arrhythmic indistinct and waves terminating arrhythmic distinct with species the half Olividae). locomotion and (Naticidae using ciliary Almost primarily of members families are present on substrata soft waves monotaxic with Species mostly on substrata. soft are locomotion discontinuous and ciliary with those while strata, sub on found hard species in mainly are composite patterns below. summarised as which live, they in environment the with strongly correlated (1974a)Miller were showed locomotor different types that c 3.10.7 adhesive foot surface. weight due the to overhanging of surfaces relative area the to or disadvantage on a flexible,vertical very and certainly it is on complex foot the is topography unless ahindrance be can shell A large detached. be to much had angle foot of the area achieve to atonce and even degrees 90 that more than turn selves over complex foot abroad with Species rarely surfaces. proved them most capableerally the be to of manipulating employadhesion. that those firm employed be can forpatterns movement except on sand, for tive wave muscular of wave various locomotory Thus, pattern. - no difficulty, had irrespec substrata hard from others of the neogastropod tor (see tenacities below), the and such patellogastropods as locomo found high with and those live substrata only on hard which of species normally on sand several gastropod speed most (1974a) effectively Miller surfaces. on hard the tested cause slippage.can surfaces smooth surfaces, movement hard climb usually can employing species unable climb. to ciliary While typically foot, are of but the individuals large adhesive part anterior is possible strombids, this only on the movement.mic In - arrhyth indistinct leaping locomotion adoptand an usually discontinuous with species surfaces, hard smooth, vertical, Shell, Body, and Muscles and Body, Shell, Ciliary and discontinuous locomotion are primarily found primarily locomotion discontinuous are and Ciliary and ditaxic, direct retrograde, In relation substratum, the to Topology waves pedal move generally Most muscular with species orrel . Species with arelatively with . Species long, foot gen narrow Nucella a tion manage poorly on sand, whereas most whereas poorly manage on sand,

wit h H ab it a t - - - - -

Denny 1988). Denny (seeby tenacity way also or increased of foot alarger area adhesive strength increased and is reduced, lift so that surface andreductionprojected the of shell, streamlining, or flatter by of dislodgement asmaller reduced be can The risk 2007). 1985; (Denny 1985;snails Nybakken et al. Denny Wright & waves selective agent is probably for important an intertidal exposure. Dislodgement by forces by the generated breaking wave and environments or subtidal preference for intertidal were not tested. motionsumably (e.g., employ ciliary Velutinidae, Triviidae) pre that substrata hard with associated sand-dwellers; taxa movers (1974a) by Miller whose was measured tenacity were ciliary All less restricted. are tenacity intermediate with taxa while on substrata, soft usually tenacity minimal with those over moving dorsally sand shellcilia (see the below). also by is assisted pedal burrowing shell, of and the some or all severalNaticidae, and shelled ‘opisthobranchs’) envelops movers (e.g., burrow that ary Olividae, caenogastropods the 1970).colonies (Robilliard of The foot several of species cili narrow-footed with relatives contrasts and on hydroid living tropod tropod vetigas the - and lottiids atonce.ward The patellogastropod waves,small back foot of moves the entire then but the for Siphonaria limpet panpulmonate marine The wave moving pedal cally alarge with ( several and muricids) neritids, typi planaxids, (littorinids, zones highest the in suchcies in situations most with taxa waves. waves found only afewpedal pedal in are Small spe relativelyshores are fast-moving have ditaxic and rhythmic, sublittoral. the shore or in the continuous locomotion were consistently also found low on - dis other with those leap and that Those sediments. of deep allow for accumulation the wave drainages inland action and found sheltered shores in where are reduced on substrata soft present (oftentaxa Olividae) burrowers. Most usually taxa are on wave-exposed while the dominate, beaches sandy terns ous movers closely and pat monotaxic with species related larger sole size can equate with increased adhesion, improved increased with equate solelarger can size lower, in occur usually tenacity a less exposed zones. While outside for range the high proportions with species while of exposed shores, parts upper on the occur tenacity high for factors. foot with Many species proportions ronmental alowthus tenacity. which have trochids and a long, relatively foot and narrow etc., rocks underneath of hide whichspecies often cypraeids waves narrow with include habitats. Others sublittoral many ( abalone in is seen pattern adhesion. This same increase to foot of the stationary area alarge waves, maintaining thus shores have on exposed living hard direct muricids short Various speed. increase to this foot increase but length, can Haliotis In the lower littoral or sublittoral, ciliary and discontinu and lower ciliary or sublittoral, littoral In the a with of types locomotory some patterns also There are and substrata, foundTaxa on hard are tenacity high with Species in the higher tidal zones of the more exposed of zones the tidal higher the in Species Foot size and shape also show also shape envi with Foot some and size correlation Tegula spp.) live which also exposed lower in and littoral have wavelength anormal of the about l/3 ≥ 1/3 foot length). length). foot 1/3 has initially 111 ------Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 the body, usuallybytheshellvalves beingpartiallyopened. from beingpushed upward bydilationoftheupper partof mayalsobeprevented (Figures 3.39and3.40). The animal the anteriorpart,enabling animaltodraw down onit muscle contraction. This expands thefootdistallyandanchors involving haemocoelicfluidbeingforcedintothefootby hydraulic system is employed, or plunger-shaped foot. A bivalves usuallyhave alaterallycompressedhatchet-shaped and differences in the properties of the sediment. Burrowing ing theshell),physiological, andbehavioural differences, differences betweentaxaresultingfromstructural(includ - 1966), thereare and, whilebasicallysimilar(Trueman et al. 3.40), themovements involve theadductorandfootmuscles hydrostatic pressure. In burrowing bivalves and (Figures 3.39 to effectively and efficiently penetrate the sediment using 1974a).burrowers (Miller Terebridae such effective very the rowing as gastropods are foot length) bur Some monotaxic. other long and (1/3–1/2 being waves in the caenogastropods from other many in seen where close relatives differ they action alone, and have ciliary wavesPedal developed are taxa some caenogastropod in Trevallion 1969), olivid the Agaronia and 3.39), melanoides (Figure Bullia nassariid the naticids (Copeland many such in species larger as 1922)in waves more effective, be to pedal appear especially muscular by lubricated mucus. substratum, the plough through and into can animal the so that body the edges streamline to mantle extensions with sidesshape, often foot the of from the or the into a foot dorsoventrallyplough-the is usually flattened gastropods, In burrowing scaphopods. all in and gastropods, (Scheltema 1998). cies of Neomenia burrow, but some spe 1998). Most solenogasters do not end (Scheltema forward posterior the bring body along the muscle anchor, longitudinal of an bands contraction as the long spicules the with posterior acting hydrostatically and, end (withrior shield) sediment the oral into pushed being the movementstheir slow. are Burrowing is achieved by ante the butCaudofoveate sediment, soft in burrow aplacophorans 3.10.7.1 refuges to more effectively. access may gain individuals possibly smaller species, that both in indicating overall a reduction size in exposed sites than and other tered shel from individuals (2005) found in Pile noand differences Prowse South Australia, in snails study ofrecent two intertidal a more (1974a),always differences occur.In intraspecific microhabitats. found protected in mainly forcies unsuitable foot with effective proportions are tenacity spe other and These microhabitats. sheltered and habitats to low found confined the often only in tion are and zones mucus (see Section 3.3.2.1). locomo arrhythmic with Species pedal of the by properties the increased be also adhesion can 112 In both scaphopods and bivalves the foot is highly adapted action, ciliary use gastropods burrowing many Although many bivalves,in The footfor is modified burrowing some found by Miller patterns the with Despite some generality

Burrowing in Soft Sediments Burrowing in Soft can do so using their protrusible pharynx pharynx protrusible do so using their can (Cyrus et al. 2012). et al. (Cyrus (nel & (Ansell ------sediment liquefaction to facilitate their burrowing. Octopods Octopods burrowing. liquefaction their sediment facilitate to also bivalves, cuttlefishburrow,like and and Octopods use anchorage, followed obtain is to expanded by its retraction. which epipodium foota unique morphology a fringed with 3.2.10). more efficient burial Section (see have Scaphopods preventing in aids back makes slippage that thus and sculpture ‘ratchet’ have gastropods developedand also asymmetrical its into shell (see contracts mal Section 3.8.2). Many bivalves seawaterani and is the foot inflate sinuses to expelled when have system’, ‘aquiferousgastropods an pedal in which takes cavities.mocoelic addition copious to In blood naticid spaces, bivalves include development the gastropods and of hae large molluscs, living in convergent seen someanisms in features is accomplishedbypushingdown withthefoot. pronounced insomewithroundedshells.Upward movement occurinbivalves with elongate shells,but canbe does not traction ofthepedalretractorandprotractormuscles.Rocking be assistedbyarockingmotioncausedthealternatecon- through thesoftenedsedimentbyfoot.Diggingcanalso shell israpidlyclosed(Figure3.40). The shell isthendragged from the mantle cavity intothe surrounding sediment as the Downward movement can alsobefacilitated byajetofwater Biol. J. Exp. E.R., Trueman, from naticid Biol. J. Exp. et al., E.R. from fied Trueman, modi Bivalve and bivalve gastropod. redrawn erodont anaticid and FIGURE 3.39 - mech hydrostatic burrowing muscular Besides similar the expansion and direc contra tion off ct

ion Comparison of the burrowing mechanism in ahet in mechanism burrowing of the Comparison oot Biology and Evolution of the Mollusca of the Evolution and Biology Heterodont bivalve P olinice water o s (Naticidae) w , 48, 663–678, 1968. 663–678, , 48, , 44, 469–492, 1966; 469–492, , 44, direc rotation tion ofshell - - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 cid cid (other patellogastropods) than including hipponi abalone, the exterior. gastropods the with nection limpet-like A few other acon maintains that atube produce they and them, around grows coral rather, the not bore, massivein They do corals. maximum vermetid Ceraesignum large the 15. and Chapters 9 foot (Figure 3.41). on bivalve given More are details in boring side sucker-likeclamping onto the borehole of their the with while shell forth back the and rocksoft or wood by rotating the file teredinids pholadids and Thus, substratum. the rasp to the shell on sculpture file-like use borers mechanical tle, while man the from usingLithophaginae) acidic secretions do this sible substrata. on calcareous dissolution chemical - only pos being twoof mechanisms, the dissolution, or chemical or acombination boring mechanical by either this shells,molluscan or limestone). They achieve coral, such or dead living as substrata calcareous or in rock, Some (wood, bivalves substrata hard into clay, burrow soft 3.10.7.2 sediment. with depression a theyin create cover which to fins themselves andtheir sepiolids and Cuttlefish use jets water mechanism. hydrostatic burrowing a muscular as which function arms, their with sediment themselves softened the into pulling before sediment the liquify to funnel their wateruse from jets Vol. 4., New York, Press, Academic 1983. 1 Part pp. 155–198, K. M.,in mollusks, and Wilbur, Physiology, A.S.M. Locomotion E.R., in Salauddin, from fied Trueman, FIGURE 3.40 Muscles and Body, Shell, A few gastropods, such as the coralliophilid Magilus coralliophilid such the as gastropods, A few mussels such date (the as borers mytilid Chemical Sabia , some siphonariids, and Trimusculus and , some siphonariids, Burrowing Substrata in Hard

Diagrammatic representation (in transverse section) of the mechanisms involved in bivalve burrowing. Redrawn and modi involved and bivalve Redrawn in mechanisms section) burrowing. of the transverse (in representation Diagrammatic substratum transverse protrac muscle retrac muscle muscle mantle cavit f oot to to y r r f oot thrustsdown V alves pressagainst substratum; ligamen t ward live embedded live embedded also construct construct also cavity high pressureinpedalhaemocoelcauses dilation ofterminal water ejec fo A and and adduc rmed insurroundingsubstratum; dduc muscle - - - tor musclescontra to ted frommantlecavit propulsion, and they can also swim by flapping their fins. Fins Fins fins. bytheir swim flapping also propulsion, can they and using jet swim to enable animals wall these mantle muscular coleoids,rapidthe the contractions of more efficiently.In rapidly cavity, expelalso mantle the water from but much cavity. mantle water expelled the being from Cephalopods by rapid closures valves of the aclapping in motion the with by ‘jetting’ (see Section 3.10.7.1). it is achieved In bivalves, most most cephalopods; and bivalves swim cephalopods and bivalves, and some adult in gastropods occurs Swimming s 3.10.9 (Huffard et al.2005). mm/sec) or faster thanthesameindividuals crawling (60 equalto molluscs withobserved ratesof60to140 mm/sec, locomotion isthefastest benthicmode oflocomotioninthe including arm. Walking behaviour alsooccursinafew cuttlefishtaxa, then rolling along the sucker edge of the distal half of the nating theplacementofeacharmonsubstratumand 2006). These octopusesbipedally‘walk’ backward byalter 2005; Huffardtheir arms using a rolling gait (Huffard et al. Some benthicoctopusesmove over sandybottomsontwo of 3.10.8 ular rasping (Lindberg & Dwyer 1983) (Lindberg & rasping ular (see Chapter 9). also involve to appears dissolution- process rad chemical and both The excavation substrata. home site depressions calcareous in r fo ot to B fo (oe &Hochberg 1988). Bipedal Metasepia (Roper wi iped rm ancho ct mm valv shell ; a y; l ing

L e r oco Retractor musclescontract fo m to pullshelldownonto ot andintosubstratu otion m

. The Mollusca 113 - - , Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 closures valves of the aclapping water in motion being the with above, noted As most bivalves in is achieved jetting by rapid 3.10.9.1 buoyant. covers that shell, by is assisted mantle the it neutrally being pseudothecosome the in mucus-feeding by webs.is assisted their Swimming feeding. in and slowly sink and mantles but feeding, Diacria while external 1986). &Harbison Most cavoliniids have reduced (Gilmer flotationabilities their to related be to appear mantle the of part external the in differences pteropods, thecosome In 1986 &Harbison for references details). and (see Gilmer ‘wings’ for of swimming parapodial a pair use all Pteropods when 1985). involvedspeeds (Satterlie prey et al. capture in much to beat higher wing swimming normal change their rapidly can probably and gymnosomes other limacina Clione and shelled thecosomes, on the predators are gymnosomes naked water The of column. members the permanent also are pteropods thecosome and gymnosome The afish. like using body movements efficient are swimmers, and column the in water live permanently Heteropods foot. a modified propulsion. jet with conjunctionin used is often octopuses. swimming Fin finned and some propulsion cuttlefish, squid, and in provide balance 1968. 179–197, Lond. Soc. A.D., Ansell, Malacol. Proc. and from N.B.Nair, modified and movements foot. Redrawn the of the indicate arrows red FIGURE 3.41 114 wmiggsrpd Fgr 3.42) or parapodia use (Figure gastropods Swimming Cavolinia Jet Propulsion, IncludingJet ‘Flight’ Propulsion, has no external mantle, but mantle, flotation no external has Limacina

have complex forand used flotation mantles Burrowing movements of a pholadid bivalve in soft rock. The green arrows show the movements of the shell, while the the show movements while shell, the of arrows the movements bivalve The green of apholadid Burrowing rock. soft in Peraclis reticulata , which has an external external an , which has

muscle play also size arole (e.g., 1971). Gould adductor in shape, and shell changes thickness, in Allometric Pecten in pronounced ferential convexity lower and upper the in valves (particularly dif and shell morphology, streamlining, including thickness, by their determined are of abilities scallops swimming ing event a single (Joll in swimming over 1989). 23 m The vary cover of can and distances capable up 1.6 m/sec to of speeds are they and ribs, by internal strengthened shells are smooth most efficient the thin, are bivalveTheir Ylistrum swimmers. Placopecten a‘zig-zag’in such Amusium as others fashion, while ably. Some such Chlamys as 1981), consider et al. vary abilities swimming their although (Gäde 1978;anaerobically et al. 1978; Grieshaber Livingstone is largely powered swimming their and for periods, short 1983). Morris (Baldwin & By way swim scallops of contrast, phosphate, glycolysis, arginine from contribution ATP and is mostly anaerobic aerobic, forplied asmall with swimming only afew atmost. Physiologically, minutes sup energy the hians Limaria or more), (15 min for such extended as others, periods while fragilis such Limaria as adductor musclelarge which rapidly closes valves. the Limids asingle with bivalves pteriomorphians Most swimming are but no adult bivalves periods, short long-term swimmers. are cavity. mantle expelled the from A few bivalves for swim can are ‘long-range are gliders’. of Species Amusium (Gilmour 1967) (Gilmour for capable of are swimming Biology and Evolution of the Mollusca of the Evolution and Biology ) to generate lift (e.g., lift generate ) to 1991). Hayami (Donovan et al. 2004) can swim swim can 2004) al. (Donovan et can only swim for short distances for only distances swim can short and and and and , 38, - - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, muscles of the mantle wall (seemuscles wall mantle of below) the by much contract as except The thick opening for off the funnel. the by sealing pressure internal builds mantle over The ity and gills. the cavmantle the into Water opening anterior the flows through muscles. mantle ofachieved contraction the apowerful with Donovan (2004). et al. by by its long tentacles, paddling wasand described mantle fragilis Limaria in of swimming mechanics behaviour and U. K. J.E., Assoc. J. Mar.Morton, Biol. New York,Press, 1964; Aplysia –Akera sources FIGURE 3.42 Cephalopods propel themselvesCephalopods using jet propulsion is less but well the understood, limids in Swimming

Morton, J.E., Locomotion, pp. 383–423, in Wilbur, K.M. and Yonge, and K.M. Wilbur, in M., C. Physiology pp. 383–423, of Mollusca J.E., Locomotion, Morton, Limacina Different swimming techniques employed by some heterobranch gastropods. Redrawn and modified from the the following from modified and Redrawn gastropods. employed by heterobranch some techniques swimming Different Ak Aplysia Hex er abr a anchus Biology of Opisthobranch Molluscs T.E., Opisthobranch of Thompson, Biology , 33, 297–312, 1954; Hexabranchus - , pods originates with the funnel, some propulsion fine and funnel, the with originates pods (O’Dor & Webber 1991). Sepia with pared Illex using jet propulsion, squid and, the invertebrates est marine fast the Squid are atspeed. enough force animal propel to the with funnel water action squeezes out narrow of the This 1974) Trueman 1972; no length. with change in Packard & 21 as While most of the propulsion and steering in cephalo in most propulsion of steering the and While 38, 121–133, Lond. Soc. 1968b. Malacol. M., Proc. Edmunds, can achieve maximum speeds of around 1.4 m/sec, of around speeds com achieve can maximum i icmeec Wr 92 ad & Wainwright (Ward 1972; circumference % in Ward , Vol. 1, 1976; Ray Society, UK, London, Limacina at 0.65 m/sec, and Nautilus and m/sec, at0.65 , Vol. 1, Academic at 0.3 m/sec m/sec at0.3 115 - - -

Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Sthenoteuthis pteropusSthenoteuthis 2012), &Gilly and (Benoit-Bird m/sec 30 approaching able briefly swim to latter at ofspeeds adults large the with ‘jumbo squid’,the airborne, capable also of becoming are A few from cement, including acyrenid also fresh-water taxa substratum. shells the to cement their can environment, of bivalves marine mostly the in A number gastropods, and c 3.11.2 its role bivalve in evolution given Chapter 15. are in byssus of the function and and structure on the More details relativeincrease wave to Suchanek 1984). (Witman & energy may evidence strength suggest to byssal that attachment anewfoot byssus. by where secreting it reattaches There is anew to location (usually creep to using the reduced) animal by byssus allowing the byssal the at the gland, released being 1974). conditionsdislodged, if allow (Paine achieved This is if including reattachment byssal threads, their reattaching and capable of are they movement shore along by the detaching (such attached mussels), as remain normally will that species transitory.be flexiblement is usually often and can Even in some bivalves. heterodont - byssal cementation, attach Unlike and for adult pteriomorphians many is important attachment isbivalve lost adults. Byssal many ability in but this larvae, foot the of by in autobranch agland secreted are Byssal threads 3.11.1 afew in used gastropods. is also method (see substratum Chapter 15). The latter the to bivalves byssus using shell their or by their attach cementing for option. bivalves Many, is not an intertidal, this especially 3.10.3), is achieved bythis foot clamping (see Section but chitons, and most gastropods For substratum. on the grip atleast temporary wave-swept the zone require in intertidal fossil by and living molluscs.substratum animals Benthic reviewed the to Bromley Heinberg (2006) and attachment 3.11 ‘Humboldt the and squid’ ( squid’ ( The ‘hooked one hundred. more than schools, in haveswim ‘flying’ observed groups been in of ‘flyingsquid’, called bartrami Ommastrephes water. of above squidthe glide to allow the surface A so- the 1950; O’Dor 2013). et al. and ‘flight’ assist stabilising Fins in up 50 m to for (Heyerdahl distances air the travelling through themselves by propelling out water of predators and the from of species squid escape A few prey capture. in required be movement forward backward, funnel is achieved, such may as By propels the itself backward. pointing animal the so that apredator, escape to forward is directed The funnel funnel. conjunction in used jet with propulsion often the from are and octopuses, andfinned somepropulsion cuttlefish, squid, in and provide Fins fins. balance the with made adjustments are 116 EMNN ATTACHMENT PERMANENT TO THE SUBSTRATUM TO THE B yss e m a ent l A a tion tt a c up to 24.5 m/sec (O’Dor up 24.5 m/sec to 2013). et al. hm ent Dosidicus gigas ), also known as ), as known also Onychoteuthis , which often ) was more difficult to manipulate. to was more difficult bivalves prey cemented because ones, apparently cemented to (1991), out by Harper carried byssate preferred predators (e.g.,pressure Vermeij 1987; experiments 1991). Harper In predation in increase Mesozoic amarked to may related be lid polychaetes,althoughthemechanismsdiffer indetail. actinian andoctocoralcorals,craniidbrachiopods,serpu- occurs inawidevariety ofotherinvertebrates, includingscler attached bytheirfoot(e.g.,Knudsen1991).Cementationalso down acalcareousplateonthesubstratumtowhichthey are dean siliquariids (e.g., this istheonlygastropod groupthatdoessootherthanafew Supertethys (seeChapter 15). formed extensive carbonatereefsalongtheshoresof extinct rudists(LateJurassictotheLateCretaceous), The secondarily detached(e.g.,someoysters andchamids). chamids (Harper1992,1997a,2012).Somemaybecome being foundinspondylids,dimyids,cleidothaerids,andmyo- mechanism ofcementationisratherwidespreadinbivalves, similar periostracum andthesubstratum(Harper1992). A ately, spheruliticcalcitecementisthendepositedbetweenthe its initialattachment(e.g.,Cranfield1975). Almostimmedi- using atannedmucopolysaccharidesecretedbythefootfor Yonge 1960b;Stenzel1971),withthesettlingoyster juvenile (Pruvot-Fol 1937). substratum cements its shell the to ?Truncatelloidea) Yangtze the from apparently River, China, Helicostoa fresh-water snail caenogastropod poorly very small known Also a Hoeh 2000). sels (Bogan & evolvedcementation has fresh-water in atleast mus twice - Pseudomulleria Mycetopodidae and the Madagascar) in and (from Africa ans, ans, Sulawesi (Bogan & Bouchet 1998), genera of unionoide three the energy needs scaling with increases in body size, velocity, body in increases with scaling needs energy the 2008). 2005; et al. Hooper Thuma its (Hooper & regulation basis of for and molecular gated contraction the insights into physiological investi muscles molluscan being studies, are focus for morphological over and Besides detailed 150 years. have diverse distinctive and both and a research been are tems physiologicalsome of their Molluscan muscle features. sys- of luscs,muscle and below wecells briefly the outline structure Chapter 5.in bivalves which with mass), lackdealt a buccal are these and (except mass set buccal of muscles the with is associated in shell(s). the with itsfoot, interaction and important Another siderably class head- from class, to the to related but is usually system con The muscular varies mesoderm. the derived from system, which muscular is body main the with Here we deal 3.12 An increase in cementing bivalve cementing Early in the in increase taxa An Most vermetid gastropods cementtothesubstratum,but Oysters arethebestknown cementingbivalves (e.g., Movement action with always nearly muscular requires muscle systemsBefore main found mol atthe in looking Acostaea Helicostoa mentionedabove, althoughhipponicidslay MUSCLES AND THE MUSCLE SYSTEMS (from Columbia, South America), Etheria and (from India) in the Unionidae, indicating that that (from Unionidae, indicating India) the in Stephopoma) and the supposed truncatelloi - Biology and Evolution of the Mollusca of the Evolution and Biology (Helicostoidae, (Helicostoidae, - - - - -

Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 a fibre. Redrawn and modified from Physiol. and modified Twarog,B.M., J.a fibre. Gen. Redrawn FIGURE 3.43 variation presentinmolluscanmuscle. Two classification (Table 3.6).Lophotrochozoa the among distributed broadly whichobliquely are striated, transversely and (or –smooth, types striated, crossed) three (e.g., Heyer 1973; et al. Silva & Hodgson 1987). invaginations plasma membrane and tubules ous intracellular vari muscle through sections the (Figure 3.43) cells are that Section 3.12.3.6) 1996). et al. muscle (Paniagua heart and opaque white catch muscle the in of bivalve (see adductors for example, atalow contraction ing required, as cost, energy maintain in important be Paramyosin may 2007). also Rhaesa extend myosin and the stabilise thought to filaments (Schmidt- is and invertebrates among Paramyosin is distributed broadly ­ and layering gives wide that of range diameters fibrethis the is by alayerwhich is surrounded of myosin molecules. It is ­ filaments muscles,luscan thick of core the the mol muscles. most vertebrate in seen In all that than ordered is less organisation filament thin and thick their and cells, gate of composed elon unicellular, muscles.molluscan They are of (1983) biochemistry Chantler and structure the described 3.12.1 of muscle physiologythis aspect Chapter 2. in is outlined efficient for for their and sources muscles crucial work, are oxygen and Energy demand. energy not the if main, main, the work one muscular of represents for animals, as other many foot. for Thus, the molluscs, etc., particularly and heart, gut, of the parts many and mass, buccal head, mantle, cles the in mus with - mass, body of for the proportion accounts a large 1983a), et al. (Hochachka molluscs, most other in it and also – e.g., component mass cant body of the over 60 Muscle amounts. tissue occupies small asignifi require mals of energy, slow-moving amounts large small, and require ani of mode movement.and Generally, fast-moving large animals Shell, Body, and Muscles and Body, Shell, These distinctions are an over-simplification of the actual into divided generally muscleInvertebrate are cells ‘vesicles’ also of sections are in seen be can that There produces fibresproduces those much of longerthan vertebrates. M uscle

Representative molluscan muscle fibres in each of the three main muscle types. Each diagram represents a small portion of portion a small represents diagram Each types. muscle main three the each of in muscle fibres molluscan Representative

C ell bre (e

M Tr ansversely striatedhear orp . g h ., Achatina ology andSepia lamen lamen vesicle dense body thick thin t ) in % in t t paramyosin paramyosin Octopus Obliquely striatedfast (e adduc . g ., Cr ------, 50, 157–169, 1967. 50, ,

tor bre assostrea ponents ofmolluscanmuscle.It issummarisedasfollows. and Amsellem (1983)andinvolved scalingsixindividual com- of aclassificationmuscletypes was developed byNicaise cell isrelatedtoanaspectofmusclefunction. Another example covary,do not necessarily and each component of the muscle based ontheZ-linesorbodiesandtheiralignment. All features Traditional schemesclassifyingmuscle types wereprimarily and smoothmusclescanbeseenusingalightmicroscope. gross featuressuchasthedifference betweenstriatedmuscles which relyonfinerscale TEMmicrographs,althoughthe systems of molluscan muscle are outlined below, both of • • • • • •

) 2 mμ periphery. cell the to is restricted reticulum sarcoplasmic the myoplasm, where the extending into tem R2, and sys tubule reticulum - asarcoplasmic to connected Golgi of apparatus) are the part are that discs brane (flattened mem cisternae where subsarcolemmal (thecolemma muscle of the membrane cell cell), R1 condition sar of the the ‘R’ –describes parameter system invertebrates (Nicaise & Amsellem 1983). the cell)andisonlysuperficiallysimilarto T brane intothemyoplasm(thecontractileportionof penetration oftubular infoldingsoftheplasmamem- ‘T’ parameter–describesthreecategories ofthe not distinguished. are cell the within location mitochondria of the the in Differences packages (M3). in (M2), section orTEM arranged (M1), rare from of plane a the present in generally ranging of‘M’ mitochondria organisation –the ­feature readilymeasuredin TEM micrographs. ‘F’ parameter–diameterofthethickfilaments,a (Voltzow filaments of the 1994). the length because of TEM using to measure difficult is parameter of speed).indicator contraction This ‘L’ filaments thick of length (an the –the parameter muscle. smooth in seen of bodies dense arrangement muscle, random Z5, to the cross-striated in as Z-bands, continuous with Z1 from –ranges ‘Z’ parameter lamen lamen dense body thick vesicl

thin e t t from adduc Smooth catchmuscle bre tor (e . g. , Mytilus

) - - 117 Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 muscle. Parallel structuresareseenin brachiopodadductor ated musclesandtheopaque partoftwo typesofsmooth tor muscleofTridacna crocea consistedofobliquelystri- Kuga (1989)reportedthatthetranslucent partoftheadduc- the performance(Voltzow Matsunoand 1994).For example, ent kindsofmusclecellsso the mixofmusclesdetermines sion increases. ten sustained maintain to ability but the decreases, speed contraction the smooth, to of along striated ing agradient When movcell.the in filaments of number contractile the to of muscle of contraction the speed is linked cell The muscles. molluscan found all muscles in are and striated vertebrate in or Z-discs equivalent Z-line of the functional the are The latter bodies. dense and of Z-discs organisation ultrastructural due the to striations the in differences with 1983), & Amsellem belowcategories discussed (Nicaise reveals amuch more complex just three the situation than 1983). of muscle molluscan cells ultrastructure the Thus &Amsellem of muscles molluscan features (Nicaise variable and two most of interesting the are parameters R by Tand the described reticulum sarcoplasmic of the 1983). Amsellem (Nicaise & parameters muscles four six of diagonal in retractor, shell, the and differ Lymnaea, gastropod heterobranch the in whereas ( pod), 2–4 2( between vary can ple, Zparameter the For exam taxa. within and between differ parameters These 118 Importantly, asingle muscle mass may comprise differ elaborations and sarcolemma of the The invaginations Achatina , gastropod), and 5( , gastropod), and Distribution of the Three Main Muscle Types Muscle Main Lophotrochozoa Three in the of the Distribution 3.6 TABLE cmd-hea A., Schmidt-Rhaesa, Source ofdata: Note: Cycliophora Micrognathozoa Rotifera Acanthocephala Entoprocta Bryozoa Gnathostomulida Gastrotricha Platyhelminthes Nemertea Sipuncula Annelida Echiura Mollusca Phoronida Brachiopoda Taxon ⚫ = Predominant, ⚪ = Present. University Press,2007. Rossia Venus Smooth , bivalve), bivalve), , , cephalo the head head the ⚪ ⚪ ⚪ ⚪ ⚪ ⚫ ⚪ ⚪ ⚫ ⚪ ⚪ The Evolution of OrganThe Evolution Systems, Oxford, UK, Oxford - - - - - brachiopod brachiopod of adductors the anterior muscleSmooth catch the from cells by (Plesch 1977). availability calcium ation is determined of relax speed the while of number mitochondria, the to the endurance and area unit per filaments thick and of thin The force by muscle number exerted the the to is related cell 1996). et al. (Paniagua arrangement their in order little ing showfilaments thin and thick the with similar superficially myofilaments, thicker having morein and but is otherwise of vertebrates that muscle from smooth Invertebrate differs nucleus. acentral with fusiform are The cells arthropods. but is absent from animals, other many and chiopods, found molluscs, in - bra type Smooth muscle main is the 3.12.1.1 (1996). ing accountislargely basedonthereview byPaniagua et al. - The follow three mainmuscletypes,asseeninFigure 3.43. in intercellularcollagen(Frescura &Hodgson1990,1992). Haliotis, andSiphonaria–have smoothmuscleunusuallyrich 1992). The shell musclesoflimpet-like gastropods –patellids, &Hodgson lar musclesofarangegastropods (Frescura other bivalves 1993)andinthecolumel- (e.g.,Matsuno et al. smooth musclesarereportedfromadductorofmost &Matsuno1988;James1997).Only muscle types(Kuga chiopods have adductorswithsmoothandobliquelystriated both smoothandtransverse muscletypes,whilelingulidbra- muscles wherearticulatedtaxahave adductormuscleswith Transverse (orcrossed) Most treatments of molluscan muscles categorise them into

Smooth Muscle Cells Muscle Smooth ⚪ ⚪ ⚪ ⚪ ⚪ ⚪ ⚪ ⚪ ⚪ ⚪ ⚪ Lingula unguis Biology and Evolution of the Mollusca of the Evolution and Biology range between 45 and 60 nm in in 45 between 60 nm range and Oblique ⚪ ⚪ ⚪ ⚪ ⚪ ⚪ ⚫ ⚪ ⚫ ⚪ ⚪ ⚪ - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, (Matsuno 1987). (Matsuno filaments small ment (or dense of the anchor the that bodies Z) arrange and densitythe myofilaments and thick ofeter the diam on the mainly based found molluscs. in been They are muscle fied smooth intotypes at least (A–D), four have which (e.g., species same the in Plesch 1977). (1987) Matsuno classi muscle different between but species, systems also between bodies. these to attach filaments The thin aligned. regionswhen are these seen Z-lines the by (or dense cated than rather bodies, Z) indi myofilamentsare between Regions of cross-linking tropomyosin. associated with filaments wide actin 6 nm are myofilaments 1974). Odense muscle The thin (Morrison & being broader, in bivalve at least filaments thicker adductor myofilaments,withthose thick of the thickness the to related et al.adductor muscles 1996). (Paniagua is The cell diameter bivalve in 125 and 231 nm to of snails stylommatophoran muscle columellar the in nm 37 to 25 around from range et al. 1982; Kuga & 1988). Matsuno of Widths myofilaments about 108 mm and width Terebratalia in length in • • • • only morphology of muscles smooth not varies The striated. a lightmicroscope,thistypeof muscleappearstobe ently uncommoninmolluscs. In cross sectionsusing tropods and caenogastropods, but is otherwise appar muscles associatedwiththebuccal mass invetigas- mantle retractormusclesofcephalopods andinsome notably annelids,andoccursinthesiphonal of muscleisfoundinseveral groupsofinvertebrates, two typesofmuscle(Paniagua et al. 1996). This type cle, anditappearstobeintermediatebetweenthese them a similar appearance to obliquely striated mus- and more regularly arranged (Matsuno 1987), giving diameter, andthedensebodiesaresmall,numerous, D typecellshave thickmyofilaments of14–40 nm (Matsuno 1987). theadductormusclesofseveral bivalves from typeofmuscle cell hasbeenreported This andfew,(diameter 60–120 nm) but large, Z-bodies. C type cellhaseven thicker myofilaments The 1987).Hodgson Typewhile (Silva & metapodium Bis found the in Typethe propodium, is found the only A muscle in foot Bullia caenogastropod of the In the Z-bodies. arranged irregularly nm) larger and about 40 eter having myofilaments thicker in type (diam A the from differs and molluscs echinoderms many ing and includ invertebrates is found- various in type The B invertebrates. some other 2012) al. 1987; (Matsuno from and tropods et Lee footadductor and muscle of a few bivalves- gas and the from recorded but been of has vertebrates, cal of muscle smooth is typi This type Z-bodies. dense arranged afew are irregularly there 14 nm and than myofilament is less thick diameter the A, type In (Eshleman (Eshleman - - - , - - - - located nucleus, and as in other striated muscles, there are muscles, are there striated nucleus, other located in as and muscles, have they transversely striated asingle centrally and smooth ateither end cell. Like of the mitochondria large (Figure 3.44), have they sarcomeres and afew arranged cally muscle heli myofilamentsare the cells, striated In obliquely 3.12.1.3 1996). et al. nents (Paniagua compo of tubules transverse reticulum sarcoplasmic the nect they myofilaments,andcon the to parallel running tubules sinuous component comprises longitudinal component. The transverse dyads the comprising forming Z-lines the join in vesicles and tubules reticulum The sarcoplasmic membrane. invaginations plasma of T-tubules as the are originate that muscles. Some striated tubules vertebrate in seen that to ilar system ‘sarcotubular’ component sim the to longitudinal and less developed, Although reticulum. mic is atransverse there vesicles and tubules with - of sarcoplas plaques intermingled attachment filament up of made thin bodies electron-dense verification. however, ultrastructural needs muscle, was which ‘remarkable’. noted they This observation, muscles fibres were ofcolumellar exceptthe composed striped (1962: 614) (Vetigastropoda) ascissurellid in that all commented muscle not been has found ‘prosobranchs’. in Graham and Fretter 1996). Interestingly, by noted Voltzow as (1994), striated typical et al. adductor muscle in muscle (Paniagua than heart in dant et al. 1996).(Paniagua In bivalves, more abun are mitochondria muscle bivalve heart in eter in adductor muscles 24–29 nm and from diam in ranging 20 nm to 17 filaments thick with aments, by musclefil is 10–12 thin surrounded in striated filament thick 1989). &Satterlie (e.g., gastropods heterobranch Each Huang (e.g., heart the foot Plesch and of 1977), some retractors, radular muscles of of bivalves, many some bivalves, in hearts and the in nucleus. adductor single muscles found central the in These are 1996). et al. muscles, smooth have cells Like these a (Paniagua muscles either obliquely as or smooth striated transverse striated of interpretation incorrect an in resulted sometimes has this poorly defined, are sarcomeres patches. the Because tron-dense consisting of multiple elec- small appearance, in discontinuous are which Z-lines its poorly in defined arthropods and brates muscle ofskeletal verte striated muscle, the from but differs etc. (seeZ-lines, above). closely This most resembles vertebrate A-bands, I-bands, of distinct arrays into organised ments are - fila thin muscle, and thick the or cross-striated In transverse 3.12.1.2 width. tion is directly related to the cell length, filament length,and their morphological characteristics, as the speed of contrac- of Neopilina galatheaeretractors (1959) Wingstrand and muscle radular the in striated reported &Schaefer 1997). Lemche monoplacophorans (Haszprunar Reynolds 1994) and found polyplacophorans (Eernisse & in only type the be to Smooth muscle have cells reported been The Z-band in transverse muscle transverse of is in composed multiple The Z-band functionofthesmoothmusclecellsisregulated by The Transverse Striated Cells Muscle Oblique Striated CellsOblique Muscle . 119 ------Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 composed of actin, like those in other muscle other in types. those like ofcomposed actin, byered myosinare 1979), (Elliot filaments thin the while cov core of a paramyosin comprised are filaments The thick 1996). et al. (Paniagua adductor muscle up 60 nm to be can in somebut nm, bivalve 20–30 around is usually filaments in filament thick havebeeneach for observed filaments thin nine although filaments, by 12molluscs thin is surrounded each systems Lymnaea in of several muscle bivalves various in and brachiopods and adductor of muscles the part translucent the in common be to was shown later muscle and where itpods, type, is adominant 1996). et al. (Paniagua its own has each characteristics although chaetognaths, and annelids, some pelagic tunicates, notably adductor muscles,groups, brachiopod nematodes, several invertebrate in muscleObliquely other occurs striated muscle smooth helical or, (1983). by cephalopods, Chantler in muscle striated spiral of called muscle been also type has this cell, the through spiral sarcomeres the cell. Because of the axis the longitudinal with aligned myofilamentsthe remain fibres, of the coiling of the because oblique Z-lines the to are instead but are not perpendicular, The myofilaments Z-lines. by delimited myofilamentssarcomeres thin forming and thick Histopathol. Cytol. J. Submicrosc. E.S., Garcia-Blanco, and R. González-Santander, from fied modi and Redrawn of muscle acoleoid cell cephalopod. striated 3.44 FIGURE 120 endoplasmic reticulum apparatus The thick filaments are fusiform in shape, and in many in and in shape, fusiform are filaments thick The cephalo in muscleObliquelydescribed was first striated Lymnaea nucleus Golgi , 11, 181–201, 1996. (Plesch 1977). The maximum width of width thick maximum (Plesch 1977). The

A diagrammatic representation of an obliquely of an representation diagrammatic A Histol. Histol. et al., , 4, R. 233–245, 1972; Paniagua, (see Paniagua et al. 1996 et al. (see for Paniagua references). elec mitochondria tron- body lamen A band H band I band thick dense t tubule - - - of thetransversely striatedmuscle(Paniagua et al. 1996). with theobliquesystemequivalent tothetransverse component that inmolluscantransversely striatedmuscledescribedabove, (Paniagua et al. 1996). The sarcotubular systemisvery similar to in thesemusclesbeingwronglyinterpretedassmooth & Kuga 1989), which has sometimes resulted ous (Matsuno Z-lines inmolluscanobliquelystriatedmusclearediscontinu- Kier 2016). & responsible for contractilevelocity adjustments (Shaffer ties, andonlyalterationofsarcomeric ultrastructureappears isoforms involved intheadjustmentofcontractileveloci- and octopodshave failed toidentifymuscle-specificmyosin Schachat 2008). Transcriptome studiesofcoleoids,cuttlefish, with different myofilamentproteins being expressed (Kier & contractile performancerelatetobiochemicalmodifications, where musclestructureisrelatively similarandvariances in in performancecontrastswiththesituationvertebrates, tion ofdifferent structuralattributes toprovide differences - Schachat 2008). The evolu pattern is less obvious (Kier & for theincreasedcontractionspeed,changeinstriation While thechangeinmyofilamentlengthappearstoaccount Schachat2008andreferencestherein). try issimilar(Kier & pared with those in the arms, although the muscle biochemis- and have muchshortermyofilaments andsarcomerescom- tentacles, thetransverse muscleshave moreelementsinseries fibre, but arestaggered,formingahelicalalignment.In the The myofilaments arearrangedparalleltothelongaxisof cally) striatedandhaving relatively longthickfilaments. muscular systems in cephalopods, being obliquely (i.e., heli- decabrachian coleoids are like those known in most other the widermiddlelayer(Boneet al. 1981;Milligan et al. 1997). mitochondria and better blood supply than the smaller cells in inner andouterlayersarecomprisedoflarger cells,withmore cuttlefish andsquid containstwo maintypes offibres. Thin muscleofthemantlewall of in theirattributes. The circular striated (Boneet al. 1995),but therearesignificantdifferences sarcomere. each within centrally grouped be to tend mitochondria the vertebrates, Chapter 2). in Also, 1994) (Hochachka metabolism fats for (see their than rather acids amino and on carbohydrates rely they tebrates, mainly (e.g.,of vertebrates 1981). et al. Mommsen most ver Unlike muscles striated the lels and have them between made been powerfully, quickly and contract to paral them enabling and Bullia foot muscle propodial of the in muscle recorded been has oblique of and forms helical striated the between mediate 1989).Satterlie inter be to which appears variation, Another & (Huang reticulum by sarcoplasmic surrounded partially pseudosarcomeres) which I-bands, are A-bands with and (called units sarcomere-like small form bodies dense The molluscs. other in those from differs Clione some pteropod theco muscle the of in cell pseudostriated type egories. A Some striated musclesabovethe into neatly do not fit Some striated cat As in the transversely striated muscle of molluscs, the The ultrastructure ofthearmtransverse musclefibresof The ultrastructure squidandcuttlefish,allmantlemusclesareobliquely In obliquely muscles typically Cephalopod striated, are (a (Silva & caenogastropod) Hodgson 1987). Biology and Evolution of the Mollusca of the Evolution and Biology - - - - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Relaxation of the muscle occurswhenCa tated byenergy releasedfrom ATP bymyosin ATPase activity. ate force,allowing isfacili- contractiontobegin. This process the actinfilament. Theserapidly cycling cross-bridgesgener on themyosinheadformingcross-bridgeswhichbindwith way ofmyosinlightchainkinase. The calcium ionsactdirectly to stimulatephosphorylationofthelightchainmyosinby 18 (Ca myosin control of ATPase activity. cells, calcium ions In these rapidly cycling cross-bridgestogenerateforce. This involves calcium ions binding directlyto the myosinhead and then molluscs andotherinvertebrates, contraction is initiatedwith molluscs. in found are (see Box 3.1). of muscle kinds contraction two main At least of muscle is complex contraction chemistry The underlying 3.12.2 Muscles and Body, Shell, involved (e.g., Yamada 2013). et al. involved muscle in play contraction, enzymes arole the in directly Magnesium ions, not although relaxation occurs. itis released activates muscle when removed and contraction lum) of calcium ions. concentration calcium controls the When ofactivity (Bagshaw contraction 1993). for regulatory essential the sites ions, are these calcium and muscle,two myosin molluscan striated binds specifically 2013). myosin the to vertebrate in Yamada et al. In contrast muscles including squid muscle 2012; (e.g., &Kier Shaffer for example, demonstrated, some molluscan in been has worked muscles,been out on vertebrate myosin ATPase head mostthe physiological While of have filament. details actin myosin each its in way ratcheting head along the This results ATPase, an ing myosin ATPase) head phosphate. and ADP to by energy hydrolysis mechanical into verted of ATP (involv molecule con that being in energy chemical the in resulting is powered byThis process myosin ATP each to binding head ‘heads’ the to bind myosin of then sitesing the can molecules. uncovered. myofilament These are - bind exposed actin on the of sites tropomyosin, binding so the structure the alters then 2008), and et al. (Tanaka troponin protein the to cium binds The cal sarcomere. the into reticulum sarcoplasmic the from molecules. For contraction pumped ions occur, to calcium are (tropomyosin) covers myosin the sites actin of binding the protein a filaments, thin system. the On regulatory linked muscle smooth actin- in having seen an in that from markedly muscle some muscles, molluscan in differs and and striated tained withlow energy utilisation(seeSection 3.12.2.1). phase withlow calciumandwherecontractioncanbemain- with vertebrate smooth muscle, thereisalsoasustained‘catch’ reticulum and/orbysimilarpumpsintheplasmamembrane. As the musclecellbyCa phorylation ofthemyosin.Calciumionsareremoved from and myosinphosphataseisreleased,whichinhibitsthedephos- A calcium-binding messenger protein. messenger A calcium-binding In the first type of contraction, typical of smooth muscle in firsttypeofcontraction,typicalsmoothmusclein In the The sarcoplasmic reticulum (a reticulum The sarcoplasmic of form endoplasmic reticu of is found vertebrate contraction in type second The 2+ ) initiatecontractionbytheirinteractionwithcalmodulin M et ab olis m

of 2+ C ATPase pumpinthesarcoplasmic ontr a ction 2+ ionsareremoved 18 - - - - -

an increase in intracellular Ca intracellular in increase an muscle. catch can by Stimulation acholinergic nervecauses 19 century (see Baylisscentury 1927 for review). early an for known over been has a energy.using little This property for while contraction of long very time periods maintaining muscles bivalve in and byssus muscles, in retractor is unusual of bivalve white part dense the cle, adductor in such occurs as over contraction long Molluscan mus catch - periods. maintain contraction), using low latter low the and calcium to energy traction) or may exhibit slow, (tonic contraction sustained Smooth muscle rapidly relax (phasic and may con contract 3.12.2.1 traction, and the subsequent decrease in Ca in subsequent the decrease and traction, myosin (2–10:1 in are longvery that mass) filaments thick and 2005; et al. Butler & Siegman 2010).ments (Funabara - fila thin the from detach tethers twitchin the and twitchin activates phosphorylation of A. This enzyme kinase protein activation and of cAMP in increase causing an stimulated, are released Catch is whenserotonergic nerves filaments. thin and thick the which tethers actin myosin, and twitchin, is athree-way complex stage, there between ments. At this - fila actin the myosin from the with detaching cross-bridges ensues, catch is reduced concentration calcium intracellular andbutas phasic muscleproceeds, filaments contraction thin the from Myosin twitchin displace cross-bridges actin to is dephosphorylated. twitchin offormation and cross-bridges muscle activates the the and in muscle, cell increases calcium follows: as proceeds catch of on the stimulation The process of phosphorylation state the of and twitchin. bridges actin to of myosin attachment the cross- on both based iscatch thus dephosphorylation. with Regulating its occurs uncoupling on phosphorylation,anddepends filaments thin the to ing 2005; Butler & Siegman 2010). extremely slow levels calcium et al. and low are (Funabara cross-bridge ofcycling ATPrate and the phase, is utilisation catch the During levelthe decreases. calcium of intracellular when allows and force catch maintained ylates be to twitchin phosphatase. This dephosphor activates acalcium-dependent Aplysia and way. scallops much same in in the occurs also Projectin functions projectin, protein, adifferent insects in while todes, Siegman 2010).(Butler & Twitchin- nema in known is also twitchin called connectin, and titin to similar aprotein to of is or phase, catch attributed phase contraction, tained sus- levels. baseline near to which is quickly reduced This nervecell the in calcium in increase atemporary with occurs (see 2005) et al. Figure 3.46). (Funabara muscle the in cell cAMP accumulating is released, serotonin until tension Catch state. catch is maintained the initiates

See Chapters 2and 7. Chapters See Both cholinergic and serotonergic cholinergicBoth and nerves The catch muscle has a high proportion of to paramyosin muscle proportion ahigh has The catch but- bind filaments, Twitchin thin and thick both to binds Activation muscle of aserotonergic the nerve by stimulating by and cholinergic nervestimulation is initiated Catch (Benian et al. 1996). et al. (Benian Catch Muscle and TwitchinCatch and Muscle 2+ which results in phasic which in con results 19 2+ control mollus control concentration concentration 121 - - - -

Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 122 4.0 International. FIGURE 3.45 thin filaments are composed composed of are filaments thin composed of elongate filaments thick complex and The of ofproteins. bundles thin comprised are and cells oflength the actively elements elongate by and ( contractile passively. conferred are properties contractile Their multinucleate cells. Muscle elongate comprises very muscle be vertebrates contract can cells in and skeletal striated while generally, muscles invertebrate although have animals in single nuclei properties and Muscle functions have cells similar dense protein, the Z-material (or Z-bodies Z-material the protein, dense of bands dark by of thin muscle. molluscan accounts is delimited in used sarcomere Each are muscle, terms same the ‘striated’.called muscle is no alignment. In smooth there cells of muscletype that cell is and be myofibrilsstriped, theto muscle the upin across cell, it appears lined are sarcomeres elongate an and ‘tail’. fully contracted, and the two Z-lines (discs) two Z-lines the closer and pulled together (Figure 3.44). contracted, are fully muscle when the is disappearing and narrower becoming H-band where overlap. they the sarcomere in the This results thealong middle of the pulled are filaments myosin toward filaments The actin concept. filament sliding the as known filaments Figure 3.45).(see actin the musclewhen it the not contain and does is relaxed, filaments. A narrow, paler H-band actin and myosin thicker the both filaments contains A-band the darker slightly is the sarcomere of The remainder filaments. actin the which I-bands, contain pale the are relaxedin a state muscle probableZ-lines the the to related the fibre. tension is thus within Abutting Z-material the I-band the across titin protein giant the Z-bodies by the to attached are filaments Some details of the morphology of each sarcomere are provided here, and, although largely based on vertebrate largely on although vertebrate provided based here, and, are morphology of of the sarcomere each Some details ( subunits intorepeated organised are The filaments When the muscle contracts, the actin and myosin filaments do not change length, but slide past each other – this is this – but each other past length, myosinslide and do not change filaments actin muscle the the contracts, When

A diagrammatic representation of the sliding filament model of muscle contraction. Creative Commons Attribution Attribution Commons Creative model of musclecontraction. filament sliding of the representation A diagrammatic and the actin filaments cross-linked with titin in the Z-line via the protein α protein the via Z-line the in titin with cross-linked filaments actin the and BOX 3.1 actin THE STRUCTURE AND FUNCTION OF MUSCLE CELLS OF MUSCLE FUNCTION AND STRUCTURE THE and the thicker filaments of filaments thicker the and or dense or bodies sarcomeres ), which is arranged in Z-lines in ), which is arranged (or linked myosin connectin),being the with filaments myosin – the contractile units) myofibril. contractile alongthe the –the If . Each myosin. Each ‘head’ molecule a globular has Biology and Evolution of the Mollusca of the Evolution and Biology lies in the centre of A-band each centre the in lies (or of Z-discs). types Both -actinin. The structure of The structure -actinin. myofibrils ) that run the the run ) that which which Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 The simultaneous stimulation of muscle smooth stimulation by simultaneous both The β and contraction, ferent α receptors; relaxation of muscle smooth and constriction dif via both fibres cells. Sympathetic cause the between space the into vesiclesof vesicles) membrane-bound (neurotransmitter 21 20 attachment viadesmosomes (2) junctionswithwidergaps andnobasallamina,(3) seen inotheranimals. These are:(1)gap-junctions (nexus) junctions) occurinmolluscsandaregenerallysimilartothose Chapter 2). –see control (either or paracrine autocrine by humoral autoregulation or local nerves, or intrinsically 2), muscles other or factors (see humoral or other Chapter 1983). Twarog muscle 1973; nerveand/or of the (Nicaise cells Muneoka & contents, may play ionic arole regulation the granular in which cells, but have these certain, is not connections glio-interstitial the of significance tissue. The interstitial Muscle fibres (cells)to nerve, muscle,connect andglio- 3.12.2.2 above,noted muscles. is not found paramyosin vertebrate in 2005). As et al. tensions high very (Funabara able stand to being plays paramyosin that gested filaments thick arole the in catch muscles, itBecause in is sug most it abundant been has tension muscle the which with develop. the can correlates and tissues, and on species depending 2005). Its content varies et al. myosin muscles invertebrate (Funabara is found all in - found molluscs, para in others of although muscle is unlike (25–100 nm) (diameter thick very 20–100 nm). and This type Motil. Cell Res. J. Muscle et al., D. Funabara, from modified and muscle. Redrawn FIGURE 3.46 Shell, Body, and Muscles and Body, Shell,

other. each to cells adhere to serve that structures protein are Desmosomes cells. between communication allow that connections ( junctions  Gap tension Smooth muscle contraction is initiated by release the Smooth muscle is initiated contraction Three kindsofmuscle-musclejunctions(ormyomuscular extrinsically,Muscles controlled be or by can hormones twitchin phosphor relax ed Muscle Activation and Control Activation and Muscle

ylated , 26, 455–460, 2005. 455–460, , 26, nexus or septate junction) are intercellular cytoplasmic cytoplasmic intercellular are junction) septate or = nexus Schematic representation of the contraction of catch of catch contraction of the representation Schematic acetylcholine ac tiv Ca adrenergic receptors cause relaxation. receptors adrenergic adrenergic receptors primarily cause primarily receptors adrenergic

e

2+

t

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n s

21 i o

(Nicaise & Amsellem 1983). n catc phosphor hr ylated ylation oftwitchin

phosphory serotonin elax ed late d

20 2+ - - , Ca many molluscan and other invertebrate muscles. invertebrate other and molluscan many byssusrior muscle retractor of Mytilus ante of the neuromodulators and multiple neurotransmitters et al. (Muneoka 1991). or neuromodulators ters The control by involved muscle be also neurotransmit as this regulating in (e.g.,monoamines may peptides and octopamine) dopamine, respectively. serotonin, acetylcholine and being Various other nerves these from released neurotransmitters principal the muscle with this innervate nerves relaxing excitatory and byssus muscle anterior retractor is the tem of Mytilus vous control of muscles complex. is often 1983). ner the that means This diversity of neurotransmitters Twarog (Muneoka & FMRFamide and serotonin, dopamine, ACh, such than glutamate, as other employ neurotransmitters junctions animals). neuromuscular Many molluscan other molluscs in (and occurs of also ions. reactions This sequence muscle of the tial fibrean outflowrestored is by potassium of poten close, to resting channels the sodium and allowing the junction down ACh neuromuscular the the in breaking ase acetylcholinester by enzyme the is terminated This process (see Section 3.12.2).cium ionstroponin with which interact releasethe of cal fibre, activate to the in stimulating diffuse also Chapter 6). also (Butler & phase catch Siegman the 2010)alone initiates (see tion of muscle, smooth aserotonergic nerveimpulse while serotonergiccholinergic and nerves causes a phasic contrac channels that ACh allows that ions and channels opens sodium (Na a clustertransmembrane contains of muscle fibre.This area vesicles on ACh the membrane discharge to onto aspecial acetylcholine (ACh). contain typically A nerve causes impulse vesicles many nervecontains of the which part The terminal muscle cause the and contract. to (cell) where terminate they (action muscle the to neuron potentials) fibre the from pass skeletal muscles vertebrate nerveimpulses ation in is that situ junctions. The typical neuromuscular in ending nerves from initiated muscle are of contractions synapse. Striated junction (orromuscular myoneural junction) is akind and iour, and retraction of a body part away from tactile stimuli. away stimuli. ofiour, tactile part a body from retraction and including locomotion, actions, reproductive feeding behav ofdeveloped. functions avariety muscles Retractor perform is well retraction and manipulation where pedal gastropods bivalves robust burrowing in in are and They responses. retraction out various muscles foot retractor carry The 3.12.3.1 categories oflook other muscles. atsome and of these aplacophorans),and eye extraocular muscles. and Below we muscles,gut adductor muscles, muscles enrolling (in chitons (including shell muscles), the ture muscles, retractor mantle dorsoventral muscula - musculature, buccal the musculature, wall body the Wanninger (2000). and are These Haszprunar muscle molluscs in Eight by systems main were recognised s 3.12.3 An exampleAn of awell-studied muscle molluscan sys- The point where a nerve and muscle connect is the neu muscle where is the anerve and connect The point

Retractor Muscles Retractor o m e M uscul a r S yste m s

in appears to be typical of typical be to appears M olluscs . Both . Both + ) to to ) 123 ------Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 25, 332–352, 1975. 332–352, 25, FIGURE 3.47 to theshellsheetsofmusclesattachedconnective tissue. luscan muscular systems ranging from pairs of muscles attached body, but thesamefunctionalarrangementiscommoninmol- opposing sets ofmusclesattachedtobonesinthevertebrate iscommonlyappliedto cle cellscanonlycontract). This term their originalsizeandshapeaftercontraction(becausemus- leastofwhichisforcing(stretching)musclesbackto not the inavariety ofways, acting inoppositedirections. They work These aresetsofmuscleswhichwork against eachotherby 3.12.3.2 head. of the muscles retractors large retractor such the as muscles. retractor bivalves in tors pedal derived from are 1989), (Wabnitz 1975). retractors penis and - The byssal retrac &Satterlie 1974), al. (Huang retractors wing pteropod et 1980), &Roberts muscles withdrawal (Carew gill (Dorsett (Plesch 1977), retractors on head retractors those buccal include gastropods in structure onSome their studies of the 124 The complex muscleThe complex includessystem also of cephalopods

Antagonistic Muscles Antagonistic

Major muscle systems in the hygrophilan Lymnaea stagnalis hygrophilan Major the muscle in systems Longitudinal muscle system tentacle Circular musclesystem

Horizontal foot muscle system (Figure 3.47). 1975) al. layer inner muscles ofan longitudinal (Plesch et muscle, layerof amiddle circular of muscles, diagonal and Lymnaea hygrophilan the 1994). In muscles longitudinal (Voltzow muscles inner and of circular consists butouter layer well of usually an studied, not been has gastropods in musculature of wall body details The responsible lack afoot. for movement body animals these as caudofoveates the is musculature body the shape.body In muscles, muscles, wall body These along maintain the with Solenogastres. in two extra bands ventral an with body the of length of the muscle bands fouraplacophorans thick run ferent –for groups classes example, shell-less of both the in 2008). al. Variations exist dif in et (Haszprunar body the muscles.longitudinal dorsoventral In addition, fibres stabilise inner and diagonal, luscs consists medial of outer circular, found most mol in musculature body molluscan This basic 3.12.3.3 Neth. J. Zool. Neth. Plesch, from et al., B. modified and . Redrawn cephalopeda cephalopeda sinus sinus Body WallBody Musculature fo ot l l Diagonal musclesystem Biology and Evolution of the Mollusca of the Evolution and Biology there is an outer layer is an there

Columellar muscle system - - , Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, arcid arcid comparativelybut developed are weakly autobranch the in foot the of bivalves present in protobranch also 1937), (Heath for details).Chapter 16 Well-developed muscles are circular 1997) Steiner (see (Shimek & musculature pedal of the bulk up the muscles make muscles that of radial longitudinal and outer layer muscles, blocks the inside of which are circular over thepedalgroove (Hoffmann 1949). muscle fibresfromeithersideofthebodycrossandintersperse to thepedalgroove (Thiele1894).In retractor muscles extend from the lateral sides of the body muscularised, however, oblique the rudimentary foot is not thin andlackinginsubstantive musculature.In solenogasters it. Unlike thesituationinchitons,innerpartofsoleis outer partisthickened andtheshellmusclesareembeddedin lar musclesrunningaroundthecircumferenceoffoot,this 1959; Wingstrand 1985),wherethereisanouterlayerofcircu- Wingstrand (Lemche & rans hasbeendescribedinNeopilina musculatureinmonoplacopho- The foot (Wingstrand 1985). muscles (Figure3.49)comprisingmuchofthatcomplexity even theplesiomorphicstateishighlycomplex withtheshell but omorphic arrangementseeninchitons(seeSection 3.8.2), The molluscan footishighlymodifiedfromtheassumedplesi- 3.12.3.4 coleoid (see in seen cephalopods Section 3.12.3.8.2). 1975) (Figure 3.47) Helix and Lymnaea panpulmonates of those the are pods complex of the descriptions gastro in head-foot musculature dependent system (Voltzow 1994). Two most of detailed the hydrostat asolid being amore to fluid- muscular from ranging of fluid spaces, shows relativeand the in importance variation however, not, ahydrostaticdoes as organ, primarily function hydrostat (Voltzow muscular nistic foot 1994). The gastropod antago muscle an combined as functions this and angles, right at are bundles of fibresfibres these with foot.of Interspersed the (if part present) operculum dorsal the to the and/or attached also columella. shell It is on the the to shell musclethe attaches and muscle muscle layer. is outer circular of snails The columellar sole the to no epithelium. There is connective tissue just internal in connections to radiate and diameter in smaller are tarsos the connective tissue,in fibres in but bound the bundles packed in (Voltzow‘tarsos’ 1985, muscles the 1986, are 1994). In both, muscle ventral columellar the dorsal and –the sections distinct entirely of muscle almost two into divided posed be which can Voltzow 1994 for review). foot is com the of asnail In general, afew (see in studied taxa only been has structure muscular nal inter well externally,although studied surprisingly, detailed the below is brieflydescribed Section 3.12.3.8.1).(see (Shigeno complex their arms et al. and musculature 2008) the Brown 1985).as modified foot In cephalopods the is markedly only obliquehas dorsoventral and muscle(Trueman & fibres 2012), al. foot the tellinoidean of while the et Park The column-like foot in scaphopods is surrounded by an by an is surrounded foot scaphopods in The column-like most developed muscles wall body molluscs in are The In gastropods, the highly muscular foot flexible is very muscular highly and the In gastropods, Tegillarca Foot (Pedal) Musculature and the venerid Gomphina the and (Trappmann 1916) (Trappmann (Figure 3.51). Proneomenia , retractor (Lee et al. 2007; et al. (Lee (Plesch et al. al. (Plesch et Donax - - - -

lid lid phasianel the scissurellids, haliotids, patellogastropods, the least someoftheseareprobablynot molluscs (seeChapter13). reported tohave onlyasinglepairofmusclescars.However, at molluscan ancestors(thesmallshellyfossils)whichhave been pods. This is incontrasttotheconditionearliestsupposed to singlepairormuscle,asincephalopodsandgastro- reduction or, possibly, fusionof muscles, ultimatelyleading shell muscles are plesiomorphic (Figure 3.50) with apomorphic (seescars Chapter 17). some fossilalthough nautiloid shells have multiple muscle have of dorsoventral shell two muscles pairs Nautilus does as muscles. of dorsoventral oblique Scaphopods and pedal pairs have protobranchs living and up seven to scars cle attachment (see Section 3.12.3.6andChapter 15). muscles arenew structuresnecessitatedbythetwo-part shell dorsoventral andobliquepedalmuscles,while theadductor bivalves, theplesiomorphicshellmusclesare groups. In taxa althoughtherearedifferent patternsoflossindifferent shell musclesarethoughttobehomologousinconchiferan dorsoventral and obliquemuscleswhichmake upthe The 3.49). pairs ofcompositeshellattachmentmuscles(Figure Both polyplacophoransandmonoplacophoranshave uptoeight 3.12.3.5 3.48). and (Figures 3.34 muscle rightpedal blocks and the left from fibres spersed waves havechitons, inter pedal which all and monotaxic (Caenogastropoda), Siphonaria and [such(Vetigastropoda), fissurellids as limpets kinds of other with monoplacophorans. in This contrasts as muscle pedal blocks, right lateral and the left fibresbetween waves, crossing ofhave was pedal muscle little there ditaxic the existence ofsuchfolds:(1)that they weredepositedby Kat (1984),whonotedtwo additionalhypotheses to explain were reviewed in‘turritelliform’ gastropods bySignorand other ideas have also been advanced. These columellar folds increase the surface areafor the attachmentof that muscle, but columella (Figure 3.51) which,insome,bearsfoldsthoughtto 1997). (Ponder & Lindberg groups four main the in independently it probably has gastropods, arisen within phenomenon Given of them. this distribution the through ing divided shellby muscles superficially blood - pass sinuses are Lepetelloidea) in the Lepetellidae and some Cocculinoidea, 1997).may by explained (Ponder & Lindberg be heterochrony Velutinidae caenogastropod the Rissoellidae) Triviidae and and shell (such muscles heterobranchs in of paired as instances muscle, muscle (Figures columellar 3.51 the 3.52). and The few heterobranchs), is asingle shell there dorsoventral attachment (i.e.,but most others in and vetigastropods, caenogastropods, Some gastropods have ofSome shell muscles, gastropods apair including Thus, in living molluscs, it may seem that multiple,paired bivalves such Pojetaia as The earliest Voltzow (1988) which limpets, patellogastropod in that noted n coiledgastropods, theshellmuscleisattachedto In Neritimorpha, (Patellogastropoda, some gastropods, In Tricolia

(Marcus & Marcus 1960), Marcus most neritimorphs, and (Marcus & Shell Muscles Shell (Heterobranchia)] and have multiple mus have multiple Crepidula 125 - - - ,

Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 pods, theirutility maydiffer acrosstaxa. have certainlyarisen independently in several groups of gastro- and,givenof columellarfoldsisstillnot understood thatthey cies withandwithoutfolds. Thus, the functionalsignificance foundnosignificant differences betweenspe- the shell.She muscle and the columella, and the depth of attachment inside and length of attachment, the total area of contact between the in taxawithandwithoutcolumellarfolds. These werethearea (2003) investigated fourparameters ofthecolumellarmuscle were highlycorrelatedwithburrowing tall-spiredtaxa.Price rejected allthreeofthesehypotheses. They also notedthatthey siphonal notchintheaperture.Basedontheirobservations, they an enlarged, foldedmantle,and(2)thatthey wererelatedtoa Evol. Syst. Zool. G., Z. Haszprunar, from modified and Bivalvia. and Redrawn (Patellogastropoda) Gastropoda Polyplacophora, Solenogastres, in cords nerve main the and rectum, and intestine FIGURE 3.48 126 and dorso fused transverse muscles

Diagrammatic transverse sections showing the relationship between shell muscles shell (i.e., muscles) dorsoventral between the relationship blue), (in showing the sections transverse Diagrammatic dorso -ventral muscle -ventral dorso transverse muscle muscle -ventral transverse muscle Gastropoda-P f oot Bivalvia- Solenogastres atellogastropoda Pr otobranchia shell , 27, 1–7, 1989a. cuticle withspicules pedal ner superior re subrec commissur subrec lateral ne latera ner cord and dorso gut fused transverse ve tal commissure f lateral ne oot l ve cord muscles tal commissure f ct oot cord In some extinct nautiloids withconicalshellsthere were In some of shell muscles in bivalves, gastropods, and cephalopods. oblique protractor(Figure 3.52). anterior andposterioroblique retractorsandasingleanterior autobranch bivalves whichoftenhave onlyasinglepairof of muscleshas been reduced in Driscoll 1964). The number shell musclesandusuallythreeposteriorpairs(Heath1937; 1998). Protobranchbivalves have multiplepairsofanterior are divided intopairedanteriorandposteriorgroups(Waller upper partoftheshellinterior, whileinmostbivalves, they appear as a circular or horseshoe-shaped grouping around the rv e al -ventral e cord There are paralleltrendsinthe reductioninthenumber There are rostroconchs,theputativeIn extinct footretractormuscles rv e transverse muscl

ligamen Bivalvia- P t olyplacophor e Monoplac Biology and Evolution of the Mollusca of the Evolution and Biology Au tobranchia a ophor shell plate a dorso- valv shell f oot muscle e ner girdle ventral pedal ve cord Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, animals as diverse as various crustaceans, brachiopods, and and brachiopods, crustaceans, diverse as various as animals 10),shell’ bivalved present in (Waller 1998, are they as p. of a bivalved requirement Adductor muscles a‘functional are bivalve in transformations many evolution (see Chapter 15). (see gastropods Chapter 20).heterobranch pendently evolved Bivalvia in bivalved the in and sacoglossan molluscs have they inde abivalvedin been shell. In living valvesAdductor the muscles muscles pull the together that are 3.12.3.6 gous (see for overview Chapter 8 an ontogeny). of their (Jones 1961). was apairofmusclesdorsallyand asingleventral muscle someCretaceousammonites,there retractor muscles.In two pairsofscarsfortheattachment ofthedorsoventral bands forattachmentofthebodyandmantlemuscles These consist oftwo continuous chamber (Mutvei 1957). cle attachmentareas,allintheposteriorpartofbody pair asincoleoids.Fossil nautiloidshave threemainmus- been reducedtotwo pairs(asinliving Nautilus)orasingle whichmayhave multiple shellmuscles(seeChapter 17), Report Galathea Monoplacophora. of Recent Relationships and Anatomy K.G., the On FIGURE 3.49 h adult adductor muscles of bivalves have undergone The homolo shell muscles not necessarily Adult are larval and

Adductor Muscles Adductor

Comparison of the shell and foot musculature of a monoplacophoran and a chiton. Redrawn and modified from Wingstrand, Wingstrand, from modified and Redrawn achiton. and of amonoplacophoran foot musculature and shell of the Comparison muscle pedal retrac post-apoph ysial to r muscle pedal retrac pre -apoph ysia to r l - - are given inChapter 5. ment andfunctioning ofthebuccal and odontophoralmuscles because ofthemyoglobinthey contain.Detailsofthe arrange- In feeders, but are lacking in suspension-feeders (autobranchs). present inprotobranchs(Heath 1937)sincethey are deposit muscles, large buccal muscles,andpalpmusculatureare of thelackaradula,althoughmultiplepairsmouth Bivalves have lesscomplexity thanothermolluscsbecause ula) comprisethemostcomplex setofmusclesinthebody. cal cavity, andtheodontophoralapparatus (includingtherad- musclesinvolved inthemovement ofthemouth,buc- The 3.12.3.7 catch muscle(e.g.,seeSection 3.12.2.1). interest inthediversity ofmusclefibres,especiallythesmooth many ultrastructuralandphysiological studies,inpartthrough above adductor muscle. posterior the (Waller adults as 1998),myarian always rectum lies the and ontogeny. bivalve even All mono if dimyarian, juveniles are adductor muscle developsin first The anterior rostroconchs. extinct bivalved the the group bivalved but not gastropods, muscle longitudinal lateral The adductor musclesofbivalvesThe adductor have beenthesubjectof ­radula-bearing groups,these musclesareusuallyred

Odontophoral Muscles Odontophoral , 16: 1–94., 1985. muscle transverse muscle oblique 127 - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 brieflybe review can below. these structures on details More systems of coleoid (e.g., cephalopods 1988), Kier which we 2009b) (see Chapter 5). (Golding caenogastropods et al. of proboscis certain is the as Bivalvestats. siphons example agood (see are Chapter 15) hydro muscular several are systems molluscan There are that 3.12.3.8 muscles. retractor cephalic the blue muscle indicates The dark 2002a. FIGURE 3.50 128 Among the most specialised are the muscular hydrostat muscular the are most specialised the Among Systems in Coleoids in Systems Hydrostatic Muscular Specialised

The main muscles in molluscs. Redrawn and modified from Wanninger, A. and Haszprunar, G., J. Morphol. Haszprunar, and from A. Wanninger, modified and Redrawn molluscs. muscles in The main ‘worm-like’ bodywallmusculature Monoplacophor Solenogastr P Pr Au Caudof C Or Pa Scaphopoda olyplacophor ephalopoda otobranchi tellogastropoda thogastropoda tobranchi oveata adult cephalicretractorspresent es a a a a - ( ) muscular hydrostat (Kier 1985, hydrostat (Kier muscular 1988). outer layer An of a as functions musculature arm 3.12.3.8.4). The Section 3.53), suckers (see bear typically they and (Figure ers a complex in of of laycomposed muscleseries arranged entirely tentacles of and almost coleoids are arms The 3.12.3.8.1 tentacles.and arms and fins, found Chapter 17. in include muscles mantle, These the the in number ofsetsadultdorso-ventralmuscles

Arms and Tentacles and Arms Biology and Evolution of the Mollusca of the Evolution and Biology (1-2) (3-8) (1) (8) (1) (1) (2) (∞) (8) (∞) , 254, 53–64, 53–64, , 254, - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 Shell, Body, and Muscles and Body, Shell, Boletzky & Boletzky 1970; Huffard et al. 2005). The paired 1970; Boletzky Boletzky & 2005). et al. The paired Huffard Messenger 1996) (e.g., even and burying sepiolids, & involved be can (Hanlon locomotion in or signalling muscle smaller. mass relatively are bundles transverse the longitudinal and larger Nautilus of muscle. transverse of the centre The cirri the through run artery an and nervecord bundles. The axial longitudinal the extending between and other each to angles at right running muscle of core fibres transverse a thick the with surround muscles of of bundles longitudinal that ring athick encases of muscle sheath oblique muscle thin layers. This relatively musclelongitudinal by is underlaid connective tissue and FIGURE 3.51 The arms are used in feeding and mating, and sometimes sometimes and mating, and feeding in used are The arms are comprised of similar layers of of muscles, similar comprised but the are tentacle anterior retrac tentacle anterior ocular tentacle Musculature of Helix of pomatia Musculature ja buccal cavit to retrac w r upper ventralbuccal y protrac buccal levatormuscle te anterior tentacle d ocular tentacle anterior tentacle retrac Muscles in the shellremoved(otherthanasmallpar levator muscle ex buccal mass tor muscle ternal labial Dorsal viewofmusclesin tor muscle retrac ocular tentacle radular sac Helix pomatia,seeninlongitudinalsec tor muscle mantle collar buccal retrac penis retrac oesophagus . Redrawn and modified from Trappmann, Zool. wiss. from Trappmann, W., Z. modified and . Redrawn head muscles buccal retrac muscles Helix pomatia,withthedorsalwallandshellremoved. tor muscle to ner r ring ve pedal retrac to

muscles r retrac lung ocular tentacle pedal retrac t ofthecolumella).Odontophorenotshown. investigated system the of movement It is only some detail. in have Recent studies ‘limbs’ animals. other in more so than Schachat 2008).(Kier & severalmusclesin arm differ and waysthe from modified tentacles are the but in those arms, the support and bend tentacles. probably Very and homologous, similar, muscles ily responsible rapid remarkably extension for this of the prey. muscles primar the are grasps and ers The transverse suck tentacles of has the part Leeuwen 1997). The terminal (Kier & tentacles rapidly extending very (about 20–40 ms) pealei capable ofare rapid very extension. squid Doryteuthis In the only forand used prey capture are tentacles of decabrachians muscles tor muscle to The arms of octopuses are extremely of are octopuses flexible arms – much The r tion fromthele , this involves the eight arms flaring open and the twothe and open involves, this flaring eight the arms to r fo ot fo ot sole ft sideofthebodywith cephalopeda cut bodywall haemocoel columella muscle dorso columella of shell horizonta -ventral r mantle longitudina l , 115, 489–585, 1916. diaphrag columella

columella l muscle of shell l m muscles r pedal 129 - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 luscan muscle,pp. 211–252,in Trueman, E.R.and Clarke, M.R.,Form andFunction. FIGURE 3.53 178, 1976. 365–384, The Mollusca K. M., Wilbur, A. in pp. 155–198,S. M. Salauddin & in mollusks, Locomotion E.R., from Trueman, modified and FIGURE 3.52 130 , Vol. 4, New York, Press, Academic 1983, Bullia and

Details ofthe musculature of anarm of Comparison of the main shell and foot musculature in a heterodont bivalve and a gastropod ( bivalve agastropod a heterodont and in foot musculature and shell main of the Comparison separating longitudinal trabeculae (thinsheets of radialmuscle br transverse muscle axial ner Bivalv Bullia transverse oblique muscle muscle) muscles (= obliqueretrac pedal retrac internal ar anterior pedal ve cor e te f oot pedal retrac ry tor muscle d muscles es longitudinal muscle adduc anterior tor) muscle connective tissue tor to sheath ex (= obliqueprotrac Octopus. Redrawn and modified from Kier, W.M., The arrangement and­ r ternal obliquemuscle protrac pedal dorso oblique muscl anterior pedal retrac median tor muscle tor muscles longitudinal circumf muscle -ventral redrawn and modified from Trueman, E.R. and A.C., Brown, E.R. Zool. J. from Trueman, modified and redrawn e tor) erential muscle

pedal longitudinal columella muscles muscle (= obliqueretrac The Mollusca, Vol. 11, Academic Press,New York, 1988. retrac posterior pedal suckers tor muscle operculum r ridge

Biology and Evolution of the Mollusca of the Evolution and Biology posterior adduc f oot tor) muscle

siphon to connective epidermi tissue and r vein dermal muscl s e s Bullia Physiology, Part 1 Part Physiology, ). Bivalve redrawn function of mol- . , Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 radial musclesofthemantleandmusculaturecollar In has animportantroleinrespirationwhentheanimalisatrest. do not (Trueman & Packard 1968). mantle also The pulsating lopods thatutilisepowerful jetpropulsionthaninthosethat 1985).Demont elastic helping rebound expel to their water (Gosline & the with cavity muscles fills, mantle when the contract radial the when stretch that muscles others and circular of the traction of conon collagen are fibresstretched consists that of some The complexarrangement bicin slow fibres used swimming. layer slow-twitch, inner outer and of mitochondria-rich aero an and zone ofin fastjetting fibreschondria-poor twitch used layer muscles mito The thick consists of of circular acentral fast glycogenic twitch, jetting. during fibres,contracting rigid arrangementindecabrachians. movement ofthemantlethanispossibleinmuchmore inoctopodsenablesgreaterflexibility and The arrangement also provide afirminsertion surface fortheradialmuscles. ing wheneithertheradialorcircularmusclescontractand prevent themantlefromlengthen- The tunics (Figure 3.54). 1997) diagonally throughthemuscles(e.g.,Budelmannet al. at right angles to each other. Connective tissue fibres also run of stiff tuniccomposedoflayerscollagenfibresthatrun longitudinal musclesarereplacedbyouterandinnerlayers there areradialandcircularmusclesindecabrachians,but the of the mantle cavity) and water is drawn in. As in octopods, fibres makes themantle wall thinner(andincreasesthe volume Demont1985).Contractionoftheradial thicken (Gosline & the mantle,andradialmusclesarestretchedaswalls tension inthelongitudinalmusclesprevents lengtheningof water (as the locomotory jet) from the mantle cavity while radial muscles. Contraction of the circular fibres expels the allcasesthereisanantagonisticactionofcircularand In Demont1985). ing thewater inthemuscletissue(Gosline & Wainwright 1972)withthemantlewall musclespressuris- and the whole system acts as a muscular hydrostat (Ward & powers thejetpropulsionthatisahallmarkofcephalopods, contractionofmantlemusclefibresinthe wall The 3.12.3.8.2 2001, 2005). (Sumbre et al. brain of independent actions of the many these (Yekutieli b;ture 2005a, Sumbre et al. et al. 2005), with 2002, movements out precise - a pseudo-jointed into struc carrying is that arm the transform of can motor control. also Octopuses complex and possible system organised highly of the because Shell, Body, and Muscles and Body, Shell, Sepia atleast,thisisduetothealternatingactivity ofthe The mantle muscleismarkedly thicker incoleoidcepha- The mantle muscles entirely coleoids, are radial the In decabrachian

Mantle Wall and Funnel - - - colour (see Chapter 17). skin the quickly changing rapidlyto thus expand or contract, Messenger 10 mm 1996). (Hanlon & be or more high can that papillae spike-like to smooth –from texture skin the have sepioidsBoth octopods and complex muscles change that 3.12.3.8.5 below lies that ganglion sucker. each small complex by is assisted of a this musculature The coordination muscles. radial the with cles presumably antagonistically act mus- of sets circular two muscles other the the to with and angles at right muscles run meridial sucker.the In addition, of circumference the mentioned) around already sphincter the muscles (including are circular sucker of there the and surface inner the to muscles perpendicular lie Radial infundibulum. or one form or more hooks. or toothed late denticu be which can chitin with sucker may lined the be and of outer part the forms Its rim stalk. or by anarrow arm the to broadly may attached be muscle.sphincter The infundibulum a with ringed section by anarrow separated both dibulum, infun the attaches, cavity that (acetabulum) outer part the and inner an into divided sucker Each be (see can Chapter 17). Coleoids rows in arms have often on their suckers arranged 3.12.3.8.4 as amuscularhydrostat asdothearmsandtentacles(Kier1985). run diagonally through the muscles. Again, the whole system acts alsostrandsofconnective tissuethat elastic support. There are a layerofconnective tissue (themedianfascia) whichprovides and aredivided horizontallyinthemiddlesectionoffinby verse anddorsoventral musclebundles work antagonistically sepioidsandsquidthe trans- &Messenger1996).In (Hanlon Vampyroteuthis, andthey vary insize,shape,andfunction Fins arepresentinalldecabrachians,cirrateoctopods,and 3.12.3.8.3 can bury themselves (Hanlon &Messenger1996). direct itdownward toblow acavity insoftsubstratumsothey puses) aeratingtheiregg mass,whilesomebenthicoctopuses squirting ajetofwater atapredator, and(forfemaleocto- pointing inaparticulardirection.Otherfunctionsinclude through thefunnelandisusedinsteeringanimalbyit ture. The jet stream of water from the mantle cavity is directed be rolledintoatube,whileincoleoidsitistubular struc- (Bone et al.1995). flaps, thecircularmusclefibresofmantlearenot involved Chromatophores have systemChromatophores enables amuscular that them of and sets muscles acetabulum for act the both Three In Nautilus, thefunnelisamobilefoldoftissuethatcan Suckers

Skin Papillae Chromatophores Skin and Coleoid Fins Coleoid 131 - - Downloaded By: 10.3.98.104 At: 22:14 25 Sep 2021; For: 9781351115667, chapter3, 10.1201/9781351115667-3 (skin) layer at the bottom. Redrawn and modified from Kier, from Thompson, J.T.,and modified W.M. and Abh. (skin) Redrawn Paläobio. layer bottom. Berl. the at FIGURE 3.54 132

Diagram of the musculature and connective tissue in a ventral region of the mantle of a squid and an octopus, with outer outer with octopus, an and of asquid mantle of region the aventral in tissue connective and musculature of the Diagram circular muscle bres radial muscle mitochondria mitochondria mitochondria -poor zone collagen super super -rich zone muscle -rich zone central radial muscle cial cial muscle bres circular muscle bres circular longitudinal tissue bres connec collagen bres tiv e longitudinal muscle bres (connec inner tunic longitudinal connec tive tissue) intramuscular connec (connec Biology and Evolution of the Mollusca of the Evolution and Biology radial muscle br outer tunic tissue bres radial muscle bres tive tissue) tissue bres connec collagen bres tive tissue bres collagen bres muscle bres collagen bres longitudinal , 3, 141–162, 2003. crimped tiv e tiv e e