On the Mantle Cavity and its Contained Organsin the Loricata (Placophora).

By

C. M. Yonge, DJSe.,

University of Bristol.

With 6 Text-figures.

CONTENTS.

PAGE1. INTRODUCTION 3672. THE MANTLE CAVITY 368

(a) Lepidochitona oinereus, p. 370; (6) Tonieellamarmorea and AcanthocMtona crinitus,p. 373; (c) Lepidopleurus asellus, p. 374.

3. THE GILLS 3764. Mucous GLANDS 3825. OSPHRADIA AND OTHER SENSE O B G A N S 3836. DISCUSSION 386

7. SUMMARY 388

8. BEFERENCES 389

1. INTRODUCTION.

The investigations described in this paper represent a con-tinuation of previous work on the mantle cavity and its con-tained organs in the Gastropoda (Yonge, 1937 c, 1938) and inthe Scaphopoda (Yonge, 19376). They are intended to formpart of a comprehensive survey, from the functional aspect, ofthese organs throughout the Mollusca. The structure and theanatomical relations of the organs contained in the mantlecavity of the Loricata are well known, as a result, in the main,of the morphological investigations of Haller (1882, 1884),Pelseneer (1898, 1899), and Plate (1898-1901). But only Areyand Crozier (1919) have made observations on the water cur-rents in the mantle cavity, and they failed to point out how thesewere brought about, giving no account either of the ciliation ofthe gills or of the manner in which the mantle cavity is dividedinto inhalant and exhalant chambers.

368 0. M. YONGB

The greater part of this work has been carried out on twocommon British species, L e p i d o c h i t o n a c ine reus (Lepi-dochitonidae) and L e p i d o p l e u r u s asel lus , which is oneof the few representatives of the primitive order Lepidopleurida.Comparative data only has been obtained from Tonice l lamarmorea (Lepidochitonidae) and A c a n t h o c h i t o n ac r i n i t u s (Oryptoplacidae).1 All of these species live betweentide-marks with the exception of L e p i d o p l e u r u s ase l lus ,which, in the. English Channel, occurs at depths ranging from15 to 43 fathoms. Comparative observations on the gills of theGastropod, H a l i o t i s t u b e r c u l a t a , were carried out atNaples during the course of other work.

Acknowledgements are due to Dr. S. Kemp, F.E.S., andmembers of the staff of the Plymouth Laboratory, for assistanceduring a period spent there in connexion with this work, toProfessor E. Dohm, Director of the Stazione Zoologica, Naples,to the Colston Eesearch Society of the University of Bristol forfinancial assistance, also to Mr. H. P. Steedman, LaboratorySteward in the Department of Zoology, University of Bristol,for cutting sections.

2. THE MANTLE CAVITY.

The mantle cavity in the Loricata consists of lateral pallialgrooves in communication posteriorly, and bounded internallyby the sides of the foot and externally by the inner margin ofthe girdle. The mouth opens anteriorly and the anus posteriorly(Text-figs. 1 and 3, A.), both in the middle line. The sole of thefoot frequently extends under the anus in life. Eeproductiveand excretory pores open into the pallial groove on either side,near the posterior end but always in the region occupied bygills. The former openings are always the more anterior. Thegills vary widely in number throughout the Loricata and areactually not constant for any one species. Thus, of the specieshere examined, Tonice l la m a r m o r e a has between 19and 26, L e p i d o c h i t o n a c ine reus between 16 and 19,A c a n t h o c h i t o n a c r i n i t u s about 15, and Lep ido-p l e u r u s ase l lus between 11 and 13. The gill series may be

1 The names used are those adopted by Wlnckworth (1932).

MANTLE CAVITY IN LORICATA 869

holobranch or merobranch according as to whether or not theyextend the full length of the pallial grooves. None of the speciesexamined possesses gill series of the former type, althoughTonicel la marmorea and L e p i d o c h i t o n a c inereus(Text-fig. 1) approach this condition.

The first-formed gill occurs in the region between plates sevenand eight. According to Pelseneer (1898, 1899) the excretorypore invariably opens immediately anterior to this gill, whichis morphologically, and also functionally as the present workreveals, of great significance. It will be termed throughout thepost-renal gill. Pelseneer also states that it is invariably thelargest gill, but, as Plate (1901) had pointed out, this is notalways the case, although, if not actually the largest, it isalways one of a group of especially large gills. This post-renalgill may be the last of the series, as in L e p i d o c h i t o n ac inereus (Text-fig. 1, GP.), in which case the condition isknown as abanal. But, during development, gills may be addedposteriorly as well as anteriorly to this gill. The former aretermed adanal gills. There may or may not be a space betweenthe last adanal gill and the anus. Of the species examined onlyL e p i d o p l e u r u s ase l lus (Text-fig. 3) possesses adanalgills, and these extend up to the anus. Finally, the thin in-wardly projecting ridge which bounds the inner surface of thegirdle is dilated on each side in the region opposite to theposterior margin of the foot. The pair of inwardly projectingmantle folds (Text-figs. 1-3, GP.) SO formed have been describedby both Pelseneer and Plate.1 This investigation has revealedtheir function.

Observations on the nature of the currents in the mantlecavity were carried out by placing animals on glass slides. Whenthe animals had attached themselves the slides were inverted on.two pillars of plasticine in a shallow glass dish, the water inwhich just covered the slides. The dish was then placed on the

1 Plate (1901) states that the folds are absent in some species, but heincludes amongst these Lep idop leurus asel lus and Tonieel lamarmorea where it certainly occurs. It is probably of universal occur-rence, Plate being misled by contraction in the fixed material which heexclusively studied.

NO. 323 B b

870 0. M. YONGE

stage of a binocular microscope, carmine added to the water,and the nature of the water currents observed with the animalventral side uppermost. The general observations of Arey andCrozier (1919) on Chi ton t u b e r c u l a t u j (a Bermudanspecies attaining a length of 9 cm.) were confirmed. The gillscreate a current of water which runs backward along the pallialgrooves and out in the mid-line posteriorly (Text-figs. 1 and 8).The regions of intake vary, being created by local liftings of thegirdle. When the animals are completely submerged these areusually anterior (Text-figs. 1 and 8, i.) but may be lateral, andthere may be more than one opening on either side. When theanterior ©nd of an animal is out of water inhalant openings arecreated by a lifting of the girdle in the region still submerged.In this way a shorter, but still efficient, respiratory current isproduced. The exhalant opening (Text-figs. 1-8, E.) is alsocreated by a local raising of the girdle, in this case always atthe posterior end. The full discussion of the mechanisms con-cerned in the maintenance of the respiratory currents demandsseparate consideration of the various species.

(a) L©pidochi tona cinereus.—Although this speciesbelongs to the order Chitonida, and so is less primitive thanL e p i d o p l e u r u s ase l lus (order Lepidopleurida), the de-scription of conditions in both species will be easier if Lepi-d o c h i t o n a c inereus is considered first. In the animalshown in Text-fig. 1 there are seventeen gills on each sideextending along some four-fifths of the pallial grooves. Theyare attached to the roof of the grooves. All but the last andlargest of these, the post-renal gill (GP.), bend inwards towardsthe sides of the foot, but the post-renal gill extends backwardswith its (morphologically) posterior surface applied to the sideof the girdle fold (GF.) and its anterior surface to the side of thefoot. It thus blocks the pallial groove in this region. The fivegills immediately anterior to it also bend backwards to a greateror less extent, but they lie against the sides of the foot only.Throughout the whole series the sides of adjacent gills arealwayi closely applied.

Lateral cilia on the gills (described later) create a current ofwater which passes from their outer to their inner surfaces.

IC

o GF

TBXT-HG. 1.

Lepidochitona cinereus, ventral aspect, drawn from life:gills and boundaries of shell plates shown in left pallial groove,osphradium and division between inhalant and exhalant chambers(denoted by broken line) shown in right pallial groove, x 10. A.,anus; E., exhalant current; EC, exhalant chamber; p., foot;o., girdle; GI., most anterior gill; GF., girdle fold; GP., post-renalgill; I., inhalant currents; M., mouth; o., osphradium. Arrowsindicate direction of currents, broken arrows those in exhalantohamber.

372 C. M. YONGB

Owing to the arrangement of the post-renal gill across the pallialgroove there is a complete separation of the mantle cavity intoinhalant and exhalant chambers (Text-fig. 1, i c , BO.). Theformer consists of the pallial groove anterior to the first gill andthe region outside the gills behind this. The exhalant chamberconsists anteriorly of the region between the gills and the sidesof the foot (and so bounded ventrally by the lateral extensionsof the sole) and posteriorly of the entire pallial groove behindthe post-renal gills. The boundary between these chambers isindicated by the broken line in the right pallial groove inText-fig. 1.

A powerful backwardly directed current runs along the in-halant chamber, water being drawn through the gills laterallyinto the exhalant chamber and also posteriorly between thefilaments of the post-renal gills. This inhalant current is sopowerful that suspended particles do not tend to settle on tothe roof of the pallial groove when the animal is inverted forinspection. Particles too large to pass between the gill filamentsare carried to the tips of the gills, and so into the exhalantchamber. The gills are muscular and may assist the respiratorycurrent by moving outwards and then drawing inwards. Thepost-renal gills are particularly active, repeatedly extending andthen retracting, while their tips move from side to side.

In the exhalant chamber the water flows backwards, asindicated by the broken arrows in Text-fig. 1, and the streamsfrom both sides finally pass out by way of the exhalant opening.This may be formed either in the mid-line posteriorly or a littleto either side of this, but it is always confined to the spacebetween the tips of the post-renal gills. Particles carried in thiscurrent become concentrated in a narrow rejection currentwhich runs along either side of the anus (see broken arrow to theright of this in Text-fig. 1). The eggs or sperms liberated fromthe reproductive pores situated between the second and thirdgills (counting from the post-renal gill) on either side, the outflowfrom the excretory pores immediately anterior to the post-renalgills (GP.) and the faeces from the anus, all pass out with theexhalant current (E.) which is responsible for their transport.Both the genital and the excretory pores open on the inner side

MANTLE CAVITY IN tOEICATA 373

of the attachment of the gills, i.e. into the exhalant chamber,the apertures being so disposed that material is directed inwardstowards the sides of the foot.

The roof of the pallial groove is throughout richly ciliated,and cilia also occur on the outer but not on the inner sides.These cilia assist to some extent in the transport of particlesposteriorly. The walls of the exhalant chamber are moregenerally ciliated notably in association with the paffial mucoustracts (see below).

GF

TEXT-MG. 2.

Acanthochi tona cr in i tus , ventral aspect of posterior region,drawn from life. X 8. Lettering as before.

(b) Tonicella marmorea and Acanthochitonacrinitus.—Both of these species belong to the order Chitonida,the former being included in the family Lepidochitonidae andthe latter in the Cryptoplacidae. As already noted they re-semble Lepidoehitona cinereus in the absence of adanalgills, and, although the number of gills differs in both speciesfrom that in Lepidoehitona cinereus, they function inessentially the same manner with the large post-renal gillextending backwards and filling the space between the girdlefold and the edge of the foot. In Acanthochitona crini-tus, where the gills only extend for some two-fifths the lengthof the pallial grooves, there is a tendency for inhalant openingsto be formed laterally, near the anterior end of the gills, rather

374 0. M. YONGE

than near the anterior end of the pallial groove as in the othertwo species with their greater and more extended series of gills.Moreover, in this species, as shown in Text-fig. 2, the post-renalgills extend farther back than in L e p i d o c h i t o n a c inereus ,leaving a more restricted posterior exhalant cavity. The ex-halant opening is usually confined to a narrow region in themid-line, but may move a little to one side or the other whenthe animal makes turning movements.

(c) L e p i d o p l e u r u s asellus.—Conditions here, withadanal gills extending posteriorly up to the anus (see Text-fig. 3),are in significant respects different from those in the threerepresentatives of the Ohitonida. The usual number of gills, asshown in Text-fig. 3, is thirteen, although it may be less. Thegills are attached nearer to the base of the foot than are thoseof L e p i d o c h i t o n a c i n e r e u s , and they extend forwardonly as far as the junction between plates six and seven (GI.).The last six are posterior to the post-renal (GP.), and so areadanal gills. The anterior six gills bend inwards towards thefoot. The first four of these, as indicated by the dotted linesin Text-fig. 3, are actually obscured ventrally by the sole ofthe foot. The last seven gills, i.e. the post-renal gill and all theadanal gills, bend outwards, their tips making contact with theedges of the girdle folds. The girdle folds have the same formas those in the Chitonida, but extend farther posteriorly (seeText-fig. 3).

Thus the pallial grooves are divided into inhalant and ex-halant chambers, but in a somewhat different manner than inL e p i d o c h i t o n a c ine reus and the other members of theChitonida. The inhalant chamber is relatively larger, com-prising the whole of the pallial grooves anterior to the seventhshell plate, and the outer portion of the pallial cavity beneaththe seventh plate, and the outer do r sa l region of the groovesin the most posterior region. The bending outwards of the gillsin the posterior region is responsible for this dorsal extensionof the inhalant chamber. Water passes laterally through thegill filaments in the anterior region and downwards (upwardsas the animal lies in Text-fig. 3) posteriorly. The exhalantchamber is thus on the inner side of the pallial groove in the

MANTLE CAVITY JUS LOBICATA §75

TEST-BIG. 3.

Lepidopleurus asellus, ventral aspect, drawn from life,arrangement as in Test-fig. 1. x 12. Lettering as before.

region beneath plate seven extending over the completev e n t r a l area posterior to that.

Inhalant openings are normally formed anteriorly. The ex-halant opening is restricted to the region immediately posterior

376 C. M. YONGE

to the anus, which is here raised on a papilla carrying it almostto the inner edge of the girdle. Owing to the smaller numberof gills the water current is slower than in L e p i d o c h i t o n ac i n e r e u s . In correlation with this particles drawn in withthe inhalant current are carried in the main by ciliated tractswhich run along the edges of the pallial groove, on the sides ofthe foot and of the girdle. Particles carried in the first of theseare conveyed to the posterior margin of the foot where theycongregate in mucus-laden masses, and are from time to timetransferred to the surface over which the animal is moving.Particles are carried in the outer current to the region of thegirdle fold where they are conveyed outwards to the exterior.The course of both of these currents is indicated by arrows inText-fig. 3. They have no counterpart in any species of theChitonida examined where all particles pass into the exhalantchamber. Particles which remain in suspension in the respiratorycurrent are carried into the postero-dorsal extension of theinhalant chamber above the outwardly extended adanal gills.They finally emerge into the exhalant chamber between thesecond and third gills counting from the posterior end (seebroken arrows on either side of B. in Text-fig. 3). Transport ofthis material is assisted by cilia on the roof of the pallial grooveand dorsally along the sides of the foot, i.e. in the regions of theneural and pedal mucous tracts (see below).

The reproductive pores open between the bases of the eighthand ninth gills counting from the posterior end, and the excre-tory pores in front of the post-renal gills. The openings of bothpairs of pores are directed downwards, and not also inwards asin L e p i d o c h i t o n a c i n e r e u s , but their products will becarried outwards in the exhalant current. Owing to the posteriorextension of the anus (A.) faeces are deposited outside the bodywith the minimum of assistance from the relatively weak ex-halant current.

3. THE GILLS.The structure of the gills of the Loricata has been described

by a number of workers, notably Burne (1896), Pelseneer (1898,1899), and Plate (1898-1901). Pour views have been advancedas to their nature. (1) Spengel (1881) considered them all

MANTLE CAVITY IN.tOBICATA 377

homologous with the etenidia of other Mollusca and suggestedthe name Polybranehiata for the group. (2) Clans (quoted byPlate, 1901) thought that each gill row represents a ctenidiumwith a greatly extended longitudinal axis, each gill being homo-logous with a single filament of the etenidium. (3) Pelseneer(1898, 1899) considered that the post-renal gills were trueetenidia, but that the remaining gills were secondary structures.(4) Ihering (1877), Thiele (1890), and Plate (1901) a l regardedthe gills as secondary structures, outgrowths of the mantle likethe gills of P a t e l l a or of the Nudibranchia. But all of thesetheories are based on exclusively morphological examinationsof the gills; apart from determining the circulation of bloodthrough them no attempt has been made to study the gillsfunctionally. In particular the arrangement and nature of theirciliation has never been determined and compared with thatof the etenidia of the prosobraneh Gastropoda.

The nature of the ciliation on the gills of L e p i d o e h i t o n ac inereus has been examined in detail. That of the gills of theother species, including L e p i d o p l e u r u s a se l l u s , agreesin all essential details. Within the inner margin of the axis ofeach gill (Text-fig. 4) passes an afferent blood-vessel (Text-figs. 4 and 5, AV.), and within the outer margin an efferentvessel (BV.). On the inner side of each of these extend strandsof longitudinal muscle (LM.), and on the outer side the internaland external branchial nerves respectively (N.). The contractionof the longitudinal muscle on the outer (efferent) side of thegill axis will pull the gill away from the side of the foot, the con-traction of the other muscles will draw it back again. Thisprovides the mechanism for the regular inward and outwardmovements executed by the gills. Contraction of both muscleswill draw the entire gill downwards—or anteriorly in the caseof the post-renal gills in L e p i d o c h i t o n a c inereus and theother Chitonida, or inwards in the ease of the adanal gills ofL e p i d o p l e u r u s a s e l l u s . Extension will follow owing topressure of blood when the muscles relax. From either side ofthe axis extend a series of filaments which diminish in sizefrom the base to the apex of the gill (Text-fig. 4). The moststriking feature about their ciliation is the presence on the sides

378 0. M. YONGE

of the filaments, extending somewhat nearer to the inner thanto the outer surface, of a broad band of cilia (AC.) which attaina length of some 35/L*. The function of these cilia is that of

LM

TEXT-ITO. 4.

Lepidoohitona cinereus, posterior aspect of a gill from theleft pallial groove, drawn from life. x90. AC, area of longattaching cilia on filaments; A.V., afferent blood-vessel; EV.,efferent blood-vessel; IM., longitudinal muscle. Arrows indicatedirection of ciliary currents (horizontal arrows respiratory currentdue to lateral cilia), dotted arrows flow in blood-vessels.

attachment to the corresponding region on the next gill. It hasalready been noted how closely adjacent gills are applied inlife. On either side of this region, and on both sides of the axis,cilia are present which beat to the tip of the gill to which alllarger particles are carried (see arrows in Text-fig. 4).

MANTLE CAVITY IN LOBICATA 879

The opposed surfaces of the filaments may be divided intothree zones (see Text-fig. 5). The region near the outer surfaceis practically devoid of cilia. The middle region, bounded at themargin by the zone of attaching cilia (AC), possesses long lateralcilia (LC.) which cause a powerful current to pass between thefilaments from the outer to the inner side of the gill (see hori-zontal arrows in Text-fig. 4). The innermost region possesses

AV- LM

EV-

TEXT-ITG. 5.

•LM

Lepidochitona cinereus, lateral view ofpair of gill filaments,drawn from life. X125. LC., lateral cilia; IT., branchial nerves.Other lettering as before. Arrows indicate direction of beat ofcilia, crosses beat to apex of gill.

scattered cilia which beat in the same direction. The currentcreated by the lateral cilia is responsible for the respiratorystream, and is so powerful that all smaller particles are conveyedby it between the filaments, only the largest ones passing tothe tips of the gills.

The structure of the gills is essentially similar to that ofctenidia, while the ciliation clearly represents no more than amodification of that present on the ctenidia of the most primi-tive living Gastropoda, i.e. species of zygobranchiate genera suchas Diodora (Fissurella) o r H a l i o t i s .

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In the latter (Text-fig. 6) a narrow band of lateral cilia (LC.)on the elongated filaments creates a water current which passesfrom the efferent to the afferent side of the axis, here in theprimitive positions, ventral and dorsal respectively. The broadband of interlocking cilia (Text-figs. 4 and 5, AC.) on the sidesof the filaments in L e p i d o c h i t o n a c ine reus correspondsto the cluster of long terminal cilia (TC.) at the apex of eachfilament in H a l i o t i s . The cilia on the margins of the filaments

AFC

LC R

TEXT-ITG. 6.

Hal iot is tnbe rcu la ta , lateral view of pair of gill filamentsdrawn from life. x l5 . AFC., abfrontal cilia; CK., chitinous sup-porting rod (shown right side only); r e , frontal cilia; LC, lateralcilia (shown left side only); TC, long cilia at tips of filaments.Other lettering and arrows as before.

on the efferent and afferent sides correspond to the frontal(FC.) and abfrontal (AFC.) cilia respectively in H a l i o t i s . •

The differences between the filaments in the two cases arenot difficult to explain. The shortening of the filaments in theLoricata, and the presence of the broad band of interlockingcilia, are both due to the increased number of gills and thecloseness with which these are applied to each other. In orderto offset the effect of the consequent decrease in the lateralsurface, the breadth of the zone occupied by lateral cilia hasbeen greatly increased. But there is no longer any need forthe chitinous supporting rods (Text-fig. 6, CR.), characteristicof the elongated filaments of the ctenidia of both Gastropoda

MANTLE CAVITY IN I.OKICATA 381

and Lamellibranchia, in the shortened filament of the Loricata.Sections reveal the absence of this although the filaments areeverywhere strengthened by strands of connective tissue whichrun across the internal cavity. Finally, the difference betweenthe direction of beat of the frontal and abfrontal cilia inH a l i o t i s and corresponding cilia in L e p i d o c h i t o n ae inereus is due to the different manner in which sedimentbrought in with the respiratory current is disposed of in thetwo animals. Cleansing is the primitive function of all sachcilia, and the direction of their beat actually varies considerablyin different Gastropoda (Yonge, unpublished work).

There is thus good reason for believing that the gills ofthe Loricata are homologous with those of the prosobranchGastropoda, i.e. are true ctenidia, and that, of the four viewsas to their nature, the original suggestion of Spengel, which hashitherto found no support, is true. The ciliation of the secondarygills of P a t e l l a has been examined and does not correspondin the slightest with that of ctenidia, whereas that of the gillsof the Loricata unquestionably does while their structure isfundamentally similar. The one point of real difference is themultiplication of the ctenidia in the Lorieata, and that is to beassociated with the elongation of the body and the consequentanterior extension of the originally posterior mantle cavity intoa pair of narrow elongated pallial grooves. The differentorientation of the ctenidia, the axes of the majority of whichextend downwards (horizontally outwards in the case of thepost-renal and adanal gills of the Lepidopleuridae), is due to thesame cause. But, like the ctenidia of the prosobranch Gastro-poda and of the Lamellibranchia, they effectively divide themantle cavity into exhalant and inhalant chambers which thesecondary gills of P a t e l l a do not. The identical structure ofthe gills lends no support to Pelseneer's theory that only thepost-renal gill is a ctenidium, while Plate (1901) has con-clusively disproved the inherently improbable theory of Glausthat the gill series represents a single ctenidium. Plate (1901)advanced as one objection to the view that the gills are ctenidiathe fact that the auricles and kidneys are not multipliedcorrespondingly as they are in N a u t i l u s . But conditions are

382 C. M. YONGB

essentially different in the two groups. In the Tetrabranchiatathe duplication of the gills may reasonably be ascribed to thegreater respiratory needs of the animals which have not beenmet, as they have in the dibranchiate Cephalopoda, by a moreefficient circulatory system including the provision of branchialhearts, and by a more powerful respiratory current created bythe muscular action of the entire mantle (confined in N a u t i l u sto the siphon). In the Loricata the respiratory needs are notgreater than in the primitive mollusc, with the single pair ofctenidia in a posterior mantle cavity, from which they certainlyevolved. Multiplication is due, as already stated, to a reductionin size of the individual ctenidia owing to the change in shapeand mode of functioning of the mantle cavity. The effectiverespiratory surface is not increased. There is, therefore, no needfor similar multiplication of either auricles or kidneys.

4. Mucous GLANDS.Plate (1898-1901) noted the presence in the Loricata of tracts

of unicellular mucous glands in the mantle cavity. He dis-tinguished between neural, pedal, pallial, and branchial tractson the roof of the pallial groove, sides of the foot, inner wall ofthe girdle, and inner axis of the gills respectively.

In none of the large number of species which he examineddid he find more than three of these tracts, while some specieshad only two, others one, and some none at all. Various com-binations of the possible series of tracts were found in differentspecies. These tracts are easily seen in sections, the gland-cellsbeing usually greatly elongated and the contained, somewhatgranular, secretion staining readily with eosin and allied stains.They are always interspersed with ciliated cells. In Lepi -doch i tona c inereus and A c a n t h o c h i t o n a c r i n i t u s(Tonicella marmorea has not been sectioned) they areconfined to a pallial tract on the dorsal haK of the outer wallsof the pallial groove in the exhalant chamber posterior to thegills. In Lep idop leu rus asel lus Plate states that onlybranchial and pedal tracts are present, although he found neuraltracts associated with these in two other species of the samegenus, Lep idop leu rus ca j e t anus and L e p i d o p l e u r u s

MANTLE CAVITY IN 10BICATA 383

m e d i n a e . But in L e p i d o p l e u r u s ase i lus neural tracts,anterior to the gills, do exist although the cells are not soelongated as in the pedal tracts. The latter extend the fulllength of the pallial grooves, i.e. in both the anterior, inhalant,and in the posterior, exhalant, chambers. The arrangement andhistology of the tracts has been wel figured by Plate (1898-1901) and Knorre (1925).

The function of their secretion is clearly to consolidate theparticles of sediment brought in with the respiratory current.They are thus analogous with the hypobranehial glands of theprosobranch Gastropoda (Yonge, 1937 a, 1938). The pallialmucous tracts on the outer sides of the roof of the exhalantchamber in the two species of the Chitonida examined maypossibly be homologous with the hypobranehial glands becausethey occur in the same relative position. Plate recognized theessential function of the tracts, although bis ignorance as to thenature of the water circulation in the mantle cavity was suchthat he suggested that the secretion of the pallial tracts in theexhalant chamber was to protect the gills from contaminationwith the faeces. Plate noted that mucous tracts are most wide-spread in the more primitive genera with merobraneh gill series.This is to be correlated with the greater water current producedby the gills of the more highly evolved species, e.g. Lep i -d o c h i t o n a c ine reus with its extensive series of gills hasonly one pair of mucous tracts, while L e p i d o p l e u r u sase i lus with fewer and relatively smaller gills has three, ofwhich one, the neural, is entirely in the inhalant chamber andthe greater part of the pedal tract also. In many of the holo-braneh species the water current is presumably great enoughto carry particles through the pallial grooves in suspension sothat mucous glands become superfluous.

5. OSPHBADIA AND OTHER S B N S B O E G A N S .

Pour sets of sense organs have been identified in the mantlecavity of the Loricata. These are (1) the osphradia, (2) theanterior 'olfactory organs', (3) the branchial'olfactory organs',and (4) the lateral sense organs.

The osphradia occur in the majority of the Loricata being

384 C. M. YONGB

apparently absent only in the Lepidopleurida and a few speciesof the Chitonida (Plate, 1901). They are present in the threespecies of Chitonida here examined. They are elongated struc-tures lying along the roof of the pallial groove and extendingfrom the anus as far as the post-renal gills (Text-figs. 1 and 2, o.).Each consists of an area of long epithelial cells containingciliated and sense cells, and bounded by a well-defined cuticlethrough which penetrate the sense hairs. Prom the cellsnumerous nerve-fibres pass into the pallial cord which runsimmediately below. They have been figured by both Plate(1898-1901) and Pelseneer (1899). Both of these workersregarded them as homologous with the osphradia of the proso-branch Gastropoda because they occur in the same relativeposition. While, as indicated below, this may be true, it shouldbe noted' that, whereas in the Gastropoda they are in the in-halant region of the mantle cavity, in the Loricata they lie inthe exhalant chamber. This is also true of the 'osphradia' inthe Lamellibranchia, as Stork (1934) has pointed out.

Plate assumed that the osphradia have an olfactory function,for' testing' water, as originally suggested by Bernard (1890) forthe osphradia of the Gastropoda. Arey and Crozier (1919) cometo the same conclusion. But an organ so situated that theexcretory products of the animal flow over it would not appearto be ideally situated for such a function, moreover it cannot' test' the water until this is on the point of leaving the mantlecavity. It has been pointed out elsewhere (Hulbert and Yonge,1937) that the osphradia of the Gastropoda may with goodreason be regarded as tactile organs concerned with estimatingthe amount of sediment brought in with the respiratory current.These organs are always present in ctenidiate Prosobranchiawhich are all exposed to the danger of having the mantle cavityblocked with sediment, whereas only some shore-living orestuarine species are ever exposed to danger from impure water.In the merobranch Chitonida examined sediment is all passedinto the exhalant chamber, and, as shown by the broken lineslateral to the anus in Text-figs. 1 and 2, actually passes along thesurface of the osphradia before being ejected. There thus appearsas good reason for considering these structures to be concerned

MANTLE CAVITY IN 10RICATA 385

with estimating the amount of sediment brought into the mantlecavity as for regarding them as olfactory organs. It is alsoeasier on this basis to account for their retention in the Loricatain the same position as in the Gastropoda. In the latter groupsediment tends to settle out on to the osphradium in the in-halant region (Yonge, 1938) which is posterior and ventral, inthe former it is accumulated in the same relative position, butthis is here in the exhalant chamber owing to the formation ofinhalant openings anteriorly and the different orientation of thectenidia.

Plate denied the presence of anterior'olfactory organs' whichhad previously been described by Blumrich (1891). Morerecently, however, Knorre (1925) has confirmed Blumrieh'sconclusions by describing these organs in I s c h n o c h i t o nherdmani and I s chnoch i t on a e q u i g r a n u l a t u s . Theycertainly occur in L e p i d o c h i t o n a c ine reus but not inL e p i d o p l e u r u s a se l lu s . They consist of longitudinalstrips of sensory epithelia anterior to the gills and lying alongthe roof of the palh'al groove. They are innervated from thepedal cord and resemble the osphradia histologically. Knorreregards them as olfactory in function, but they may with equalreason be regarded as tactile organs concerned with estimatingsediment. They would certainly be in a position to detect anyabnormally great amount of sediment carried in with the in-halant currents and enable the animal to respond at once byclosing the inhalant openings.

The branchial and lateral sense organs occur only in the orderLepidopleurida where, as a result probably of the posteriorextension of the gills, osphradia are absent. The former consistof sensory patches of epithelia running along the efferent axesof the gills, i.e. on the topographically outer side in the case ofthe anterior gills, and on the upper side in the case of the post-renal and all adanal gills. Burne (1896), who originally describedthem, gives a detailed account of their position and innervation.He regarded them as true osphradia, but Plate, with goodreason, considered them secondary structures. They lie in thepath of the water current which passes through the gills butalso of the sediment which it carries. The lateral sense organs

NO. 323 C c

886 C. M. YONGE

were first described by Tbiele (1895). They consist of a series ofsmall patches of elongated sensory epithelium about the middleof the pallial wall and so project slightly into the cavity of thepallial groove. They extend along the entire pallial groove, andtheir number varies according to the age and size of the animal.They have not been counted in L e p i d o p l e u r u s ase l lusbut in L e p i d o p l e u r u s c a j e t a n u s they vary from 26 to35 pairs. The epithelium is of the same type as in the othersense organs, and, like them, they are innervated from thepalh'al cord. Their function also must remain problematical,Plate regarded them as olfactory, but they lie in the path ofsediment carried along the outer walls of the pallial groove andmay therefore with equal reason be regarded as being concernedwith the estimation of this. In either case the branchial andlateral sense organs of the Lepidopleurida very probably meetthe needs served by the osphradia and anterior sense organsin the majority of the Chitonida.

6. DISCUSSION.

The Loricata are a group of Mollusca in which the body hasbecome elongated and the original single shell valve convertedinto a series of eight overlapping plates. This change has fittedthem admirably for creeping over the uneven surfaces of rocks,particularly within the tidal zone where the encrusting algaeon which they feed grow in greatest abundance. Pretter (1937)has shown how highly adapted for this diet are the organs offeeding and digestion in the Chitonida. The extensive ventralsurface provided by the foot and girdle enables them to clingclosely to the uneven surface when the tide is out and to resistdislodgement during stormy weather. The articulating platespermit protection by curling up should the animal becomedetached. The capacity for creating inhalant apertures overa wide area on either side of the body, and for producing arespiratory current even when the anterior half of the body isout of water, are both of considerable biological significance.The Loricata are amongst the most highly specialized of shore-living animals.

The anterior elongation of the mantle cavity into a pair of

MANTLE CAVITY IK LOBICATA 387

narrow pallial grooves and the consequent formation of inhalant-openings a n t e r i o r to the gills instead of a single ventralposterior opening have been responsible, as already noted, forthe modification of the organs normally present in the mantlecavity of Mollusca. The ctenidia have been altered in positionand reduced in size but correspondingly increased in number,while their filaments have been modified in shape and citation.As a result the necessary functional division of the mantlecavity into inhalant and exhalant chambers has been main-tained. The mucous glands have been in some cases increasedin number, in others remain paired structures on the roof ofthe mantle cavity near the anus, and in others are entirelysuppressed, all in correlation with the number and position ofthe ctenidia. The osphradia—assuming these structures to behomologous with those so designated in the Gastropoda—per-sist in the majority of cases, but may share their problematicfunction, tactile or olfactory, with an anterior sense organ ofsimilar structure. Where absent, as in the Lepidopleuridaeowing to the posterior extension of the ctenidia, they are re-placed by branchial and lateral sense organs. The nature of themodified mantle cavity has further involved the appearance ofnew structures, the girdle folds, which enable the all-importantpost-renal gills (aided by adanal gills where these occur) tocomplete the functional division of the pallial grooves intoinhalant and exhalant chambers.

It is along such lines that we may explain, on a functionalbasis, the arrangement in the Loricata of these organs, thestructure of which has been so admirably described by morpho-logists such as Haller, Plate, and Pelseneer.

There remains for discussion the significant differences whichexist between the members of the orders Lepidopleurida andChitonida. The former are characterized by the absence, orpresence in a smooth condition only, of insertion plates. Theyare phylogenetically older than the Chitonida, the extinct familyGryphoehitonidae being Paleozoic and the surviving familyLepidopleuridae appearing in the early Tertiary. At the presenttime the Chitonida are, with a few isolated exceptions, shore-living animals occurring universally between tide-marks, where-

388 C. M. YONGE

as the Lepidopleurida seldom occur on the shore. They extend,unlike the Chitonida, into deep water, having been taken fromdepths exceeding 3,000 fathoms.

There appears, as outlined above, good reason lov believingthat the characteristic form of the Loricata evolved undershore-living conditions. The evolution of the more highlyspecialized Chitonida with their more efficient respiratorysystem and more complicated shell plates, possibly led to themigration into deeper water of the species of the four survivinggenera of the Lepidopleurida. Their descendants retain notonly the primitive shell structure, but also a smaller number ofgills producing a relatively weak respiratory current. The latterwill be no disadvantage when they are continually under water,and so do not need to interrupt the current when the tide isout. Eejection of waste material from the inhalant cavity andthe associated presence of neural and pedal mucous tracts isprobably also a primitive loricate feature, although acquiredafter these animals evolved from the original molluscan stock.But the presence of adanal gills and the substitution of branchialand lateral sense organs for the osphradium must be consideredsecondary developments, although certain of the Chitonida haveacquired adanal gills independently.

7. SUMMARY.

1. The course of the water currents in the mantle cavity ofthree species of the Chitonida, and one species of the Lepido-pleurida, has been determined.

2. Inhalant openings are created anteriorly or laterally bylocal raising of the girdle. The single exhalant opening isalways posterior and confined to the region between the lastpair of gills.

3. The exhalant current carries with it the genital andexcretory products, and, in the Chitonida, the faeces.

4. The bridging of the pallial grooves in the region of thegirdle folds by the post-renal gills (and adanal gills in theLepidopleurida) completes the functional division of the pallialgrooves into inhalant and exhalant chambers.

5. The gills possess the typical structure of ctenidia, and their

MANTLE CAVITY IN LOBICATA 889

ciliation is a modification only of that of ctenidia. They areto be regarded as multiplied ctenidia and not as secondarystructures.

6. The individual filaments are shortened, attached to thoseof adjacent gills by long interlocking cilia, and have a broadband of lateral cilia which create the respiratory current.

7. Four possible tracts of mucous glands in the pallial groovesare concerned with the consolidation of sediment. The pallialtracts may be homologous with the hypobranchial glands ofthe Prosobranchia; all are analogous with these. In theChitonida sediment is rejected only from the exhalant chamber,in the Lepidopleurida mainly from the inhalant chamber.

8. Osphradia,possiblyhomologouswiththoseinthe Gastropoda,occur in the majority of the Chitonida. With them may beassociated anterior sense organs. In the Lepidopleurida theyare replaced by branchial and lateral sense organs. All aresimilar in structure and innervation. They have been consideredolfactory in function, but with equal reason may be regarded astactile organs concerned with the estimation of sediment.

9. The Loricata probably evolved between tide-marks, theircharacteristic structure being admirably adapted for life on theshore.

10. The reasons for the differences between the structure andhabits of the Lepidopleurida and the Chitonida are discussed.

8. BEFEKENCES.

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Bernard, F., 1890.—"Rech. s. 1. organes palleaux des Gasteropodes Proso-branches", 'Ann. Sci, nat. Zool.', (7), 9.

Blumrich, J., 1891.—"Integument der CMtonen", 'Zeit. wiss. Zool.',52.

Bume, R. H-, 1896.—"Anatomy of Hanleyi abyssorum, M. Sars", 'Proo.Malac. Soc. Lond.', 2.

Fretter, V., 1937.—"Structure and Function of the Alimentary Canal ofsome Species of Polyplacophora (Mollusca)", 'Trans. Roy. Soc. Edin.',59.

Haller, B., 1882.—"Organisation der CMtonen der Adria, 1", 'Arb. zool.Inst. Univ. Wien', 4.

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Hulbert, G. C. E. B., and Yonge, C. M., 1937.—"A Possible Function ofthe Osphradia in the Gastropoda", 'Nature', 139.

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Knorre, H. von, 1925.—"Schale und Riickensinnesorgane von Trachyder-mon (Chiton) einereus u. d. ceylonischen Chitonen der SammlungPlate", 'Jena. Zeit. Naturw.', 61.

Pelseneer, P., 1898.—"Morphologie des branchies et des orifices renaux etgenitaux des Chitons", 'Bull. Sci. France Belg.', 31.

1899.—"Rech. morphologiques et phylogenetiques sur les Mollusquesarchaiques", 'Mem. cour. Acad. Belg.', 57.

Plate, L. H., 1898.—"Anatomie u. Phylogenie der Chitonen (a)", 'Zool.Jahrb.', Suppl. 4, Fauna Chilensis (1).

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Spengel, J. W., 1881.—"Geruchsorgane und Nervensystem der Mollusken.Beitr. z. Erkennt. der Einheit des Molluskentypus", 'Zeit. wiss. Zool.', 35.

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1895.—"tJ. d. Verwandtschaftsbeziehungen der Amphineura", 'Biol.Centralb.', 15.

Winckworth, R.? 1932.—"BritishMarine Mollusea", 'Journ. Conchol.', 19.Yonge, C. M., 1937a.—"Biology of Aporrhais pes-pelecani and A. ser-

resiana", 'Journ. Mar. Biol. Assoc.', 21.19376.—"Circulation of Water in the Mantle Cavity of Dentalium

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