OBSERVATIONS ON THE ANATOMY OF MIKlfDOTROCIIUS AMABILIS BAYER'

VERA FRETfER University of Reading, England

ABSTRACT The gross anatomy of the hoJotype specimen of Mikadotrochus amabilis Bayer, 1963, is described insofar as the state of preservation permits. A brief description of the external features is given to point out differences between this and those previously described, especially Mikado- trochus beyrichi (Hilgendorf).

INTRODUCTION The most comprehensive description of the anatomy of a member of the gastropod family is given by Woodward (1901) for Mikadotrochus beyrichi (Hilgendorf). With three preserved speci- mens he was able to examine the most important systems of the body and compare this species with what was already known of the anatomy of Entemnotrochus adansoni{Jnl!s (Crosse & Fischer) and quoyanus (Fisher & Bernardi); owing to poor preservation of the speci- mens our knowledge of these two species is confined to external features, radula, some details in connection with the pallial complex and for P. quoyanus the nervous system (Dall, 1889: Bouvier & Fischer, 1899). The single specimen of a new species, Mikadotrochlls amabilis Bayer, 1963 (described below), was trawled southeast of Sombrero Key, Florida. It was fixed in alcohol and retracted into the shell. When removed it was found that the stomach was damaged so that nothing but its contents could be justifiably examined, and the posterior part of the right kidney was torn. The rest of the was moderately well preserved for work on gross anatomy. A brief description of the external features will be given to emphasize certain differences between this and other species which have already been described, especially M. beyrichi (Woodward, 1901); the value of some of these remarks will be known only when more specimens of pleurotomarians become available so that the living animal can be studied and the extent of variation within a species revealed.

IContribution No. 524 from The Marine Laboratory, Institute of Marine Science, University of Miami. The material described herein was collected during deep water operations of R/V GERDA supported by grant G-20355 from the National Science Foundation. 1964] Fretter: Anatomy of Mikadotrochus 173

EXPLANATION OF LETTERING a, anal papilla j, jaw aa, anterior aorta la, left auricle ahv, afferent brachial vein lav, left afferent branchial vessel ah, accessory lobe of hypobranchial lh, left hypobranchial gland gland lk, left kidney h, bolus of food held by dorsal n, supraoesophageal nerve in blood folds of oesophagus sinus ha, bulbus aortae ad, odontophore bbs, basibranchial sinus of, dorsal fold of oesophagus bf, dorsal folds of buccal cavity og, oesophageal gland bw, body wall opened mid-dorsally as, osphradium overlying branchial c, columellar muscle ganglion ca, ctenidial axis ov, oesophageal valve ee, cerebral commissure p, papillae cm, cut edge of mantle skirt showing pc, pericardium blood spaces pa, posterior aorta cpv, cephalopedal vein pg, opening of anterior pedal gland ct, ctenidium r, rectum d, morphologically mid-dorsal wall ra, right auricle of oesophagus rav, right afferent branchial vessel e, eye rk, right kidney ebv, efferent branchial vein rkp, urogenital papilla of right kidney ep, left epipodium rs, rectal sinus ev, efferent branchial vessel sn, snout f, foot sg, salivary gland h, heart sm, strands of muscle and he, head connective tissue hv, hypobranchial vein (Fig. 2) or t, tentacle vessels (Fig. 4) ve, ventricle if. inner vh, visceral hump

DESCRIPTION The relatively large head, resting on the propodium, has a truncated snout (Fig. 1, sn). The outer lip which surrounds the oral area is in- terrupted mid ventrally and its inner surface is densely papillated. It encloses a deep membranous frill, the inner lip (it), which also bears papillae and is brown. This inner lip enveloped a mass of detrital material, which the mollusc selects as food, and this suggests that it may be used to hold particles which will be gathered into the buccal cavity later by the radula. It is reminiscent of the frill associated with the outer lip of some members of the Acmaeidae and Lepetidae (Fretter & Graham, 1962) which has been shown by Thiem (1917) to be sensory. Although the lip is not mentioned by Woodward (1901) in M. beyrichi, he refers to, and figures, a number of "small flattened papillae" immediately in front of the jaws, suggesting a structure similar to, though much smaller than, the inner lip of M. amabilis. There is no reference to anything comparable in the descriptions of E. adansonianus and P. quoyanus. 174 Bulletin of Marine Science of the Gulf and Caribbean [14(1) The cylindrical tentacles, lying low on the head, are contracted. They do not branch at the tip as in M. beyrichi. The eye, on an eyestalk at the base of each, is partly hidden by the lateral lobe of the mantle skirt. The mantle skirt or pallial fold encircles the body. It is very shallow posteriorly and except in this region is fringed with rows of papillae (p). These increase in length and number in the region of the pallial slit. The

17 mm

FIGURE 1. Mikadotrochus amabilis. Animal removed from shell and seen from the left side. The damaged visceral mass is not shown. (For explanation of lettering of all figures, see list on page 174.) slit is conspicuous though its margins were retracted from the shell slit in the intact animal; on either side projects the tip of a ctenidium. The foot is large and pointed posteriorly. A transverse furrow across the broad anterior limit of the sole is overhung by the thin edge of the propodium. This has been mentioned in all species and presumably in all, as in P. amabilis, the furrow marks the opening of an anterior pedal gland (pg), though the gland was not known to previous authors. The surface of the anterior part of the sole, or mesopodium, is relatively smooth and has a deep, median longitudinal groove, whilst that of the more posterior parts is contracted to give transverse furrows. The lateral 1964] Fretter: Anatomy of Mikadotrochus 175 surfaces of the foot are minutely papillose and reddish in color, re- sembling the shell. The papillae extend over the epipodial folds. These are rather shallow anteriorly but deepen posteriorly so that they arch over the surface of the metapodium. The edges of the folds are fringed with papillae. There are no epipodial tentacles or sense organs. The right epipodium is better developed than the left and extends forward to near the level of the anterior limit of the foot. The left (ep), arising about half way along the side of the foot, resembles the condition de- scribed by Dall (1889) for P. quoyanus. In E. adansonianus it is even shorter, but appears to be as long as the right in M. beyrichi. The opercular lobe of the meta podium is small and its posterior edge is some distance from the posterior tip of the foot. Spanning the distance between them and originating beneath the lobe is a deep median groove bordered on each side by a prominent tumid edge which, with the con- traction of the foot, is folded to give the appearance of fairly regular crenations. This edge is bounded laterally by a more or less straight, thickened ridge. When the edges of the groove are forced apart two or three shallow ridges are seen along its length, though undoubtedly the surface would be smooth in the relaxed state. A similarly modified metapodial area is present in E. adansonianus (Dall, 1889) and M. beyrichi (Woodward, 1901) but does not appear to be developed in P. quoyanus (Dall, 1889). The opercular groove is a slit on the right side of the foot and pro- duces a polygyrous operculum of spiral pattern. The oldest part of the operculum shows a large number of turns which gradually increase in breadth as in trochids. In the peripheral younger part, the turns are considerably broader, suggesting that at a certain age there was a rapid increase in the extent of the groove. This increase is greater than sug- gested by Woodward's figure of the operculum of M. beyrichi. As in this species the operculum is not big enough to close the opening to the shell through which the animal had retracted so that a fully retracted animal lies high up the body ; when extended it would presumably protect the metapodium against mechanical injury which might be caused by the shell rubbing against it. Anterior to the opercular lobe the metapodial surface is smooth. Here the posterior part of the double columellar muscle passes dorsally to a right and left attachment on the shell; the right muscle is the larger. A double columellar muscle may be present in other pleurotomarians though no mention has been made of it by previous authors. The pallial complex of M. beyrichi has been admirably described and that of M. amabilis appears to agree in general layout (Fig. 2). There are, however, further details to be added, especially in connection with the vascular system, and some different interpretations of the structures. 176 Bulletin of Marine Science of the Gulf and Caribbean [14(1) hv

sn r rkp lav

17 mm

FIGURE 2. M. amabilis. Dissection to display the contents of the mantle cavity. The ctenidial axes, especially the left one, are considerably contracted.

The mantle cavity is deep, narrowing posteriorly, and the gills do not extend into the posterior third. Each ctenidium, except for the free anterior tip, is attached to the mantle skirt by an afferent membrane, and through this runs the efferent branchial vessel (ev). The afferent vessel can be seen along the afferent edge of the ctenidial axis. There is no afferent membrane. Posterior to the ctenidial leaflets each efferent vessel takes a direct course to the heart (h) and can be traced at the junction of mantle skirt and body wall. The course of the afferent vessels in this posterior region is different on the two sides (lav, rav). On the left the ctenidial axis (ca) extends back some distance behind the leaflets and carries the afferent vessel on a ridge to near the point where it emerges from the ventral wall of the left kidney. The left gill is considerably longer than the right in accordance with the dextral coiling of the shell which restricts the left side of the pallial complex. The shorter right afferent vessel projects from the mantle skirt to which it is attached. A special lobe of the hypobranchial gland overlies the posterior 1964] Fretter: Anatomy of Mikadotrochus 177 part of each of these vessels (ah), the left lobe being by far the larger. It is wrapped around the ridge on which runs the long prebranchial region of the vessel. The efferent edge of the free tip of the ctenidium is thickened by skeletal tissue. The osphradium lies at its confluence with the mantle skirt over the branchial ganglion (os), giving an arrangement which is characteristic of other zeugobranchs and trochids. The roof of the mantle skirt is thickened by the development of the hypobranchial glands, one being associated with each ctenidium (lh). They are separated anteriorly by the hypobranchial vein (hv), which arises from the rectal sinus, and posteriorly by this sinus and the rectum. Branches from the vein pass between the lamellae of the gland and ultimately join the efferent branchial vessel; in such other diotocardians as have an afferent membrane, they join the afferent vessel.

2 mm ve

FIGURE 3. M. amabilis. Heart. The dorsal wall of the pericardium has been removed.

The pericardial cavity which lies across the basal part of the visceral mass encloses the ventricle (Fig. 3, ve) (through the center of which runs the rectum), left and right auricles (la, ra), and the bulbus aortae (ba), arising from the left end of the ventricle. Each auricle receives blood from an efferent branchial vessel (ebv). The left auricle opens into the anterior wall of the ventricle; the right into the posterior wall. The anterior and posterior aortae (aa, paY arise from the bulbus. The former becomes attached to the body wall and passes forwards beneath the left efferent branchial vein. Not far from the branchial ganglion, and anterior to the forwardly directed loop of the intestine, it leads dorsally, runs beneath the dorsal body wall to the right side (Fig. 5, aa) and then 178 Bulletin of Marine Science of the Gulf and Caribbean [14(1) passes ventrad to enter the cephalopedal sinus beneath the buccal mass. This sinus divides into cephalic and pedal arteries. From the former is given off the radular artery which forms a sinus around the radular sac. The posterior aorta makes its way up the visceral coils and branches to the stomach, digestive gland and gonad; owing to damage in this part of the specimen details of the branching could not be traced accurately.

ct ct

ebv

!.. lk) ...... ;;..~.::._-~ .

FIGURE4. M. amabilis. Diagram of the vascular system. The dashed line marks the afferent renal vein, which was not traced in detail. The efferent renal veins are not labeled.

The venous sinuses which collect blood from the cephalopedal haem 0- coel (Fig. 4, cpv) drain into a large vessel at the posterior end of the mantle cavity. This is the basibranchial sinus (bbs). It is from here that blood passes to the afferent branchial veins (abv) and to the mantle skirt by way of the rectal sinus (rs) and hypobranchial vein (hv). The right and left arms of the basibranchial sinus also drain the kidney of the corresponding side. The smaller left kidney is embedded in the thickness of the mantle skirt and as the sinus passes forward along its ventral wall blood from the renal tissue enters it. The right arm of the sinus receives blood from the right kidney and then passes forwards along the dorsal wall of the urinogenital papilla which connects this kidney with the mantle cavity. The passage of blood into this part of the vessel, which 1964] Fretter: Anatomy of Mikadotrochus 179 may be suddenly constricted when the animal retracts into its shell, is regulated by a valve, in the form of a fine muscular papilla, which is immediately anterior to the entry of the renal vein. A basibranchial sinus with a similar efferent system is present in Baliotis; it is homologous with the transverse pallial vein of trochids. In Batiotis, however, the sinus does not drain the cephalopedal haemocoel which opens into the right kidney, though the transverse pallial vein does so in trochids. The left kidney receives its blood supply from the left efferent branchial vein which branches not far from the auricular opening. The blood supply to the right kidney drains from the visceral haemocoel; an undamaged specimen would be needed to verify the details of this. This kidney spreads posteriorly into the visceral mass and anteriorly beneath the dorsal body wall where, as in some trochids, it lies around the forwardly directed loop of the intestine, first covering it dorsally, and then, more anteriorly, spreading ventrally beneath it. The ventral part receives an artery from the anterior aorta. The large urinogenital papilla bearing the opening of the right kidney (Fig. 2 rkp) is relatively thin walled and muscular. The opening is over- hung by a valvular flap. In M. beyrichi the walls of the papilla are thick and glandular in the female, but unmodified in the male, and no valve covering the opening has been described (Woodward, 1901). Sections of the gonad of M. amabilis show the specimen to be an immature female. Glands may develop in the walls of the papilla only as the gonad becomes mature and this specimen may be a young individual which has never spawned. The buccal region of the alimentary canal is surprisingly short and there are no buccal pouches (Fig. 5). Two jaws (j), side by side, cover its anterior wall, their edges projecting ventrally to prevent the escape of food drawn in by the radula. A pair of longitudinally directed folds project from the roof (bi) and form the side walls of a broad dorsal food channel; they deepen considerably at the entrance to the oesophagus. The acinous salivary glands (sg) spread over the roof, one on either side, and extend back to the region of torsion. Their ducts are short and do not pass through the nerve ring (cc). They open to the buccal cavity lateral to the dorsal folds and toward their anterior ends. The odontophore is not a very massive structure but the broad radular sac which lies immediately above the columellar muscle extends straight back to the posterior end of the body whorl. The radulae of Perotrochus quoyanus (Bouvier & Fischer, 1899) and Mikadotrochus beyrichi (Woodward, 1901) have been described in considerable detail and the same type of teeth are exhibited in both species, though the number in a row varies. The number is alwavs high, makin~ the slight variations from species to species appear insignificant. On either 180 Bulletin of Marine Science of the Gulf and Caribbean [14(1) aa

d

sg b

of og

ov

3.4 mm sn

FIGURE 5. M. amabilis. Dissection to show buccal cavity and oesophagus cut open mid-dorsally and along the line of torsion. 1964] Fretter: Anatomy of Mikadotrochus 181 sidc of thc single rachidian tooth are five different groups sharply differen- tiated from one another and referred to as the central, lamellate, hooked, brush and f1abelIiform teeth. These are present in the radula of M. amabilis with the brush teeth, which are characteristic of the family, forming the largest group; the brushes show considerable wear at the functional end of the radula and are often broken. In M. amabilis the number of teeth in a single row is: 8 + 63 + 21 + 24 + 3 + R + 3 + 24 + 21 + 63 + 8. This is greater than in P. quoyanus in which the formula for each half row is R + 3 + 24 + 13 + 63 + 6, and also than in M. beyrichi which has R + 3 + 20 + 17 + 63 + 7. In Entemnotrochus adansonianus the number in a half row is considerably less (R + 69) and the teeth do not conform to the types displayed by the other species (Dall, 1889). The first of the group of hooked tecth in M. beyrichi differs from the rest in its smaller size and the absence of a strong hook; each edge is incurved, a feature displayed by the rest. In M. amabilis this tooth is similar but the transitional teeth between it and those with the characterisic hook differ from the corresponding ones in M. beyrichi. The differences are displayed in Figure 6, and show a cusp on either side of the hook in the first of these teeth; in subsequent ones the cusps weaken and are lost. In M. beyrichi only the lower cusp is developed.

FIGURE 6. M. amabilis. Hooked teeth of radula: 2nd, 3rd, 4th, and 5th from left to right.

The oesophageal region of the gut is marked anteriorly by the oeso- phagea] valve and posteriorly by a sphincter at the entrance to the stomach. It is divisible into anterior, mid and posterior sections. Whereas in other zeugobranchs and in trochids glandular pouches are formed 182 Bulletin of Marine Science of the Gulf and Caribbean [14(1) by the expanded lateral walls of the mid oesophagus, the section af- fected by torsion, and the lateral walls of the anterior oesophagus form separate pouches and may accommodate food during feeding, in M. ama- bilis and M. beyrichi (Woodward, 1901, Fig. 9), the oesophageal glands extend anteriorly to the buccal cavity (Fig. 5, og). Their secreting surface is similar to that of these diotocardians in that it is increased by the development of finger-like outgrowths. Moreover, as in trochids, the anterior and most of the mid oesophagus is linked to the body wall by strands of muscle and connective tissue (Fig. 5, sm). The food channel along the oesophagus is formed by the dorsal and ventral walls. Anteriorly a deep channel is formed between the muscular folds which hang from the dorsal wall (of), and boluses of food were found to be retained there (b). The ventral wall is also bounded on either side by a fold, insignificant at first, but becoming more prominent along the mid oesophagus where the four folds regulate the passage of food and allow access of secretion from the oesophageal glands. Other dioto- cardians retain traces of right and left ventral folds in the anterior oesophagus and in the mid oesophagus they merge and ultimately unite. The third section of the oesophagus posterior to the glands is short: its walls are folded longitudinally. It was impossible to make any investigation of the stomach which was shattered except for a fragment of spiral caecum. The contents showed the animal to be a micropragous scavenger and consisted of a large number of sponge spicules, foraminiferans, diatoms and algal fragments. The course of the intestine is similar to that of a trochid with an anterior loop which spreads forward over the oesophagus. In trochids it is limitei anteriorly by the transverse septum (Fretter & Graham, 1962), but in the absence of this septum in the pleurotomarian the intestinal loop reaches halfway along the mid oesophagus. The intestine then passes through the ventricle from left to right and on reaching the mantle skirt passes dorsally to a median position; in trochids it continues along the right wall of the skirt. The nervous system agrees with the description given by Woodward (1901) for M. beyrichi. SUMMARY The foregoing description of the anatomy of Mikadotrochus amabilis shows certain structural differences distinguishing it from M. beyrichi: the cephalic tentacles are not branched; the left epipodium is shorter than the right; the inner lip is a long papillated frill; the pattern of radular structure is R + 3 + 24 + 21 + 63 + 8 as compared with R + 3 + 20 + 17 + 63 + 7 in M. beyrichi, and there are differences in the form of some of the hooked teeth. Other distinguishing features in internal anatomy may be revealed when fresh specimens of both species become available. 1964] Fretter: Anatomy of Mikadotrochus 183 Throughout the description references have been made to the resem- blance with trochid organization. These include the gut, the kidneys, and the vascular system. Differences in the arrangement of organs and blood vessels associated with the mantle cavity may be attributed to the presence of two ctenidia in the pleurotomarian which do not extend into the posterior third of the cavity and have no afferent membrane. The majority of zeugobranchs and members of the Patellacea have taken to a rock-clinging mode of life, assuming a limpet-like form with concurrent specializations in structure. This makes the resemblances between pleurotomarian and trochid all the more striking. They substantiate the idea that trochids are sufficiently unspecialized to be regarded as a basic stock for mesogastropod evolution.

SUMARIO OBSERVACIONES EN LA ANATOMfA DE Mikadotrochus amabilis BAYER Un estudio de la anatomla del unico ejemplar de Mikadotrochus amabilis que fue conservado en alcohol, muestra que esta especie difiere en ciertos detalles de M. beyrichi (Woodward, 1901). La gran cabeza tiene un solo par de tentaculos que no estan ramificaoos en los extremos como en M. beyrichi. La tromp a es truncada y el labia exterior que rodea la region oral esta interrumpido en su parte media ventral. Este labia envuelve una masa de alimento seleccionado por el molusco y es presumiblemente usado para aguantar partfculas que seran reunidas mas tarde en la cavidad bucal por medio de la radula. Una estructura tan bien desarrollada no es descrita en M. beyrichi, que no obstante, tiene un area con un numero de pequenas papilas aplastadas inmediatamente en frente de las mandibulas. EI pie es grande y puntiagudo posteriormente. La abertura de una glandula pedial anterior, que no ha sido previamente descrita en un pleuro- tomacio, aparece como un profundo surco en el borde anterior de la superficie ventral y al que sobresale el propodium. Los dobleces del epipodio son bajos anteriormente y mas profundos posteriormente para cubrir la superficie del metapodio. El epipodio derecho se extiende a 10 largo del pie, pero el izquierdo es mas corto, levantandose solo la mitad de su longitud. En M. beyrichi los dos dobleces parecen ser de iguallongitud, semejandose al doblez derecho de esta especie. La radula muestra los mismos tipos de dientes en ambas especies, pero la formula de la estructura radular es R + 3 + 24 + 21 + 63 + 8 compara do con R + 3 + 2'0 + 17 + 63 + 7 en M. beyrichi y hay diferencias en los primeros pocos dientes curvados. El segundo muestra una cuspide a cada lado del gancho que se debilita en los dientes subsi- guientes y se pierde; solamente la cllspide inferior esta desarrollada en M. beyrichi. 184 Bulletin of Marine Science of the Gulf and Caribbean [14(1) Ninguno de los dos ctenidios se extiende dentro de] tercio posterior de ]a cavidad del manto. Cada uno esta unido a] manto por una membrana eferente, pero no hay membrana aferente. E] vaso branquia] aferente puede ser seguido a 10 largo del borde aferente del eje ctenidia] y posterior a las hojas ctenidia]es esta protegido por un 16bulo especial de la glandula hipobranquia] asociada con e] ctenidio. Hay dos glandulas hipobranquiales separadas por ]a vena hipobranquial. Una gran papila urogenital se proyecta en la extremidad posterior de la cavidad de] manto. Es, relativamente, de paredes de]gadas y musculares y a la abertura sobresale una aleta valvular. En M. beyrichi las paredes de ]a papila son gruesas y g]andu]ares en la hembra y no modificadas en e] macho; no ha sido descrita ninguna valvu]a cubriendo la abertura. Sec- ciones de las g6nadas de M. amabilis muestran que e] animal oesuna hem bra no madura. Pueden desarrollarse glandu]as en la pared de la papila, s61amente cuando la g6nada se madura. E] intestino, los rifiones y e] sistema vascular recuerdan ]a organizaci6n de un tr6quido. Esto apoya la idea de que los tr6quidos son diotocardios no especia]izados, suficientemente no especializados para ser considerados como e] sup]emento bcisico para la evoluci6n de los mesogaster6podos. REFERENCES BAYER,F. M. 1963. A new pleurotomariid gastropod trawled in the Straits of Florida by R/V GERDA.Bull. Mar. Sci. Gulf & Carib., 13: 488-492.

DALL, W. H. 1889. Reports on the results of dredging ... in the Gulf of Mexico (1877- 78) and in the Caribbean Sea (1879-80), by the U.S. Coast Survey Steamer "Blake" ... 29. Report on the . Part 2. and Scaphopoda. Bull. Mus. compo Zool., Harvard, 18: 1-492. FRETTER, V. ANDA. GRAHAM 1962. British prosobranch molluscs. Ray Society, London, xvi + 755 pp., 317 figs. BOUVIER,E. L. ANDH. FISCHER 1899. Reports on the results of dredging ... in the Gulf of Mexico and the Caribbean Sea, and on the east coast of the United States, 1877-1880, by the U.S. Coast Survey Steamer "Blake", ... 38. Etude monographique des Pleurotomaires actuels. Bull. Mus. camp. Zool. Harvard, 32: 193-249. THIEM, H. 1917. Beitrage zur Anatomie und Phylogenie der Docoglossen. 2. Die Anatomie und Phylogenie der Monobranchen. lena. Z. Naturw., 54: 405-630. WOODWARD,M. F. 1901. The anatomy of bey'richU Hilg. Quart. l. micro Sci., 44: 215-268.