the anatomical basis of function in the buccal mass of prosobranch and amphineuran molluscs

J. Zool., Lond. (1973) 169, 317-348

The anatomical basis of function in the buccal mass of prosobranch and amphineuran molluscs

ALASTAIR GRAHAM Department of Zoology, University of Reading

(Accepted 10 October 1972)

(With 6 figures in the text)

A comparative account is given of the muscular anatomy of the buccal mass in chitons and a number of species of prosobranch gastropods. From this can be deduced a basic muscular organization consisting of buccal constrictors and dilators, protractors and retractors of the odontophore, protractors and retractors of the subradular membrane and an approximator muscle of the supporting cartilages. In addition to these many ancillary muscles act as tensors : these are numerous in chitons, monoplacophorans and rhipidoglossan prosobranchs. In the first two groups, which have a poorly developed anterior end covered by a shell, they act in place of the muscles of the mobile wall of the head of gastropods; in the last they are necessary for the fine control of an odontophore brushing the substratum. In prosobranchs which forcibly rasp their food they are lost.

The dominating influence in the evolution of the buccal mass in neogastropods is the proboscis. Its narrowness and elongation have had profound effects on the anatomy of the buccal mass.

Contents

Introduction. . . . . . . . . . . . Organization of the buccal mass of prosobranchs Feeding in prosobranchs . . . .

Opening of the mouth . . . . .. Protrusion of the odontophore . . . . Protraction of the subradular membrane . . Dorsoventral movement of the cartilages . . Retraction of the subradular membrane . .

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Retraction of the odontophore . . .. Closing of the mouth . . . . . . Swallowing of food .. . .

Amphineurans . . . . . . . . . . Discussion . . . . . . . . . . . . Summary . . . . . . . . . . . . References . . . . . . . . . . . . Abbreviations used in figures . . . . . .

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Page 317 318 322 323 323 327 33 1 33 I 334 336 336 337 340 346 346 348

Introduction The characteristic rasping organ of the molluscs, the radula, has been most fully

exploited by chitons and gastropods; it is of less importance in cephalopods and has been lost by bivalves. In gastropods the pattern of radular dentition has undergone an evolution

317

318 A. GRAHAM

related to changes in the nature of the food and in the process by which it is gathered. How a radula works and the different ways in which each type functions were first demonstrated by Ankel(l937, 1938), later by Eigenbrodt (1941) and have been summarized by Graham (1959) and Fretter & Graham (1962). The value of the radula to gastropods has been enhanced by association with an odontophore, which allows more efficient and better controlled use of the teeth. The evolution of radular pattern has a parallel evolution in the anatomy of the odontophore and, in particular, in the cartilages which support it and the muscles by which it is manipulated.

Although there are many papers already published describing buccal musculature in not too much detail they are almost without exception accounts of single species in which comparative and evolutionary aspects are not discussed. Until the work of Nisbet (1953), too, the function of a muscle was deduced from its anatomical relationships. Even when the stimulation of living muscles which he introduced is used to discover what happens when they contract, caution must be exercised in assuming that what a muscle does in a dissected snail is also what it does in the intact animal: its relationships to other parts have been altered, the possible role of blood as a hydrostatic skeleton destroyed and, perhaps, the wrong stimulus given. Electromyography of intact animals as used by Ballantijn & Hughes (1965) has not yet been applied to this problem.

The most important studies of the anatomy of the prosobranch buccal mass are those by Huxley (1853), Geddes (1879), Amaudrut (1898), Woodward (1901) on Pleurotomaria, Herrick (1 906) on Busycon (= Sycotypus), Dakin (19 12) on Buccinum, Kuttler (1 9 13) on UZiva, Weber (1927) on Tonna (= Dolium), Crofts (1929) on Haliotis, Johansson (1939) on Littorina, Wilsmann (1942) on Buccinum, Carriker ( 1 943) on Urosalpinx, Starmuhlner (1952) on Viviparus, Bithynia and Valvata, Nisbet (1953) on Monodonta, Fretter (1964) on Mikadotrochus, Graham (1964) on Patella, Fretter (1965) on neritids, Graham (1965) on Ianthina, Burton ( 1 97 1) on Nassarius and Nucella. Descriptions of the buccal musculature of chitons have been given by Sampson (1895) and Plate (1897); of that of Neopilina galatheae by Lemche & Wingstrand (1959).

In the work reported in this paper I have examined, by dissection and stimulation, primarily specimens of Diodora apertura (Montagu), Crepidula fornicata (L.) and Olivella biplicata (Sowerby) and all references to these animals are based on these observations. I have also dissected specimens of Haliotis tuberculata L., Littorina littorea (L.), Viviparus viv@arus (L.), Nucella lapillus (L.) and Buccinum undatum L. and certain findings on these animals confirming or correcting previous work are marked by the initials A.G. I have also dissected specimens of Lepidochitona cinereus (L.) and Katharina tunicata (Wood) in relation to the comparison of gastropod and amphineuran buccal masses.

I am grateful to Dr Vera Fretter for bringing me live specimens of Olivella biplicata from Santa Catalina, California.

Organization of the buccal mass of prosobranchs To facilitate understanding of the buccal musculature some account of the relationships

of buccal mass, nervous and vascular systems is necessary. In the typical prosobranch the anterior end of the head is extended into a short snout

which lies anterior to the tentacles. It is bent ventrally and the mouth lies on its down- turned end. From the mouth a short passage, the oral tube, leads inwards to an expanded

B U C C A L MASS I N CHITONS A N D GASTROPODS 3 I9

chamber lodged within the head, the buccal cavity, and thence to the rest of the gut. Continental malacologists tend to use the terms buccal cavity for what is here called the oral tube and pharynx for the expanded chamber.

Tn the buccal cavity lies the odontophore, which projects into it from the posterior wall, beyond which it extends back into the cephalic haemocoel. The space between the underside of the odontophore and the floor of the buccal cavity is known as the sublingual pouch, those between its sides and the lateral walls o f the buccal cavity as buccal pouches, whilst the main channel of the gut passes dorsal to it to run into the oesophagus. The odontophore is a highly muscular structure supported by skeletal cartilages and covered by a cuticle, the subradular membrane (elastic membrane of some authors), on to which the anterior part of the radula is fused. The membrane is movably attached to the rest of the odontophore. The anterior end of the radula runs in a groove along the middle of the dorsal surface of the odontophore, ending anteriorly at its tip. It may be traced back into the radular sac which extends into the body cavity and ends blindly there, almost always at a point posterior to the hinder tip of the odontophore.

Between the mouth of the radular sac and the point where the oesophagus leaves the buccal cavity lies a broad but shallow space, the radular diverticulum, more prominent in lower than in higher prosobranchs. Its roof is formed by a fold which is also the floor o f the first part of the oesophagus. It is a mobile structure, its movements helping to pass food from the radular teeth into the oesophagus and, at the same time, to prevent food entering the radular sac. It will be called the transverse fold.

In many species the roof of the buccal cavity bears a pair of jaws, sometimes fused into a median structure, close to its junction with the oral tube. Behind the jaws two longitudinal folds arise which run along the roof of the cavity and enter the oesophagus. The openings of the salivary glands lie lateral to their anterior ends.

The walls of the oral tube, of the buccal cavity and of the anterior part of the oesophagus are all bound to one another and to the odontophore by an array of muscles so as to form a structural and functional unit occupying much of the space within the head: it is this unit to which the name buccal mass is applied. The buccal mass is, in its turn, related to the body wall of the head, to the major nervous centres and to the vascular system. The relationship to the body wall is simply that numerous muscular ties exist which are described below.

The main anterior ganglia, cerebral, pleural and pedal, and their interconnexions, are superficial to the buccal mass. In diotocardians (Fig. 1 ) the cerebral ganglia lie laterally alongside its anterior end and their long commissure runs in front of it rather than dorsal to it. The pleural and pedal ganglia are closely associated with one another and are placed posterior and ventral to the buccal mass (Fig. 21, their connectives to the cerebral ganglia being long trunks running lateral to the buccal mass just within the body wall. In mesogastropods concentration of the ganglia has occurred in such a way that the cerebral ganglia lie posterior to the buccal mass at the level of the pleural and pedal pairs; the former ganglia have migrated dorsally and lie alongside the cerebrals rather than the pedals.

In diotocardians the cerebral ganglia are linked to each other (in addition to the cerebral commissure) by the stomatogastric loop, running ventral to the oral tube, and carrying labial ganglia on its length. Each labial ganglion is connected to a buccal ganglion which lies in the transverse fold, dorsal to the odontophore, dorsal to the radular diverticulum

320 A. G R A H A M

but ventral to the oesophagus, the two buccal ganglia being interlinked by a commissure. Most odontophoral structures are supplied by nerves of labial or buccal origin. As part of the process of nervous concentration which monotocardians have undergone the labial ganglia come to lie alongside the cerebral ganglia, their commissure breaking down; the buccal ganglia now present the appearance of being linked directly to the cerebrals.

I I

IPO oc bw

FIG. 1. Dissection of buccal mass of Diodora apertura seen from above and to the right. The oesophagus and part of the roof of the buccal cavity and radular diverticulum have been removed and the buccal membrane split, (Explanation of abbreviations see p. 348.)

In the higher monotocardians (neogastropods) the relationship between buccal mass and nervous system has been greatly changed by the formation of a proboscis as an elongation of the snout anterior to the tentacles (Amaudrut, 1898). The buccal mass (Fig. 3) necessarily remains in the proximity of the mouth at the tip of the proboscis whereas the nerve ring lies at its base, an extended oesophagus and elongated nerves linking the two. A further change is due to the fact that the buccal ganglia (bg) have migrated so as to lie close to the fused labials and cerebrals (cg). As a result of this no ganglia lie in the buccal mass, only nerves of cerebral or buccal origin, both of the original pairs of ganglia having become incorporated in the nerve ring and this, in contrast to the diotocardian condition, is associated with the oesophagus rather than with the buccal mass.

The vascular supply of the buccal mass is provided by the anterior aorta and its branches. In diotocardians, the aorta (Fig. 2, aa) runs forward from the heart and approaches the head ventral to the oesophagus. At the level of the posterior end of the buccal mass it surrounds the radular sac and gives off a radular artery which lies around the whole of the backward extension of that structure. At this point, too, the pedal artery (pa) descends into the foot and a buccal artery passes forward into the buccal mass. The wall of this artery expands to form a membrane, the buccal membrane (bm), often strengthened with sheets or bundles of muscle, which forms the outermost layer of an

B U C C A L M A S S I N C H I T O N S A N D G A S T R O P O D S 32 I

arterial space around and within the odontophore and separates it from the other haemocoelic cavities in the head, except ventrally, where they communicate. The nerve ganglia and oesophagus lie external to this membrane and therefore in venous spaces.

soc aa 5m

2 m m

FIG. 2. Dorsal view of dissection of' posterior part of buccal mass and neighbouring structures of Holiofi.5 tubemdata. The oe3ophagus, radular diverticulum and radular sac have been removed and the buccal membrane split. (Explanation of abbreviations see p. 348.)

The same arrangement holds in the mesogastropods, but in neogastropods the formation of the proboscis has necessitated alterations in the details of the vascular anatomy con- sequent upon the separation of buccal mass and nerve ring. The point at which the pedal artery separates from the main anterior aorta remains at the level of the latter and a new vessel (Fig. 3 , mpa), the median proboscis artery (buccal artery of some writers), runs the length of the proboscis. On reaching the odontophore, however, this vessel does not open into a large sinus, but tends to branch elaborately into numerous separate arteries (Carriker, 1943; Burton, 1971).

The odontophore is supported by cartilages which decrease in number as one ascends the prosobranch series. The greatest number is found in Patella (Graham, 1964) in which no less than five pairs occur, though the fifth pair takes the form of small nodules embedded in the radular retractor muscles. The others are a pair of large anterior cartilages which support the tip and greater length of the odontophore, a posterior pair aligned behind these, and two small lateral pairs near the front end of the odontophore, the anterolaterals dorsally, the ventrolaterals below. The anterior and posterior cartilages on each side are firmly linked by membrane; all the others are interconnected by muscles, mainly parts of protractor and retractor muscles.

322 A . G R A H A M

The ventrolateral cartilages (Amaudrut, 1898) tend to fuse with the anterior cartilages and in zeugobranchs and Viviparus only three pairs occur. The anterolateral cartilages also tend to unite with the anterior cartilage and in Pleurotomaria, trochids (Nisbet, 1953) and neritids (Fretter, 1964) only two pairs are found. In monotocardians fusion is complete on each side with only two cartilages in all and in some neogastropods these show incipient fusion across the mid-line.

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FIG. 3. Olivella biplicata. Dissection of head from the left. (Explanation of abbreviations see p. 348.)

Feeding in prosobranchs Feeding in prosobranchs is a rhythmical process and comprises a series of events

cyclically repeated and carefully analysed by Ankel (1937, 1938) and Eigenbrodt (1941). Before the start of feeding the snout is lowered to the substratum and at the end of feeding it is raised from it; between these events a number of rasping cycles intervene. Each cycle may be said to contain several phases, though all unite into one continuous movement- (1) the mouth opens; (2) the odontophore is protracted and its tip is protruded through the mouth near the ventral lip; (3) the subradular membrane is pulled outwards over the tip of the odontophore so that a small number of rows of radular teeth are carried over the bendingplane (Ankel, 1938) and erected; (4) the tip of the odontophore is moved anteriorly (dorsally) over the surface of the substratum and (5), whilst this is occurring, the subradular membrane and radular teeth are retracted over the tip of the odontophore and bending plane so that they close and rasp the substratum; (6) the odontophore is withdrawn, and (7) the mouth closes. In addition movements of the jaws (where present) take place so that they are pressed over the odontophoral tip or lifted free of it and (8) the food which has been collected is swallowed.

These different phases may be conveniently used as the basis on which to describe the comparative anatomy of the buccal mass.

BUCCAL M A S S I N C H I T O N S A N D G A S T R O P O D S 323

Opening of the mouth In prosobranchs the mouth has usually the form of a vertical slit bounded by lateral

lips; smaller dorsal and ventral lips are sometimes visible. The oral tube continues the same shape and is a narrow vertical space with thick lateral walls. In stenoglossans which bore molluscan shells, such as Urosalpinx (Carriker, 1943) and Nucella (Burton, 1971) and in those, like Nassarius (Burton, 1971), in which sucking plays a prominent part in the ingestion of food, the mouth is round. A circular fold within the lips of Tonna (Weber, 1927), Urosalpinx and Nucella seems to be formed by fusion of the right and left inner lips which occupy a similar position in such genera as Patella (Graham, 1932), Littorina (Fretter & Graham, 1962) and Viviparus (Starmuhlner, 1952).

In all prosobranchs the wall of the oral tube is tied to the inside of the body wall by a large number of small muscular strands, irregularly arranged. The most anterior of these emerge from the lips. On the assumptions that blood pressure maintains the body wall rigid and that antagonistic muscles relax, contraction of these strands will simultaneously dilate the oral tube and open the mouth. In addition, contraction of the longitudinal component of the muscles of the body wall pulls the lips backward and contributes to the same end. Of greater significance than either of these, however, is the termination, in the lips, of some fibres of the lateral and ventral protractors of the odontophore (see below) : when these muscles contract not only is the odontophore moved forwards, but the lips are pulled apart. This pattern has already been described for Patella (Graham, 1964), Monodonta (Nisbet, 1953), Viviparus (Starmuhlner, 1952), Iunthina (Graham, 1965), Tonna (Weber, 1927), Busycon (Herrick, 1906), Urosalpinx (Carriker, 1943), Nucella and Nassarius (Burton, 1971) and may be deduced as also occurring in Haliotis (Crofts, 1929), Littorina (Johansson, 1939) and Buccinurn (Wilsmann, 1942). To this list can now be added Diodora, Crepidula and Olivella.

The inner lips and bulges are so arranged as to move apart along with the opening of the mouth. In Patella (Graham, 1964) the muscles responsible are partly the lateral protractors of the odontophore, partly the retractors of the subradular membrane (see pp. 331-334) and partly local muscles running to the adjacent ventrolateral cartilages. This arrangement ensures that the lips are retracted during protrusion of the odontophore (contraction of the protractors, relaxation of the retractors of the subradular membrane) and also during its retraction (relaxation of the protractors, contraction of the retractors). In Monodonta (Nisbet, 1953) the dorsal lips provide attachment for fibres of the mandi- bular protractor muscle which run from the anterior (dorsal) face of the jaw; on their contraction the jaw is protruded and the dorsal lip withdrawn since both ends of this muscle are mobile. The lateral lips contain endings of slips of the inner part of the ventral protractor muscle of the odontophore, but not, apparently, of any part of the retractor musculature.

Protrusion of the odontophore In diotocardians and mesogastropods with a ventral mouth the odontophore lies at

rest in the buccal cavity making an angle of about 45" with the long axis of the head-foot. In neogastropods the mouth is no longer ventral but placed more or less terminally at the apex of the proboscis; correlated with this the resting odontophore lies nearly parallel to the long axis. In the former group protrusion involves not only the forward translation of

324 A . G R A H A M

the odontophore but also a ventral movement, almost of a rotational nature, in order that its tip reaches the mouth near the ventral lip. By contrast, a simpler forward motion is all that is required in the neogastropod to achieve the same end; this is reflected in the muscles which perform it.

In general the protractor muscles are the most superficial in the odontophore and form a sleeve of bundles and sheets which originate anteriorly on the wall of the snout, in and near the lips, and which are inserted on the cartilages at the posterior end of the buccal mass. The sleeve is incomplete dorsally where the oesophagus interrupts it and it becomes increasingly more powerful towards the ventral side. Three sets of muscles are distinguishable in the prosobranch series, the dorsal, lateral and ventral protractors of the odontophore.

The dorsal odontophoral protractor muscles are the weakest and least common in occurrence. The greater part of their length lies in the wall of the arterial sinus of the odontophore, the buccal membrane; only at their anterior end do they leave it to pass to the body wall.

In Patella and Diodora (Fig. 1 , dpo) they arise from the posterior face of the posterior cartilages and run to the roof of the radular diverticulum, the buccal roof and finally the dorsolateral wall of the snout, passing dorsal to all other parts of the odontophore. Most of their branches are medial to the anterior levator muscles and dorsal to the cerebral ganglia. In Patella nearly all fibres cross to the opposite side of the body between origin and insertion; in Diodora many, but not all, do this. In other diotocardians it is difficult to be sure that these muscles are present. In pleurotomariids (Woodward, 1901 ; Fretter, 1964) and Nerita (Fretter, 1965) nothing comparable seems to exist, and whilst it is possible to make some comparison with muscles in Monodonta there are distinct differences. Nisbet (1953) described (under the name dorsal buccal tensor) a muscle on each side of the head which runs from the posterior surface of the posterior cartilage to the dorsolateral wall of the snout, but these muscles do not run in the buccal membrane, do not decussate, pass ventral to the cerebral ganglia at their anterior end and are lateral to the anterior levators.

In the mesogastropods Viviparus, Littorina and Crepidula a muscle runs from the hinder end of the cartilage on each side to the dorsolateral body wall, but external to the buccal membrane. In Littorina these muscles are those called m, and m, by Johansson (1939). In all three, however, they may be more directly comparable to the buccal levators of other genera (see below). No similar muscle is visible in Ianthina.

In the neogastropods Carriker (1943) described dorsal odontophoral protractor muscles in Urosalpinx, as did Burton (1971) in Nucella and Nassarius. These appear comparable to muscles in Buccinum called jugalis muscles by Wilsmann (1942) and dorsal odontophoral protractors by Dakin (1912) and to similar muscles in Busycon (Herrick, 1906). In position, course and relations to other structures they are not homologous with the dorsal odontophoral protractors of the diotocardians but are the most dorsal parts of the next group of muscles, the lateral and ventral protractors.

Lateral and ventral protractor muscles are of universal occurrence in all the animals examined or described in the literature, and constitute the major source of power for protrusion of the odontophore. They are best regarded as a single muscle or group of muscles, inserted at the posterior end of the odontophore and originating on the lateral and ventral walls of the snout anteriorly, which has become divided into more dorsal

BUCCAL MASS I N CHITONS A N D GASTROPODS 325

portions which form the lateral protractors, and more ventral parts, the ventral protractors, the line of division varying from genus to genus. Like the dorsal protractors they run attached to the inner side of the buccal membrane though often becoming free of it as they pass forwards. All have to pass through the membrane or its ventral gap to reach their origin on the body wall. They pass medial and ventral to the cerebral ganglia though lateral to the cerebrobuccal connectives, buccal ganglia and the anterior levator muscles. As already mentioned, some branches of the lateral protractor muscles end anteriorly in the inner lips; others may attach to the lateral parts of jaws, if they occur, and to the dorsal wall of the buccal cavity at about the same level. Their contraction presses the jaws and buccal roof against the tip of the odontophore as it moves forward, with two effects- one, to keep shut the groove on the odontophore within which the radula lies, avoiding premature spreading and erection of the teeth; two, to help to rotate the odontophore ventrally towards the mouth.

Lateral and ventral odontophoral muscles occur in Patella (Amaudrut, 1898- protractor, ,fch ; Graham, 1964), Diodora, Haliotis (Amaudrut, 1898-fch ; Crofts, 1929- P.9, P.9a, P. 10, P. 10a, P. 17; A.G.), Pleurotomaria (Woodward, 1901-lateral ventral protractors), Monodonta (Nisbet, 1953-lateral, ventral protractors), Nerita (Amaudrut, 1898-fch ; Fretter, 1965-lateral, ventral protractors), Viviparus (Starmuhlner, 1952- protractor of buccal mass ; A.G.), Ianthina (Graham, 1965), Crepidula and Tonna (Weber, 1927). All agree with the description given above except that in Crepidula the muscles lie medial to the buccal ganglia and cerebrobuccal connectives, a fact which may invalidate their homology.

The same muscles occur in stenoglossans though the names by which they have been previously described have been affected by the absence of true dorsal odontophoral protractor muscles. Muscles which are clearly homologues of the lateral protractors of diotocardians and mesogastropods in respect of origin, insertion and course have, for this reason, commonly been called dorsal protractors. They have been recorded, along with the homologues of the ventral protractors, in Urosalpinx (Carriker, 1943-dorsal, ventral odontophoral protractors), Nucella (Burton, 197 1-dorsal, ventral and ventrolateral odontophoral protractors), Buccinum (Dakin, 191 2-dorsal odontophoral protractor, median ventral retractor; Wilsmann, 1942-anterior jugalis superior muscle, radular protractor), Busycon (Herrick, 1906-odontophoral protractors), Nassarius (Burton, 1971-dorsal odontophoral protractors) and in Olivella.

Some variation occurs in the origin of the protractors in neogastropods: in Urosalpinx fibres originate in the oral sphincter muscles rather than the body wall; in Nucella the most ventral fibres, and in Buccinum the most dorsal fibres do the same. In Busycon the dorsal fibres come from the lateral walls of the oral tube. In Buccinum all (according to Dakin and Burton but not Wilsmann) and in Nassarius some of the ventral muscle bundles originate on the wall of the sublingual pouch. Only in Urosalpinx is the branch to the roof of the buccal cavity retained.

In mesogastropods the protractor series of muscles becomes markedly more powerful towards the ventral side; in neogastropods it is more evenly developed. The powerful ventral musculature imparts a dorsal component to the forward drive of the odontophore which has to be corrected by a variety of devices if the odontophore is to arrive properly placed for the next phase of the feeding cycle: jaws, levator and depressor muscles are all part of the apparatus. Despite its apparent inefficiency, nevertheless, the dorsal motion

326 A . G R A H A M

is preserved because, once the odontophoral tip has made contact with the substratum near the ventral lip the next phase is a movement towards the dorsal lip. Since the radular teeth are now biting the substratum considerable power is required to bring this about. In neogastropods this movement, though still present, is a much less important part of feeding and the radular teeth are pulled by much more powerful muscles than occur in lower prosobranchs. This action is dealt with on pp. 331-334.

The ventral rotatory movement is partly due to three pairs of muscles, the anterior and posterior levators and the depressors, which are confined to diotocardians and mesogastropods. These muscles run from the ventral surface of the odontophoral cartilages at their anterior and posterior ends to the dorsolateral wall of the snout (levators) and from the posterior end of the cartilages, dorsally, to an origin in the musculature of the anterior half of the foot (depressor).

Anterior levator muscles have already been described in Monodonta (Nisbet, 1953) and in Patella (Graham, 1964). Tn both the muscle runs from the ventral side of the anterior end of the anterior cartilage to the dorsal body wall where it attaches posterior to the base of the tentacle. It runs, at least in part, in the buccal membrane and passes lateral to the buccal ganglion and (in Patella) to the dorsal odontophoral protractor, but medial to the lateral protractor and to the cerebral ganglion and its connectives. Similar muscles occur in Diodora (Fig. 1, al), in Nerita (Fretter, 1965) and in Pleurotomaria (Woodward, 1901- lateral protractor). No comparable muscle seems to occur in any monotocardian.

The posterior levators also occur in Monodonta (Nisbet, 1953) and Nerita (Fretter, 1965); they are absent from Diodora and Patella (Graham, 1964) and are either absent from or undescribed in Pleurotomaria (Woodward, 1901). Each muscle runs from the posterior end of the cartilage ventrally to the dorsal body wall medial to the cerebral connectives but lateral to the buccal ganglion and the lateral protractor muscle.

The situation in Haliotis is confusing. Crofts (1929: 60) described as a lateral protractor (P.5) a muscle inserting on each posterior cartilage ventrally and running “dorsal to cerebro-pleural connectives” to the body wall. Her figure (plate V, fig. 19), however, shows this muscle as ventral or, preferably, medial to the connectives and to the lateral protractor muscles, P.9). Dissection of specimens of Haliotis shows two muscles, both originating on the dorsolateral body wall, both medial to the cerebral connectives, both lateral to the buccal ganglion but one lateral and the other medial to the protractor muscle. The muscle medial to the protractor (and therefore agreeing in its relations with the anterior levator of other diotocardians) inserts at the hindermost part of the cartilages like a posterior levator, whilst that with the insertion comparable to an anterior levator lies on the wrong side of the muscle for strict homology.

Unlike the anterior muscle the posterior levator appears to be found in some monotocardians. Johansson (1 939) described paired muscles in Littorina (ml, m,) which seem directly comparable. Tn Crepidula a muscle runs on each side from the posterior end of the cartilage to an origin in the body wall of the neck. It joins the anterior end of a longitudinal sheet of dorsolaterally attached vertical muscle strips which form the outer boundary of a space in which lies the salivary gland. When it contracts it undoubtedly acts to a certain extent as a buccal levator, but whereas in all the other animals which have posterior levator muscles the lifting of the odontophore is accompanied by a protractor movement, in Crepidula it involves some degree of simultaneous retraction. The

B U C C A L MASS I N C H I T O N S A N D GASTROPODS 327

difference may perhaps be connected with the elongation of that part of the limpet’s head which liw between buccal mass and nerve ring.

Odontophoral depressors have been described in Monodunta (Nisbet, 1953) and Nerita (Fretter, 1965). Muscles which may act in this way but are more probably radular retractors occur in Diudura running on each side from the cartilage at the posterior end of the odontophore to the foot, which they enter one on either side of the pedal artery where it originates from the anterior aorta. On the lateral side of each lies an extension of the ventral part of the cephalic haemocoel which Nisbet named the postlabial sinus in Monodunta. The relations of muscle and vascular spaces are similar in both animals. The question of the occurrence of this muscle in Haliotis is discussed on p. 334. Muscles corresponding to depressors were described by Weber (1927) in Tonna but otherwise it is doubtful whether they occur in mesogastropods. A pair of muscles partly comparable can be detected in Viviparus and perhaps in Crepidula. In the former genus a muscle is formed on each side of the buccal mass by the union of two branches, one from the posterior end of the cartilages and the other from the lateral walls of the posterior part of the buccal cavity and initial part of the oesophagus. It runs to the muscles of the foot passing posterior to the cerebral commissure and between the cerebropleural and cerebropedal connectives. These muscles are probably those described by Starmuhlner (1952) as retractors of the buccal mass. In Crepidula the muscle which was discussed as a possible levator could almost equally well be regarded as a modified depressor.

Neither levator nor depressor odontophoral muscles occur in neogastropods ; where levator muscles have been described, as in Urosalpinx (Carri ker, 1943), Nucellu, Buccinum, Nassarius (Burton, 1971) they are completely different, running from the middle to the anterior tip of each cartilage which they tilt upwards on contraction, an effect dependent on a greater degree of flexibility in the cartilages than is found in the other prosobranch groups.

Profroction of the subradu~ar membrane As the odontophore is brought forward and projected through the open mouth the

subradular membrane is pulled outwards over its tip. This brings about ten rows of radular teeth out of the groove on its dorsal surface, in which they normally lie folded away, over the bending plane and on to the ventral surface. As the radular ribbon passes over them the tips of the cartilages move apart so that it is laterally stretched and out- spread on the ventral side of the odontophore. This has the effect of erecting the teeth. Muscles involved in these movements are uniform throughout the prosobranchs, though modified in neogastropods with the formation of a proboscis.

Protraction of the subradular membrane involves two paired muscles, the median and lateral protractors and, at least in some animals, a tendon, Tendons have been most clearly described by Nisbet (1953) in Munodonta-indeed they have not been convincingly demonstrated elsewhere except perhaps in some neogastropods-and of the three which he mentioned only the nuchal tendon is important here. This runs from the inner end of the sublingual pouch to the musculature of the foot. Since the tendon is neither con- tractile nor extensible this is a fixed distance; on forward movement of the odontophore the inner end of the sublingual pouch remains immobilized and the subradular membrane is necessarily pulled over the odontophoral tip. I n addition to this passive movement an active traction on the membrane is initiated by protractor muscles.

328 A . GRAHAM

The median protractor muscles are inserted on the subradular membrane in the roof of the sublingual pouch, at the anterior tip or even slightly dorsal to that point, when the odontophore is at rest. Each runs posteriorly just within the roof of the pouch, ventral to the ventral approximator muscles of the cartilages (see p. 330); behind this they move dorsally, come to lie within the arterial sinus enclosed by the buccal membrane and thence pass into the radular artery close to where it, the pedal artery and anterior aorta all join. They are frequently anchored at this point by transverse muscle fibres connecting with the body wall on each side. The muscles then penetrate the vessel walls, enter the cephalic haemocoel and ultimately join the columellar muscle. They thus pass through the nerve ring and are, indeed, the only odontophoral muscles to do so. This is most obvious in mesogastropods where the nerve ring forms a tighter loop round the gut than in diotocardians; the muscles traverse it one on either side of the anterior aorta, ventral to the oesophagus and salivary ducts.

Muscles showing this pattern may be found in Monodonta (Nisbet, 1953-oblique anterior radular tensor), Littorina (Johansson, 1939-retractor of the bulbus ; A.G.), Crepidula, though not apparently in Pleurotomaria (Woodward, 1901), Viviparus (Starmuhlner, 1952) or Zanthina (Graham, 1965). They occur in diotocardian limpets like Patella (Amaudrut, 1898-pai, p’a‘i; Graham, 1964), Cellana (Schuster, 191 3-ventral tensor), Scutus (=Parmophorus, Amaudrut, 1898-pai, p’a’i) and Diodora but in these animals the muscles diverge laterally from the radular artery and originate on the anterior parts of the shell muscle.

Some variation occurs. In Nerita (Fretter, 1965) the anterior insertion of the muscles is to cartilaginous nodules in the wall of the sublingual pouch. In Haliotis Crofts (I 929) described (as ventral tensors, R.18) two muscles (Fig. 2, mpm) which originate in the walls of the anterior aorta at the point where buccal artery, radular artery, pedal artery and aorta all join and where they are enmeshed with muscle fibres running transversely in the vessel wall and with others running into the neighbouring haemocoelic spaces. From here they run to the anterior tip of the odontophore. Though called “tensors for the radular sheath” by Crofts these muscles are so precisely equivalent to protractors in other genera that this must be their true function and this had already been recognized by Amaudrut (1898) who called them retractors of the elastic membrane (rtel, r’t‘e‘l, fig. 49, plate VI).

Though the median protractors are remarkably uniform throughout diotocardians and mesogastropods this is not true of the neogastropods. In the genus Olivella a pair of muscles (Fig. 3, mpm) may be traced from the subradular membrane at the tip of the odontophore and from the roof of the sublingual pouch to a point where they unite with the columellar muscle after passing through the nerve ring. At the hinder end of the odontophore they are joined by two slips which come one from each side of the odontophore to which they are attached laterally, and dorsally in the region of the radular diverticulum. Posterior to the odontophore the muscles run on either side of the median proboscis artery (mpa). The relations of these muscles to subradular membrane, vessel, nerve ring and columellar muscle leave no doubt of their homology with the median protractors of lower prosobranchs, even if they have acquired new connexions with the muscles and cartilages of the odontophore. This development is of interest, however, in analysing the anatomy of other neogastropods.

Amongst the muricaceans, generally accepted as more primitive than the buccinaceans, Urosalpinx and Nucella show a pair of muscles arising from the columellar muscle just

BUCCAL MASS I N CHITONS AND GASTROPODS 329

posterior to the nerve ring, through which they pass alongside the anterior aorta. They then run forwards along the length of the proboscis one on either side of the median proboscis artery, which arises from the anterior aorta close to the origin of the main pedal artery, At the posterior end of the odontophore they diverge and insert on the hinder end of the odontophoral cartilages. The relations of these muscles in respect of everything except their insertions are so precisely those of the median protractors that it seems inevitable to recognize their homology, despite the fact that they now act as odontophoral retractors (Carriker, 1953-odontophoral retractor of Urosu[pinx ; Burton, 1971-odontophoral retractor of Nucella) rather than membrane protractors. Their course may easily be derived from the condition in Olivella by loss of the anterior extension to the subradular membrane.

In buccinaceans two arrangements are found. In Buccinum two muscles (Dakin, 19 12- centrodorsal muscle; Wilsmann, 1942-median radular retractor) insert on the anterior part of the subradular membrane and run posteriorly alongside the median proboscis artery, but instead of travelling the whole length of the proboscis to the nerve ring and columellar muscle, they diverge from the artery and end among ventrolateral bundles of longitudinal muscles of the proboscis wall, mainly retractors of the proboscis. It must be remembered, however, that these retractors are themselves partly extensions of columellar bundles so that the muscles correspond in most details of their course with median protractors ; their homology seems acceptable. In Busycon and Nussarius Burton (1 97 1) described muscles which also present much, though not total, similarity with the median protractors. In the former genus a pair of muscles (which Burton called ventral tensors of the subradular membrane) runs posteriorly from an attachment to the subradular membrane at the inner end of the sublingual pouch, one on either side of an (unnamed) median artery, to end amongst fibres of the most powerful retractor muscle of the odontophore, the ventral radular retractor; this lies around the median proboscis artery and has its origin amongst the bundles of longitudinal muscle in the proboscis wall. In Nussurius Burton described muscles (ventral odontophoral protractors) which also run posteriorly from the ventral wall of the sublingual pouch; behind this the fibres come together in the mid-line on either side of the median buccal artery (his name for the most anterior part of the median proboscis artery) and behind the odontophore join with the ventral radular retractor as in Busycon. Though the homology of these buccinacean muscles is more obscure, their associations with (1) the subradular membrane in the sublingual pouch, (2) the median proboscis artery and its extension the median buccal artery and ( 3 ) through the ventral radular retractor muscles with columellar bundles in the wall of the proboscis, are strongly suggestive of median protractor muscles now, clearly, with a different function. Change of function is already indicated in the muricaceans where the anatomical evidence supporting homology is very strong. In buccinaceans the great length of the proboscis would make the original arrangement of these muscles mechanically inefficient so that changes in anatomy and in function are perhaps not surprising.

As universal in occurrence as the median protractors and even more uniform in pattern are the lateral protractors of the subradular membrane. They insert on the membrane alongside the median muscles but more laterally, run back beside the median protractors, but have their origin on the posterior end of the cartilages, minor changes in the precise location of this being almost the only respect in which different animals vary. Throughout their course they lie ventral to the ventral approximator muscle of the cartilages. They are

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strap-shaped and more powerful than the median protractors. They are present in Patella (Amaudrut, 1898-inferior tensors, ti; Graham, 1964), Cellana (Schuster, 19 13-ventral tensor), Scutus (Amaudrut, 1898-ti), Diodora, Haliotis (Amaudrut, 1898--ti; Crofts, 1929-S.6; A.G.), Turbo (Amaudrut, 1898-ti), Monodonta (Nisbet, 19534irect anterior radular tensor), Nerita (Fretter, 1965), Littorina (A.G.), Crepidula, Ianthina (Graham, 1965), Ampullarius and Cypraea (Amaudrut, 1898-ti), Urosalpinx (Carriker, 1943- ventral subradular membrane protractor), Nucella (Burton, 1971-ventral protractor of the subradular membrane), Buccinum (Dakin, 1912-lateral radular retractor; Wilsmann, 1942-ventral tensor), Busycon (Herrick, 1906-protractor of the lingual ribbon; Burton, 1971-ventral tensor of the subradular membrane), Nassarius (Burton, 1971-ventral protractor of the subradular membrane) and Olivella. They are not recognizable in Woodward‘s description of Pleurotomaria and in Viviparus (Starmuhlner, 1952-protractor of radula; A.G.) are unusual in having their origin in the ventrolateral wall of the snout.

As the subradular membrane is protracted its lateral spread is augmented by a movement apart of the anterodorsal ends of the cartilages forming the main skeleton of the odontophore. This is brought about by a series of muscle bundles which run across the mid-line from cartilage to cartilage and which may, collectively, be called the ventral approximator of the cartilages, although the action which is of significance in the functioning of the buccal mass is the separation of their dorsal edges. The muscle fibres, however, are invariably attached to the most ventral parts of the cartilages and approximation of their ventral edges is accompanied by a lateral rotation of their dorsal ones. Though the majority of the fibres attach to the medial faces of the cartilages, in several species some or all may fasten to the ventral edge or lateral face: in this case the divaricating action of the muscle is direct and it could perhaps be more appropriately called ventral divaricator. The muscle occurs in all the prosobranchs which have been investigated except Olivella. Its absence in this genus and its weakness in other neogastropods reflect a tendency towards fusion and consequently reduced mobility of the cartilages in this group. It is muscle S.16 of Crofts (1929) in Haliotis, the transverse muscle of Woodward (1901) in Pleurotomaria and of Carriker (1943) in Urosalpinx, the spreader of the cartilages of Starmuhlner’s (1952) account of Viviparus, the ventral muscle sheet of Dakin (1912) in Buccinum (called horizontal muscle in Wilsmann’s description (1942) of the same animal) and the ventral sheet of cross fibres of Herrick’s account (1906) of Busycon. Fibres run from medial face to medial face in Patella, Diodora, Pleurotomaria, Crepidula, Viviparus and Buccinum; from ventral edge to ventral edge in Haliotis, Nerita, Urosalpinx, Nucella and Busycon; from lateral surface to lateral surface in Patella, Monodonta, Littorina, Ianthina and Nassarius. Since it is movement of the anterior parts of the cartilages which is important it is significant that this muscle is always present anteriorly but often fails to occur in the posterior half of the odontophore.

As the odontophore and subradular membrane are protracted they pull the radular sac forward, a movement aided and controlled by muscles linking the two structures. In Patella (Graham, 1964) small slips run from the median protractors to the wall of the radular sac; in Haliotis (Fig. 2, rt) from muscles linking the anterior cartilages back to the radular sac (Crofts, 1929-R.15; A.G.). This muscle is that erroneously believed by Amaudrut (1898) to be the homologue of the median protractors of the subradular membrane. In Monodonta Nisbet (1 953) described (as posterior ventral radular tensors) small muscular strands running from buccal sphincter to radular sac wall close to the


median retractors. In monotocardians these muscles appear to be absent: since the need to co-ordinate movement of odontophore and radular sac has not disappeared it must be met in some other way, perhaps by controlled relaxation of radular retractor muscles.

Dorsoventral movement of the cartilages The photographs of marks made by the radular teeth of feeding prosobranchs (Ankel,

1938) show that once the radula has been everted over the tip of the odontophore and applied to the substratum two things happen-the odontophore moves forwards over the substratum towards the dorsal lip and the radula starts to move backwards over the bending plane into the buccal cavity. The former movement is largely a continuation of the protractor movement by which the odontophore has been brought to the level of the mouth, now limited by contact with the substratum. Doubtless contraction of anterior levator and posterior buccal depressors (where they occur) helps to change the direction of movement of the odontophore. The retraction of the radula is the beginning of the next phase of the feeding process and is discussed below.

In addition, however, both Eigenbrodt (1941) and Nisbet (1953) reported that, once the radular teeth had been applied to food and held stationary in this position, the tips of the cartilages moved ventrally behind them. This movement might be followed by a dorsal one and that, in turn, by a second ventral one. This action has the effect of causing the teeth to erect or fold away according to the direction in which they cross the bending plane. Each time they are depressed they scratch the substratum and so possibly increase feeding efficiency. This behaviour seems to be confined to gastropods with rhipidoglossan and taenioglossan radulae. In Monodonta it is brought about by contraction of a muscle (called the outer approximator of the cartilages by Nisbet) which links the two cartilages of each side and, on contraction, rotates the anterior ventrally on the posterior. The same muscle is evident in Haliotis (Crofts, 1929-S.13) and perhaps the muscle described by Woodward (1901) as the lateral longitudinal permits this movement. There are also muscles of similar function in Diodora. Though alleged to occur in both Viviparus (Eigenbrodt, 1941 ; Nisbet, 1953) and Littorina (Nisbet, 1953) it is difficult either on the basis of Johansson’s work (1939) and Starmiihlner’s (1952) or of my own dissections of these animals to find any muscle by means of which it could be brought about. Though movement of the cartilages behind the subradular membrane to change the siting of the bending plane was part of Geddes’s (1879) interpretation of the mode of action of the stenoglossan radula, Burton’s (1971) work with Nassarius has shown that this does not occur.

Retraction of the subradular membrane Movement of the subradular membrane may be brought about in several ways, any or

all of which may be used by a given animal. Muscles may run from an attachment on the membrane back to the posterior parts of the odontophoral cartilages or from the initial part of the radular sac behind the radular diverticulum to the same origin: in either case contraction moves both radula and membrane backwards in relation to the rest of the odontophore. There are, in addition, other muscles which run from the radular sac to an origin behind the odontophore. They have retraction of the subradular membrane as one effect of their contraction but also bring about retraction of the entire odontophore. The

332 A . GRAHAM

extent to which each of these things happens depends upon the species and upon other muscles. The degree of development of the different muscles in prosobranchs is related to the kind of radula which they possess since it is largely against the friction between teeth and substratum that the retracting force must act, but there is also an evolution in the efficiency of the machinery between lower and higher forms.

In prosobranchs with rhipidoglossan radulae friction with the substratum is minimal so that membrane and radular retractor muscles tend to be weak. Those with taenioglossan radulae, however, apply their teeth with some pressure against food, and in docoglossans the radular teeth are forced longitudinally over the substratum with great power (Ankel, 1938). In such animals the retractors are hypertrophied and constitute the largest bulk of muscle in the buccal mass. In most diotocardians and mesogastropods the movement is brought about by muscles which run from the subradular membrane or the walls of the initial part of the radular sac, or both, to the posterior ends of the cartilages. Two pairs are distinguishable, the retractors of the subradular membrane and the retractors of the radular sac, though varying degrees of fusion may be present. In general terms both pairs pass internal to the buccal membrane and so ventral to the dorsal odontophoral protractors. They are also ventral to all the muscles running into the transverse fold, to the buccal ganglia and commissure, and medial to the lateralprotractors, the buccal levators and buccal depressors.

In Diodoru retractors (Fig. 1, rsm) insert on much of the subradular membrane, dorsally and laterally and run back to the lateral face of the posterior end of the posterior cartilage; their course ensures-as in other genera-that contraction not only retracts the membrane but brings the dorsal parts of the cartilages together, helping to fold the radular teeth into the groove on the odontophore. At a deeper level, bundles of radular retractors pass from the lateral walls of the radular sac to the medial face of the same cartilages. The same two pairs of muscle recur in Neritu (Fretter, 1965), though anterior fibres attach to the main cartilage in this animal, in Vivipurus (Starmuhlner, 1952- radular tensors, radular folders ; A.G.), Ampullarius (Amaudrut, 1898-superior median tensor, tsm), Cypraea (Amaudrut, 1898--tsm), Crepidulu, Iunthina (Graham, 1965), Tonna (Weber, 1927). In Littorinu Johansson ( 1939-m8) described only membrane retractors but deeper dissection reveals radular retractors as well. In Huliotis the retractors of the subradular membrane take the form of a few bundles of muscle which run to the floor of the anterior radular sac, to the dorsal parts of the subradular membrane at the level of the radular diverticulum and anterior to that, from an origin on the more posterior parts of both cartilages. Anterior and median fibres run to the ventral side of the main cartilage; anterior and more laterally inserted fibres, and all posterior ones, run to the ventral side of the posterior cartilage (Crofts, 1929-S.7; A.G.). Crofts did not describe muscles recognizable as radular retractors but a muscle (Fig. 2, rr) extends from each anterolateral wall of the radular sac anteriorly to the posteromedial face of each posterior cartilage. It is difficult to extricate from Nisbet’s (1953) elaborate account of Monodonta any muscle precisely equivalent to the membrane retractors, although radular retractors are clearly present (posterior radular retractor). A muscle which Nisbet called ventrolateral tensor of the elastic membrane qualifies, in terms of attachment to cartilage and membrane, for consideration as the homologue of the membrane retractor, and this is supported by his statement (table, p. 258) that it is homologous with the dorsal longitudinal muscle of Pleurotomuriu (Woodward, 1901), a muscle which Fretter’s later

BUCCAL MASS I N CHITONS A N D GASTROPODS 333

description of Mikadotrochus amabilis (1964) showed was undoubtedly a retractor of the subradular membrane. It is not possible to be certain of a radular retractor in pleuroto- marians. In docoglossans such as PatelZa (Graham, 1964) both muscles are clear and separate and the membrane retractor, in particular, has hypertrophied to a great mass of fibres which run from an attachment to the more posterior parts of the subradular membrane backwards and through the ventral part of the odontophore to a similar contro- lateral insertion, as well as sending branches to the small anterior cartilages, the jaw and the inner lips. Many of these bundles are the intercartilage muscles described by Amaudrut (1 898-malss, malsm, malsi, mlils, mlis, mlii, pls, pli).

In the mesogastropod Tonna (Weber, 1927) which is provided with a proboscis, an approach is made to the neogastropod position in that strong retractors run from the sides of the odontophore back to an origin on the lateral walls of the proboscis.

Among neogastropods this group of muscles is, like others, different in muricaceans and buccinaceans, with animals in the former taxon (and with them the volutacean OZivella) showing a greater similarity to the lower gastropods. Both Carriker (1943) and Burton (1971) have described, in Urosalpinx and NuceZZa respectively, powerful muscles which they named dorsal and either ventral (Carriker) or lateral (Burton) retractors of the subradular membrane, which insert on the membrane and radular sac and pass thence partly to an origin on the posterior parts of the cartilage and partly (dorsal muscles only) to join lateral odontophoral retractors which attach to the wall of the proboscis. Except in this last respect these muscles match those of lower prosobranchs, and provide much of the power for the inward movement of the subradular membrane. In buccinaceans, however, as first pointed out by Burton (1971) a different mechanism exists: the retraction of the feeding organs is primarily due to a powerful pull on the radular sac by muscles running to an origin on the proboscis wall. These muscles link anteriorly with a tensor system which transmits the pull to the rest of the odontophore. At least part of this system is formed by muscles running from cartilage to subradular membrane (Nassarius only- lateral retractor of the membrane), or from cartilage to the lateral walls of the radular sac (in Nassarius4ateral radular retractor; in Buccinum-lateral tensor 1 (Wilsmann, 1942)=dorsal radular retractor 1V (Dakin, 1912)=superior median tensor (Amaudrut, 1898); in Busycon-part of the great retractor of the radula (Herrick, 1906)). These muscles, it seems likely, are homologous with the membrane and radular retractors of the muricaceans and lower prosobranchs, but, as with other muscles of the buccinacean buccal mass, have a new function. The last muscle described by Burton in the tensor system, the median retractor of the membrane, seems to be homologous with a muscle which occurs sporadically throughout the prosobranch series, acting as a short tensor linking radular sac and membrane (like the anterior tensor of the radular sac in Patella (Graham, 1964)) and ensuring co-ordinated retraction of these two structures.

As the radula is withdrawn over the bending plane the teeth fold into the groove on the dorsal surface of the odontophore. Several muscles aid this. In many lower prosobranchs protraction of the jaw causes it to press against the odontophoral tip with increasing pressure as the two approach one another. The force exerted by the protractor of the jaw helps to fold the radula away, just as at an earlier stage in the cycle it had helped to keep it flat. Contraction of the protractor also helps to keep the mouth open. Should the radula have strands or pieces of food caught in the teeth some cutting action may occur at this time in those animals in which the jaw is a robust structure.

334 A. GRAHAM

Folding of radular teeth is also helped by the fact that the membrane retractors run from the lateral side of the cartilages over their dorsal edges towards their insertion on the mid-line and so bring the cartilages closer on contraction. Approximation of the cartilages is actively brought about in a rather small number of prosobranchs by a dorsal approximator muscle. Such muscles, with fibres running from the dorsal or lateral surface of one cartilage to the corresponding point on the other, have been described only in the buccinaceans Nassarius (Burton, 1971-dorsal approximator), Buccinum (Dakin, 1912- circular muscle sheet; Wilsmann, 1942-circular muscle 4) and Busycon (Herrick, 1906- dorsal cross fibres), but there are other muscles in other prosobranchs which could achieve the same effect. Most prosobranchs, indeed, have a circular muscle sheet around the whole anterior end of the buccal mass (Fig. 3, bcm) contraction of which helps to bring cartilages closer, but which is primarily involved in shutting the mouth (described on p. 336). In Haliotis and Crepidula there is also a constrictor muscle which is attached ventrally on each side to the odontophoral cartilage and runs dorsally over the odontophore between these points, lying dorsal to the radular diverticulum and ventral to the oesophagus. It is dorsal to the buccal ganglia in HaZiotis but ventral to them in Crepidula. It is the constrictor muscle, C.2, of Crofts (1929).

Retraction of the odontophore As the tip of the odontophore approaches the dorsal lip a withdrawal into the body

cavity begins. In most diotocardians and mesogastropods this is largely a passive process starting as soon as the protractor muscles relax and brought about by pressure from surrounding parts of the head, though some muscles do help. In neogastropods the placing of the buccal mass at the tip of an extended proboscis with relatively weak muscular walls reduces the forces able to cause return and muscles become primarily responsible. It follows that the degree of development of odontophoral retractor muscles is very different in the two groups.

In Munodonta an apparently single muscle, probably formed by fusion of a pair (Nisbet, 1953-postmedian retractor of the radula), runs from the columellar muscle to the ventral surface of the radular sac at the level of the posterior end of the odontophore. The muscle is stretched by protraction of the odontophore and its contraction helps to return it to the resting position. Nisbet noted, however, that the muscle is not used to maintain the buccal mass in that situation since it is then relaxed. In Haliotis (Fig. 2, mrr) a similar muscle (Amaudrut, 1898-radular retractor, rtp; Crofts, 1929-R. 19, median retractor; A.G.) runs from the ventral surface of the radular sac to an origin amongst pedal muscles. Its course is similar to that of the retractor in Munodonta-penetrating the buccal membrane (bm) to lie in the venous haemocoel, passing left of the anterior aorta (aa), anterior to the sub- (sbc) and supra-oesophageal (SOC) connectives but posterior to the pedal commissure, and reaching into the foot. It shows no trace of pairing. In Diodora, however, it is double throughout its course, one muscle passing on each side of the pedal artery to enter the foot in a venous channel linking cephalic and pedal sinuses just posterior to the pedal commissure. It is paired too in Pleurotomaria (Woodward, 1901-ventral retractors). It is not present in Patella (Graham, 1964) nor in Nerita (Fretter, 1965). Amongst mesogastropods it is absent in Crepidula, Ianthina (Graham, 1965) and Littorina (Johansson, 1939; A.G.). Only in Viviparus can a tentative homologue be discovered in the muscle described as a radular retractor by Starmuhlner (1952), though his description is not

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wholly accurate (if my identification of the muscle under discussion is correct). The muscle originates in the mid-line amongst foot muscles, posterior to the pedal commissure but anterior to the suboesophageal connective, and passes to the ventral surface of the inner end of the radular sac. Here it bifurcates, the two halves entering the radular sheath and attaching one to each side of the radular sac.

Though these muscles are well developed none can retract the odontophore without help from other sources. In neogastropods these aids no longer operate to the same extent or do not function at all. Odontophoral retractor muscles are therefore stronger and are usually the largest in the buccal mass, though it must be remembered that they are also involved in retraction of the subradular membrane and the radula-indeed, it is impossible to separate the three movements-and that radular action is more powerful. Neogastropod arrangements are complicated by the way in which the evolution of a proboscis prevents any anchoring of a retractor muscle in pedal musculature. Instead a new connexion is established with the retractor muscles of the proboscis, which are anterior branches of the columellar muscle.

The buccinaceans (in contrast to what has been said about other muscles) seem to be more primitive than the muricaceans in respect of this one, in that the whole bulk of the massive retractor muscle runs from the wall of the radular sac to the ventral half of the proboscis wall. It can be compared with a median retractor of the radula composed of paired bundles which have come together to produce a single muscle. It is found in Nassarius (Burton, 1971-ventral radular retractor), Buccinum (Dakin, 1912-dorsal longitudinal muscles ; Wilsmann, 1942-radular retractor) and Busycon (Herrick, 1906- ventral radular retractor). In the muricaceans there is no muscle which can be unequivocally homologized with the median radular retractor. Instead, a different evolutionary line seems to have been followed and an innovation introduced by which some part of the retractors of the subradular membrane extend out of the odontophore and establish a link with retractor bundles in the wall of the proboscis. These are found in Urosalpinx (Carriker, 1943-lateral odontophoral retractors) and in Nucella (Burton, 1971-lateral odontophoral retractors). There is nothing comparable in diotocardians, mesogastropods or buccinaceans. In the volutacean Olivella an odontophoral retractor muscle (Fig. 3 , lor) arises on the dorsal parts of the cartilage on each side, from the subradular membrane of the floor and lateral edges of the radular diverticulum and runs back to the hinder end of the odontophore. Here it is joined by a branch from the side of the radular sac and then runs posteroventrally to join the proboscis retractor bundles (pr). This is like the arrangement of retractor muscles in another volutacean, Marginella marginata (Graham, 1966). This pattern is to some extent intermediate between what is found in muricaceans and buccinaceans, but looks nearer to the latter, in which case the connexion to the radular sac may represent a paired retractor of the radula (otherwise not present) which has acquired an extension to the subradular membrane.

In addition to radular retractors, muscles involved with other activities in mesogastropods have been recruited to help with retraction in neogastropods. It has already been suggested (p. 333) that the muscles lying alongside the median proboscis artery and acting as odontophoral retractors in Olivella, Urosalpinx and Nucella are the original median protractors of the subradular membranes adapted for a new function, and that the same muscles, along with the lateral protractors, have become integrated into the anterior portion of a retractor system in buccinaceans.

336 A . G R A H A M

Closing of the mouth Like retraction of the odontophore this is partly a passive process and is followed by

immediate re-opening for the next feeding cycle. Parts of the process, however, are accelerated by muscular action and there are occasions unrelated to feeding when the mouth has to be forcibly shut.

The muscle of most regular occurrence to bring this about is a ring lying around the oral tube and most anterior part of the buccal cavity (Fig. 3, bcm). It is often better developed dorsally, where the gut continues to the oesophagus, than ventrally. The muscle is almost universal in prosobranchs and is a development of the circular musculature of the original stomodaeal wall. It has been described in Monodonta (Nisbet, 1953- outer, inner buccal constrictors), Haliotis (Crofts, 1929-S.2, sphincter), Nerita (Fretter, 1965), Viviparus (Starmiihlner, 1952-sphincter) and Littorina (Johansson, 1939-m,,). It is absent in Pleurotomaria (Woodward, 1901), Diodora and Patella (Graham, 1964) in which closure of the mouth is indirect. Among stenoglossans it has been described in UrosaZpinx (Carriker, 1943-buccal circular muscle), Nucella (Burton, 1971-buccal circular muscle), Buccinum (Wilsmann, 1942-circular muscle l), Nussarius (Burton, 197 1-buccal circular muscle) and Busycon (Herrick, 1906-ring muscle).

Some subsidiary events accompany shutting of the mouth. The jaws are retracted after the odontophore has passed them. A retractor muscle runs from the anterior (dorsal) surface dorsally to the wall of the snout. As it contracts the protractors of the odontophore relax so that tension is reduced in the branches to the jaw and the buccal roof. The pressure of blood in the cephalic haemocoel must be responsible for pushing such structures as the dorsal and inner lips back to their resting position since no muscles are present which could bring this about.

Swallowing of food The events analysed in the seven previous sections lead to the point where the radular

teeth, with whatever food they have collected, have been brought with the odontophore into the buccal cavity. The food is now passed from the radula into the oesophagus, mainly by way of the dorsal folds and food channel on the roof of the buccal cavity. These structures bear cilia beating into the oesophagus, but muscular suction and peristalsis also help. Another area of importance in swallowing is the transverse fold.

Muscular dilatation and constriction of the buccal roof are easily visible in living preparations of prosobranchs and provide both a suction removing food from the radula and a propulsion along the oesophagus. The former action is due to the irregularly arranged series of buccal and oesophageal dilator muscles which cross the haemocoel from gut wall to body wall; the latter is the result of contraction of circular muscle fibres in both buccal and oesophageal walls. The two sets of muscles are found in every prosobranch, but the second is only weakly developed in diotocardians where the transport of food along the oesophagus is primarily by means of cilia.

Movement of the transverse fold appears of considerable importance in transferring food from radula to oesophagus, and may also be involved in keeping food out of the radular diverticulum. It is an extremely mobile structure supplied with numerous slips of muscle connected to different parts of the buccal mass. Of these muscles the most regular in pattern and occurrence is a pair of retractors which have their origins on the lateral

B U C C A L MASS I N CHITONS AND GASTROPODS 337

walls of the radular sac and run forward along the sides of that structure to fan out into small bundles extending across the breadth of the fold. Contraction of these muscles pulls the transverse fold backwards and widens the oesophageal aperture. The muscle lies within the buccal membrane and so is dorsal to all muscles except the dorsal odontophoral protractors. It is also mainly dorsal to the buccal ganglia and their commissure, though some slips-the number varies from species to species-pass ventrally. The retractor of the transverse fold occurs in Patella (Graham, 1964), Diodora, Haliotis, in which several strands can be recognized running (1) from radular sac to fold (Crofts, 1929-D.lu; A.G.), (2) from oesophageal wall to fold (Crofts, 1929-part of R.1, lateral retractor; A.G.) and (3) from buccal membrane to fold (A.G.), Monodontu (Nisbet, 1953-retractor muscle of the transverse fold, tensor muscle of the caecal folds, posterior radular tensor muscle), Neritu (Fretter, 1969, Littorina (Johansson, 1939-m, ?), Crepidula, Viviparus (A.G.). It is found in Olivella where its origin, however, is on the posterior end of the cartilage rather than on the radular sac, but it does not seem to occur in any other neogastropod.

In addition to this muscle there are, in some prosobranchs, others which could affect the transverse fold. In Patella (Graham, 1964) an oblique retractor runs from the fold to the anterior end of each main cartilage and on contraction pulls the fold ventrally. This effectively closes the mouth of the radular diverticulum, and at the same time, aids the retractor in dilating the opening into the oesophagus. It can also be recognized in Diodora, may have been described as muscle m3 by Johansson (1939) in Littorim and is perhaps present in Olivellu, where a muscle runs from the fold ventrally on each side to the cartilage. Though not the same muscle, the constrictor of Haliotis (Crofts, 1929-C.2) and of Crepidula has largely the same action.

A combination of sucking, dilatation of the oesophageal opening and approximation of food channel walls to radula brings about transfer of the collected food to the oesophagus in diotocardians and mesogastropods. In neogastropods these processes are important but so, too, is another-the dorsal tilting of the odontophore to bring the food into an easier position for entry to the oesophagus. The levator muscles of the cartilage are responsible for this : they have both origin and insertion on the cartilage and bend that structure dorsally at its tip as it is withdrawn so that teeth and food are pressed towards the oesophageal aperture. This kind of movement is not possible in lower prosobranchs in which the cartilage is too rigid for bending to take place.

Amphineurans Although there is no account of feeding in chitons comparable in detail with those of

Ankel (1937, 1938) for prosobranch gastropods there is every reason for supposing that it involves similar behaviour of odontophore and radula. It is not surprising then, that a comparable anatomical organization can be discerned. Provision must also be made, however, for an extra degree of mobility in the roof of the sublingual pouch since Heath (1903) showed that the subradular organ, a sensory structure located there and provided with a local ganglion, is protruded to test all food before it is eaten.

The most important features of the buccal musculature of Lepidochitona cinereus are shown in Figs 4 and 5. It is not always easy to relate these to previous findings described by Sampson (1895) for Chiton olivaceus Solander and C. viridis Quoy and Gaimard or to those for Acanthopleura echinata (Barnes) and the eight other species described by Plate

338 A. G R A H A M

(1897). The results of the latter worker are summarized by Fischer-Piette & Franc (1960) and Hyman (1967) and reference to this will be made by quoting the numbers allocated to the muscles by Plate and reproduced in these two texts.

2 mm bd df

I a05 aa 1 mrn

FIG. 4. (a) Dissection of anterior end of Lepidochitona cinereus, in dorsal view. The anterodorsal body wall, the front end of the aorta and oesophagus and the buccal roof have been removed. (b) Dorsal view of deeper dissection of odontophore after removal of subradular membrane and radular sac. (Explanation of abbreviations see p. 348.)

As in prosobranchs irregularly arranged buccal dilator muscles (bd=muscles 26, 27, 31, 34) run from the buccal roof to the body wall under shell plate I. Lateral protractors of the odontophore (lpo=muscles 6, 7) and ventral protractors (Fig. 5, vpo=muscle 15) run from the posterior ends of the cartilages to the body wall around the mouth and into its lips, which bring the odontophore forward and open the mouth. Dorsal odontophoral protractors are not present.

The level at which the odontophore arrives at the mouth is under more elaborate control than in gastropods. Powerful buccal circular muscles (muscle 28), supplemented by a pair of bundles belonging to the lateral protractors (Fig. 4, blp=muscle 8) which run from the posterior end of each cartilage to the buccal roof, can pull the dorsal wall of the oral tube and buccal cavity-there are no jaws-down on to the upper surface of the odontophore so as to push it towards the mouth and keep the radular teeth from erecting. The action of these muscles can be opposed by that of two other pairs, the anterior levators and posterior depressors of the odontophore, and aided by two further pairs, the posterior levators and anterior depressors. The anterior levators (Fig. 4, al, ? not described by Plate) run from the ventral surface of each cartilage to an origin on transverse muscle 2

BUCCAL MASS IN CHITONS A N D GASTROPODS 339

in the dorsal body wall (tm 2); they are very directly antagonized by a pair of anterior depressors (muscle 14) which run ventrally from a similar attachment to the cartilage to the musculature of the floor of the head-foot. Posterior levators (PI=? muscle 9) run forward from an insertion on the posterior end of each cartilage to an origin on transverse muscle 1 (tm l), while posterior depressors (pd=muscle 11) go from the same insertion area to an origin in the midventral body musculature.

va

' I m m I

vim

FIG. 5. Dorsal view of deep dissection of odontophore and some posterior structures of Lepidochitonu cinereus. (Explanation of abbreviations see p. 348.)

Protraction of the subradular membrane and of the radula is brought about by three pairs of muscles, the median, lateral and outer protractors. All insert on the subradular membrane at the tip of the odontophore and on the roof of the sublingual pouch. The first (mpm) run backwards and dorsally to attach to the underside of the third shell plate. The lateral protractors (lpm) pass ventral to the cartilage in Lepidochitona to an origin among lateral pedal muscles; in Kuthariiza, however, they originate, as in prosobranchs, from the posteromedial face of each cartilage. The outer protractors (not present in prosobranchs and perhaps associated with the extra mobility required in this area for use of the subradular organ) are inserted further from the mid-line than the others (Fig. 5, opm), at the lateral margins of the sublingual pouch, and run, slightly medially, to an origin among ventral muscles just anterior to those of the posterior depressors (pd). These three pairs are muscles 20, 21, 22 of Plate (1897). Spreading of the radular teeth is helped by a divarication of the cartilages due to a ventral approximator muscle (va= muscle 1).

Retraction of subradular membrane, odontophore and radula is due to the action of a series of muscles of which four pairs, the retractors of the subradular membrane, the radular retractors, the dorsal and the posterior radular retractors, are the most important.

340 A . GRAHAM

All four interconnect with one another to a marked extent and form what appears to be a single functional unit. The retractors of the subradular membrane (rsm=muscles 2, 3,4) are the most powerful part of the complex and run dorsally from an origin on the ventral side of the cartilages, round their lateral surfaces to an insertion mainly on the subradular membrane of the floor of the radular diverticulum but also extending on to the radular sac. The most anterior bundles have the most lateral insertion, those lying more posteriorly attach to the membrane close to the mid-line whereas the most posterior insert on the lateroventral walls of the radular sac. Intermingled with the last group are other bundles which may be divided into two sets according to their origin: one set (Fig. 4(a), drr= muscle 17) runs to shell plate I1 and may be distinguished as dorsal radular retractors; the second set, the posterior radular retractors (prr), runs more posteriorly to an origin on shell plate 111. The fourth pair in this group (Fig. 4(b), rr=muscle 10) is directly comparable to the radular retractors of prosobranchs in running from the lateral walls of the radular sac to the medial face of each cartilage.

Other muscles involved in retracting or anchoring the odontophore are (1) an unpaired muscle which runs from the mid-ventral part of the sublingual pouch to the mid-ventral body wall (muscle 42), and (2) a pair of muscles, the odontophoral retractors (Figs 4(b) and 5, or=muscle 14), which run from the posterior ends of the cartilages to join body wall muscles. The former muscle appears to have no homologue in prosobranchs, but the latter pair may be compared with the odontophoral retractors of Haliotis, Diodora, Monodonta (postmedian retractor of Nisbet) and Viviparus.

As in prosobranchs some manipulation of the transverse fold is involved in the transfer of food from odontophore to oesophagus. This is mainly achieved by a muscle, comparable to the retractor of the transverse fold in prosobranchs, which runs from an origin on the posterior part of the radular sac to an insertion on the sides of the transverse fold (Fig. 4(a), rtf=muscle 41).

The means by which the subradular organ is used are not clear. There is n o muscle which could evert the roof of the sublingual pouch independently of other structures so that its movement towards the mouth must be associated with that of the odontophore and this can be verified by watching a chiton feeding. To bring the subradular membrane forward relative to the rest of the odontophore calls for the contraction of such muscles as the retractors of the subradular membrane and radula at a time when they are relaxing to permit protraction of the odontophore. Since Heath (1903) and Fretter (1937) both stated that food is regularly tested by the subradular organ before being eaten some interruption of protrusion of the odontophore must occur at a time before the radular teeth make contact with the substratum. If the result of the testing is satisfactory the process is completed and the next phase in the feeding cycle (protraction of the subradular membrane) automatically retracts the subradular organ to its resting position in the roof of the sublingual pouch.

Discussion On the basis of what has been said on previous pages a strong argument can be developed

for believing that the buccal mass of all prosobranchs conforms to a common anatomical pattern which has been modified to adapt it for different uses, and that the amphineuran buccal mass also exhibits the same fundamental structure. Before discussing these points it is helpful to outline the basic organization (Fig. 6).

BUCCAL MASS I N C H I T O N S A N D GASTROPODS 34 1

The odontophoral part of the buccal mass lies within an arterial space bounded by a membrane (bm) which is continuous with the wall of the anterior aorta (aa). There are windows in this membrane, especially anteriorly and ventrally, which allow the space to communicate with the venous haemocoel of the head and also give passage to muscles.

ho r t f cm rs Im nr

ipm mpm rsm bm r t pa prr dl m bs v l

bm pd Pa

VPO

FIG. 6. Two diagrammatic representations of the generalized prosobranch buccal mass, seen from the left. Arterial spaces are stippled. The insertions of muscles are shown branched. (a) Shows body wall muscles, jaw muscles, membrane protractors, membrane and radular retractors and the ventral approximator. (b) Shows odontophoral protractors, levators and depressor. (Explanation of abbreviations see p. 348.)

The angle at which the odontophore lies within the buccal cavity is partly controlled by levator (al, pl) and depressor (pd) muscles which run more or less vertically from the cartilages to the body wall.

342 A. GRAHAM

There are two essential components in the activity of the odontophore: (1) a forward and backward motion of the whole odontophore within the buccal cavity and oral tube, and (2), superimposed upon this, a protraction and retraction of the subradular membrane carrying the radular teeth. Movement of the membrane goes on simultaneously with, but faster than, the corresponding movement of the odontophore, so that rows of radular teeth are pulled outwards over the bending plane during protraction of the odontophore and inwards over it on retraction. There must therefore be two sets of antagonistic muscles, the protractors and retractors of the odontophore and the protractors and retractors of the subradular membrane, the activity of all four being co-ordinated. The two sets differ in that odontophoral protractors are more powerful than odontophoral retractors, but membrane retractors are more powerful than membrane protractors.

The strength of the odontophoral protractors is necessitated by the fact that forward motion of the odontophore towards the tip of a tapering snout takes place against the resistance of the body wall and because the odontophore has to be actively held in the protruded position. Return of the protruded odontophore is aided by the body wall musculature and starts automatically as soon as the protractor muscles stop their contraction : muscles directly responsible for return, therefore, are weak by comparison with the protractors. Some protraction of the subradular membrane is a direct consequence of forward movement of the odontophore, some is brought about by the contraction of special muscles, but they are not, for this reason, particularly powerful. The muscles responsible for the retraction of the membrane, however, are those causing the feeding strokes of the radular teeth and are amongst the most powerful in the buccal mass.

The odontophoral protractors (dpo, Ipo, vpo) lie partly embedded in the arterial membrane, partly internal to it, forming a cone-shaped array of muscles running from the posterior end of the cartilages to origins in the anterior body wall and lips. The protractor layer is least developed dorsally and becomes progressively more massive towards the ventral mid-line. The odontophoral retractors consist merely of a pair of strands from the posterior ends of the cartilages or (more commonly) radular sac to the body wall behind the buccal mass. These are the posterior odontophoral or posterior radular retractor muscles (prr).

The muscles responsible for protraction of the subradular membrane are lateral protractors (Ipm), from subradular membrane to the posterior ends of the cartilages, and median protractors (mpm), which run back through the nerve ring to join the columellar muscle, of which they are branches. Radular tensors (rt) help to co-ordinate movement of the radular sac and membrane. The erection of the radular teeth as they move over the bending plane is aided by a moving apart of the dorsal edges of the front ends of the cartilages due to contraction of their ventral approximator muscle (va). There are two pairs of muscles responsible for retraction of the membrane: retractors of the subradular membrane (rsm) and radular retractors (rr). The former are massive muscles running from cartilage to membrane and radular sac in such a way that they not only retract the membrane but bring the cartilages together and so help to fold away the radular teeth.

Swallowing requires movements of buccal wall and transverse fold brought about by buccal dilators (bd), buccal circular muscles (bcm) and a retractor of the fold (rtf).

These are the muscles which carry out the basic movements of feeding in both prosobranch gastropods and amphineurans. There are others which perform a variety of ancillary functions, primarily by acting as local tensors, but one of the obvious evolutionary


trends which can be noted is their gradual elimination. Thus in Acanthopleura Plate (I 897) listed no less than 38 different buccal muscles (the number can be reduced to about 30 by grouping) and Nisbet (1953) 33 in the diotocardian Monodonta, whereas Burton (1971) described 24 in Nassarius and Carriker (1943) only 15 in Urosalpinx. When the details of the musculature are examined it is found that, with the exception of levators and depressors, all the primary muscles described above persist throughout the series : simplification involves loss only of ancillary muscles. There is more than one reason for this: one is an increasing organization of the head, a second is a changing activity of the radula, a third is the simpler use of the buccal mass which results from the evolution of a proboscis.

The most primitive gastropods have a rhipidoglossan radula, a structure which brushes rather than scrapes the substratum. No great power is required for this, but many minor adjustments of position and tension are. With taenioglossan or stenoglossan radulae this fine control is unnecessary, but greater power is needed to scrape the substratum with coarser teeth, and in prosobranchs with docoglossan radulae the demand for power is still greater. A comparison of the musculature of the rhipidoglossan, taenioglossan and docoglossan buccal mass shows the abandonment in the two last types of the ancillary muscles required for adjusting the odontophore in the first, but the retention and strengthen- ing of the muscles responsible for fundamental odontophoral movements. The typical mesogastropod odontophore therefore contains only buccal dilators and constrictors, protractors and retractors of the odontophore, protractors and retractors of the subradular membrane and a ventral approximator of the cartilages, A reduction in the number of cartilages also strengthens the odontophore by lessenihg flexibility. In docoglossans some of the great hypertrophy of the musculature derives from the fact that multiple cartilages are still present and must be held firmly during the use of a radula that requires rigidity and stability for proper functioning.

The radula of chitons seems to behave like that of taenioglossans yet the buccal mass has even more muscles than are found in rhipidoglossan prosobranchs. Since this can hardly be due to the need for accurate control it must be assumed either that complexity is archaic and that in the evolution of the odontophore improving efficiency has led to a secondary simplicity in structure, or that there is some special feature of polyplacophoran anatomy which requires many muscles. Both points, indeed, may be involved. In chitons the head is poorly developed, is much less mobile than in prosobranchs and the dorsal wall is made rigid by the anterior valves of the Shell. In gastropods, by contrast, the head is an agile structure with a flexible and muscular wall, which, as has been seen, is part of the apparatus by which the odontophore is manipulated. In the absence of this a more elaborate musculature is needed by chitons to do the same work.

If this is a valid argument it must apply equally to monoplacophorans whose head is also little developed and roofed by shell. When the description of Neopilina given by Lemche & Wingstrand (1959) is studied it is easy to pick out muscles which correspond to those of other molluscs. The following can be recognized: ventral approximator (m. impar radulae of Lemche & Wingstrand), protractors of the odontophore (mm. protractores vesicae major, minor along with mm. vesicae anteromediulis, anterolateralis and mm. protractores cartilaginis dorsalis, profundus), protractors of the subradular membrane (m. radulae longus), retractors of the subradu1a.r membrane (m. retractor radulae), retractors of the odontophore (mm. vesicae posterolateralis, posteromedialis, ventralis) and dilators

344 A. GRAHAM

of the buccal cavity (m. pharyngeipraeorulis, m. praeoralis). (It will be noticed that in this list I disagree with Lemche & Wingstrand about the use of m. radulae longus: they ascribed to it retraction of the radula and stated that it is the main feeding muscle. In view of its identity of course with the protractor of the subradular membrane in chitons and diotocardians I believe that this must be its function in monoplacophorans too.) In addition to these muscles, however, Lemche & Wingstrand listed a further 11, mainly concerned with steadying parts of the feeding apparatus. Though the total number of muscles in Neopilina is less than in a chiton, there is indeed a comparable number of ancillary muscles.

The neogastropods-toxoglossans are excluded from the following discussion-stand out from other prosobranchs in their buccal anatomy and in the use to which they put their radula, and are specialized in the possession of a proboscis. It is true that some higher mesogastropods also have a proboscis but its presence has had only a minor effect on their buccal mass whereas it has caused a profound re-arrangement of anatomy in the neogastropods. The length of the proboscis is interposed between buccal mass and nerve ring, two structures primitively close together, and between buccal mass and columellar muscle, to which some buccal muscles originally attach. The mouth is terminal instead of ventral as in lower prosobranchs and the proboscis is narrower in diameter and less muscular than their cephalic wall. All these features have their effects on the organization and functioning of the buccal mass. Since the length of the proboscis is least in such animals as muricaceans and volutaceans and greatest in buccinaceans the changes in anatomy are most noticeable in the last group.

In association with the simpler piston-like action of the odontophore in animals with a terminal mouth the odontophoral protractor muscles become more evenly developed dorsally and ventrally; levator and depressor muscles, already sporadic in mesogastropods, are lost. In accord with the dimensions of the proboscis the odontophore has narrowed and elongated; this alone may be an adequate explanation of the origin of the rachi- glossan type of radula. The resulting slenderness of the cartilages is such that (retaining the same histological structure) they flex under the pull of the protractors, and a variety of corrective measures have to be taken (Burton, 1971) to prevent their buckling as the odontophore is pulled forwards. Their flexibility is so great that, were they to give origin to muscles sufficiently powerful to retract the subradular membrane during feeding (and running, as in mesogastropods, from cartilage to membrane) they would bend, and little or no retraction would follow. This situation cannot, however, arise because the narrowness of the proboscis does not permit the development of muscles of such a size within the odontophore. There are thus two reasons why retraction of the subradular membrane can be achieved only by transferring the muscles responsible to a position outside and posterior to the odontophore, with their origin on the walls of the proboscis. The major retractive effort, in all neogastropods, is then applied primarily to the walls of the radular sac though some is transmitted to the posterior tips of the cartilages, where it has no flexing effect.

In muricaceans and volutaceans, with a shorter proboscis, part of the original arrangement persists in that a few retractor fibres still run from the subradular membrane to the posterior ends of the cartilages, but these have been lost in buccinaceans. In the two former groups the pattern of insertion of fibres-some on the membrane, some on the cartilages, some on the radular sac-ensures the co-ordinated withdrawal of all three parts. In

BUCCAL MASS IN CHITONS A N D GASTROPODS 345

buccinaceans the pull is applied only to the radular sac and has to be relayed to other structures by a special system of tensor muscles (Burton, 1971) derived from a transformation of the original retractors of the membrane and the radula. In this way the buccinacean odontophore has become one of the most highly modified in the whole prosobranch series.

In addition to changes due to the narrowness of the proboscis its elongation in neogastropods has affected the buccal musculature which primitively ran back through the nerve ring to join columellar or pedal muscles. This is no longer possible and, like the oesophagus (Graham, 1941), the posterior parts of these muscles have been pulled through the nerve ring and now connect with the wall of the proboscis. That they once penetrated the nerve ring, however, is suggested in development. Abro (1969) and Fretter (1972) described the course of velar retractor muscles in larvae of the mesogastropod Lacuna and the neogastropod Nassarius. The latter author in particular showed how, in Lacuna, some branches of the ventral bundles of velar retractors attach to the mouth of the radular sac at the stage where it is developing posterior to the nerve ring, while others continue through the nerve ring to the lips, where they insert, mainly ventrally, but some laterally and dorsally. At metamorphosis migration of the radular sac through the nerve ring brings the first group of fibres to the tip of the odontophore. They appear to persist in the adult as the median protractors of the subradular membrane, muscles of outstandingly regular occurrence and course throughout the prosobranchs. Fretter reported that the other fibres of the ventral velar retractors lose their posterior connexions at metamorphosis but that their anterior ends appear to contribute to the buccal musculature: if this is so their position and course suggest that they are the precursors of the adult odontophoral protractors. A similar distribution of fibres of ventral velar muscles may be inferred from the description of the larva of Nassarius, at a time prior to the differentiation of the proboscis, when the buccal region is still close to the nerve ring. With subsequent separation of these two areas those fibres which produced median protractors in mesogastropods become confined to the neogastropod buccal mass and are given a new role to play. Fretter (1972: 174) suggested that the figures of the veliger of HaEiotis given by Crofts (1937) showed muscle fibres in a situation similar to those of Lacuna, though they are not mentioned in her text. The regular occurrence in diotocardians of membrane protractor muscles would make this extremely likely.

The other muscles of the buccal mass do not appear to be derived from larval origins, but to be later local developments.

When this work was started it was hoped that a careful correlation of buccal and radular structure would show changes in musculature corresponding to changes in dentition. This hope has been only partly fulfilled, mainly in the obvious differences between rhipidoglossans and all other kinds of prosobranchs. What has emerged instead as the dominating factor i n the evolution of the buccal mass is the proboscis. This has altered buccal anatomy more fundamentally than any change in radular pattern. Though it has been relatively without effect in mesogastropods, perhaps because in these animals it is acrembolic, the pleurembolic proboscis of the neogastropod has changed the organization of a t least three of the superorders (Muricacea, Volutacea, Buccinacea) so markedly as to show them, not only as a more unified taxon than study of some other systems suggests, but also as one standing at an altogether higher evolutionary level than the other prosobranchs.

346 A . G R A H A M

Summary An account is given of the muscles of the buccal mass of the chiton Lepidochitona

cinereus (L.) and of the prosobranchs Diodora apertura (Montagu), Crepidula .fornicata (L.) and Olivella biplicata (Sowerby), together with new observations on Haliotis tuber- ciilata L., Viviparus viviparus (L.) and Littorina littorea (L.).

The muscles responsible for each phase of the act of feeding in these animals are investigated and compared with those previously described. In this way it has been possible to show a common structural plan in the prosobranch buccal mass. It contains: buccal circular muscles (including an oral sphincter), buccal dilator muscles, protractors and retractors of the odontophore, protractors and retractors of the subradular membrane, radular tensors (co-ordinating movements of the radular sac and the subradular membrane) and a ventral approximator which links the supporting cartilages of the odontophore and affects the spreading of the radula.

In addition to these basic muscles there are ancillary ones which act as tensors. These are particularly numerous in chitons, monoplacophorans and in prosobranchs with a rhipidoglossan radula, but are greatly reduced or lost in taenioglossans and neogastropods. The need for these muscles in chitons and monoplacophorans is due to the lack of a mobile head with a muscular wall and to the presence of a dorsal shell. In prosobranchs the muscular wall of the head is an integral part of the feeding apparatus and the animals can dispense with many of these muscles except in rhipidoglossans where they are needed to control the fine movements of an odontophore used to brush food off an irregular substratum. When the radula changes to a rasping organ the muscles are useless and disappear.

The neogastropods have a buccal organization which differs markedly from that of mesogastropods even although the same basic plan is recognizable. This is linked with their acquisition of an elongated and narrow pleurembolic proboscis in which the mouth is terminal. The narrowness of the proboscis has made the buccal cartilages so thin that they have become flexible and this has necessitated the removal of the retractor muscles of the subradular membrane from their original position within the odontophore to a new situation behind it. This, in turn, has caused an alteration of function in some muscles as the odontophore undergoes consequential reorganization. The elongation of the proboscis, separating buccal mass from foot and nerve ring, has pulled the origin of many muscles forward from a primitive attachment to columellar and pedal muscles, and they now originate on the walls of the proboscis.

The median protractor muscles of the subradular membrane are shown to be branches of the ventral velar retractors of the veliger larva. The rest of this muscle is probably represented by the odontophoral protractors of the adult.

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348

aa a1 b

bc bcm bd bg blP

bm br bs bw C

cc cg cm col cpd CPl df dl do3

drr gs J Im Ima lor

dpo

b d IPl Ipm

IPO m mor

mpa

A . G R A H A M

Abbreviations used in figures

anterior aorta anterior levator of odontophore boundary between buccal cavity and radular

buccal cavity buccal circular muscle buccal dilator muscle buccal ganglion and commissure buccal part of lateral odontophoral protractor

buccal membrane roof of buccal cavity buccal sphincter muscle body wall cartilage cerebral commissure cerebral ganglion circular muscle of body wall columellar muscle cerebropedal connective cerebropleural connective dorsal fold on buccal roof dorsal lip oblique muscle of shell plate 111 dorsal odontophoral protractor muscle dorsal radular retractor muscle ganglion on sublingual pouch jaw longitudinal muscle of body wall longitudinal muscle of aortic wall lateral branch of odontophoral retractor

left pedal ganglion left pleural ganglion lateral protractor muscle of subradular

lateral odontophoral protractor muscle mouth median branch of odontophoral retractor

median proboscis artery

diverticulum

muscle

muscle

membrane

muscle

mpm

mrr nr

od oe om opm

or P Pa

oc

pd pj PI P k

prr Pr

PV r rd rj rr rs rsm rt rtf sbc sd sg sh SIP sm

srm tf

SOC

median protractor muscle of subradular

median radular retractor muscle nerve ring odontophoral constrictor muscle odontophoral depressor muscle oesophagus origin of blp, Ipm outer protractor muscle of subradular mem-

brane odontophoral retractor muscle proboscis pedal artery posterior depressor muscle of odontophore protractor muscle of jaw posterior levator muscle of odontophore pleural ganglion proboscis retractor muscle posterior radular retractor muscle opening of pedal venous sinus radula radular diverticulum retractor muscle of jaw radular retractor muscle radular sac in radular artery retractor muscle of subradular membrane radular tensor muscle retractor muscle of transverse fold suboesophageal connective salivary duct salivary gland sheath of proboscis sublingual pouch shell muscle supra-oesophageal connective subradular membrane transverse fold

membrane

tm1,2 transverse muscle of shell plate I,II va ventral approximator muscle vl ventral lip vlm ventral longitudinal muscle vpo ventral protractor muscle of odontophore

the anatomical basis of function in the buccal mass of prosobranch and amphineuran molluscs

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