BIOLOGICAL INVESTIGATIONS OF THE DEEP SEA. 16. OBSERVATIONS ON THE ANATOMY OF PEROTROCHUSl

VERA FRETIER University of Reading, England

ABSTRACT The gross anatomy of two new species of pleurotomariid gastropods from the Western Atlantic, Perotrochus midas and P. lucaya, is described and the external features, the stomach, and the buccal cavity of P. midas, are figured. Reference is made to resemblances and differences between these species and those previously described, and with trochid organization.

INTRODUCTION Three new species of the pleurotomariid Perotrochus, collected from the Western Atlantic, have been described recently by Bayer (1965). He formulated these on shell characters; no soft parts were associated with one of the shells (P. gemma). He kindly submitted the of the other two to me for examination. Both were preserved in formalin and fully contracted. The larger specimen, P. midas (Fig. 1), measures 10 em across the body from the dorsal surface of the snout (sn) to the roof of the posterior part of the mantle cavity. The corresponding measurement of the smaller one, P. lucaya, is 2.6 em. P. midas is a mature female; P. lucaya is immature and its sex was not determinable. In both the visceral coils are intact permitting an examination of the stomach, which in most pleurotomariids previously described has been damaged and so neglected. Confirmation of the vascular supply to the right kidney, not traceable in Mikadotrochus amabilis (Fretter, 1964), was also possible. The external features, radula, and some structures of the pallial complex of another species of Perotrochus, P. quoyanus, were described by Dall (1889). Later, Bouvier & Fischer (1899) examined in greater detail the radula and the nervous system of this species.

DESCRIPTION In both new species of Perotrochus the head is large, the cylindrical snout bent downwards and the mouth, extending back midventrally from its tip, all but hidden from view. The tentacles, low on the sides of the head, are contracted. Each tapers distally to a blunt point and immediately posterior to its base is a small eye (Fig. l,e) on a slight protuberance. The eye is an open vesicle, apparently with no lens. The foot is relatively large with the sole broad anteriorly and tapering posteriorly. The slit-like

'This paper is the sixteenth in the series of scientific resulls of invcstigations in the deep sea and open ocean conducted by the Institute of Marine Science. For a list of the first fifteen papers in the series, please see p. 641. 604 Bulletin of Marine Science [16(3)

e

ev sn ray dg

2.5 em FIGURE 1. Perotrochus midas. removed from shell and seen from the right side. (For explanation of lettering of all figures see list in text.)

EXPLANATION OF LETTERING aI, left accessory lobe of hypobranchial gland bt, brush teeth of radula bw, body wall opened mid-dorsally cc, cerebral commissure ct, clenidium dg, digestive gland e, eye em, edge of mesopodium bordering sole ep, epipodium ev, efferent branchial vein gj, intestinal groove gs, gast.ric shield hp, horny papillae iI, inner lip J, jaw la, left auricle lh, left hypobranchial gland 1966] Fretter: Anatomy of Perotrochus 605 opening of a pedal gland separates the anterior edges of propodium and mesopodium. A median longitudinal groove along the dorsal surface of the metapodium links the posterior tip of the sole with the opercular lobe. The groove is deep in the contracted foot and bordered on either side by small transverse grooves originating from it. In the living animals this post- opercular region must be of considerable length. The opercular groove on the right side of the opercular lobe of the metapodium produces a poly- gyrous operculum (op) with 151h turns in P. midas and 71h in P. lucaya. Each operculum is small for the size of the snail, closing the shell well above the shell slit. Fine papillae cover the surface of the head and lips of P. midas, the bases of the tentacles, the lateral surfaces of the metapodium and the edges of the mesopodium bordering the sole (em); the lateral parts of the mesopodium, distended with blood, have an apparently smoother texture, but in some areas coarse papillae are visible. The papillation is less distinct in P. lucaya except on the snout and lips. The epipodial folds are shallow (ep) especially anteriorly. They are fringed with papillae, have no tentacles and no macroscopic sense organs. The mantIe skirt encircles the body. It is very shallow posteriorly and, except in this region, is bordered by papillae, most numerous in the mature specimen (p). The columellar muscle is large, suggesting a double origin, and has an extensive insertion on the right side of the columella. Our present knowledge indicates that these external features are common to all pleurotomariids so far described, except for some specific variation

Ik, left kidney in mantle skirt oa, oesophageal opening od, odontophore 01, outer lip op, operculum osc, opening 01 spiral caecum ov, ovary p, papillae r, rectum rav, right afferent branchial vesselgorged with blood rh, right hypobranchial gland rk, right kidney rl, right accessory lobe of hypobranchial gland rm, radular membrane sc, spiral caecum sn, snout sg, salivary gland ss, style sac t1, t2, typhlo~oles ud, glandular urinogenital duct v, oesophageal valve ve, ventricle wbc, buccal wall open mid-dorsally 606 Bulletin of Marine Science [16(3) such as the occurrence of bifirl or trifid tips of cephalic tentacles in Mikadotrochus beyrichi (Woodward, 1901) and the degree of papillation of the body surface. Other differences will undoubtedly become apparent when living material is available for study. The structure and arrangement of the organs associated with the mantle cavity and their vascular supply are similar to that described for M. amabilis (Fretter, 1964). In both new species the hypobranchial glands (Fig. 1, rh, lh), though not the accessory ones (aI, rl), are deep orange, indicating differences in histological detail between the two. In P. lucaya the pigment has spread to the ctenidial leaflets. This species, unlike M. amabilis, M. beyrichi (Woodward, 1901), and P. midas, has no right accessory hypobranchial gland. In the other species the right is distinctly smaller than the left in accordance with the reduction of the right half of the pallial complex. The absence of the lobe may indicate a specific difference or be associated with the small size and immaturity of the specimen; it is less likely to be a sexual difference as both are present in M. beyrichi in which both sexes are described. Right and left kidneys open to the post-branchial part of the mantle cavity. The left one Ok), the papillary sac, is anterior to the pericardium and, as in trochids and turbonids, spreads through the thickness of the mantle skirt; it is asso- ciated with the left efferent branchial vein and the basibranchial sinus. The right kidney (rk) spreads into the visceral mass posterior to the pericardium and anteriorly it extends around the forwardly directed loop of the intestine beneath the dorsal body wall; its blood supply comes from the visceral haemocoel and drains to the basibranchial sinus. In details of location and vascularization the two kidneys agree with those of tro- chaceans, and also in the fact that the urinogenital papilla of the mature female is enlarged to form a glandular duct. The duct in P. midas (ud) is 3.5 em long and 1.3 em broad, and appears better developed than in M. beyrichi (Woodward, 1901). In the immature specimen of M. amahilis (Fretter, 1964) a duct is present but its walls are thin and muscular; in P. lucaya there is no duct suggesting that the specimen may be a male. Woodward (1901) concludes that the possession of this secondary sexual character is an important link between pleurotomariids and trochids. In some trochaceans the duct projects freely into the mantle cavity (Mar- garites); in others (Calliostoma) and in pleurotomariids it is associated with the mantle skirt. Entrance to the buccal cavity of P. midas is blocked by the dorso-Iateral jaws (Fig. 2,j) which are deep folds of the buccal wall covered by cuticle. Their edges are chisel-shaped and show signs of wear. A study of the functioning of the odontophore of two rhipidoglossate prosobranchs, Monodonta lineata (Nisbet, 1953) and Nerita fulgurans (Fretter, 1965) show that the jaws or their equivalent (buccal fold of Nerita) span the 1966] Fretter: Anatomy of Perotrochus 607

rm

cc

01 1 em FIGURE 2. Perotrochus midas. Buccal cavity exposed by a mid-dorsal incision. breadth of the buccal cavity. They depress the anterior end of the odontophore as it is protruded, spreading the radular ribbon, and adjust the horns of the anterior cartilages to the feeding position. It is probable that in the pleurotomariid gastropod their function is similar. Dall (1889) describes the jaws of as two small and weak quadrate pieces about 1.5 mm square. His specimens were about half the size of P. midas, in which the corresponding measurements are 6.0 X 7.0 mm, and considerably larger than P. lucaya in which each jaw measures 1.5 X 1.8 mm; 10 both species the jaws are broader than they are deep. Woodward (1901) also holds that the jaws of pleurotomariids are feebly developed and agrees with Dall's suggestion that their function is to protect the soft walls of the buccal cavity against the radular teeth and, presumably, the abrasive particles of food. 608 Bulletin of Marine Science [16(3) The radula in the two new species conforms to that of Perotrochus quoyanus (Bouvier & Fischer, 1899) and Mikadotrochus beyrichi (Wood- ward, 1901) in having five distinct groups of teeth on either side of the single rachidian. These are referred to as central, lamellate, hooked, brush, and flabelliform. The formula for P. quoyanus is R + 3 + 24 + 13 + 63 + 6 and that of P. midas and P. lucaya agrees closely being R + 3 + 26 + 13 + 63 + 6 and R + 3 + 25 + 13 + 61 + 6 respectively. I had considerable difficulty in counting the teeth of the smaller specimen as the functional part of the radular ribbon was retracted into the deep groove between the anterior cartilages of the odontophore. Moreover, hooked, brush, and flabelliform teeth were erected and left and right rows folded against one another. The brush teeth (Fig. 2,bt) make up the greater part of the length of the arms of the V-shaped rows and are bordered medially by strong hooks, foreshadowing the tendency within the Rhipidoglossa for the teeth next to the brushing marginals to become enlarged and specialized. The flabelliform, brush, and most hooked teeth show little wear even in the most anterior rows from which rachidian, central, and lamellate teeth are lost; their retention increases the sweeping efficiency of the radula. The median part of the radular membrane asso- ciated with the lost teeth (rm) curves round into the shallow subradular pocket and although shrivelled still shows indications of the sites of tooth rows. Posterior to this, in both P. lucaya and P. midas, is a roughened cuticular area reminiscent of the "licker" of limpets and topsheUs. The whole appearance suggests that the subradular membrane is gradually moving forwards from the posterior to the anterior end of the buccal mass. The feeding area covered by the radula will be enveloped by the outer lip (Fig. 2,01) spreading over the odontophore as it advances. The inner surface of the lip is densely papillated. It encloses a membraneous inner lip with papillae over inner and outer surfaces (il). The single specimen of Mikadotrochus amabilis previously described (Fretter, 1964) showed the last mouthful of food, gathered together on the backstroke of the radula, scooped up by the inner lip, suggesting that it enhances the gath- ering action of the odontophore. The fragility of the lip (it is partly disintegrated in P. midas) may account for it being overlooked by other workers. It is, however, indicated in Woodward's (1901) figure of M. beyrichi (his Fig. 9), though he labels only the dorsal "horny papillae" associated with its base and immediately anterior to the jaws. Large papillae are present in this position in both new species under consider- ation. In P. midas they are irregular in size and shape (hp); in P. lucaya they appear as the pointed teeth of a rake projecting from between the jaws, and would be effective in helping the radula and inner lip gather up the food. The brown cuticular covering of these teeth of P. lucaya sloughed off with the thick cuticle covering the jaws as one continuous sheet. In 1966] Fretter: Anatomy of Perotrochus 609

0.6 em

FIGURE 3. Perotrochus midas. Stomach opened from above. the description of M. amabilis (Fretter, 1964), tooth-like papillae in this position were overlooked. Re-examination of the dissected specimen reveals them. The presence of similar papillae in Diodora apertura (Fretter & Graham, 1962) suggests a close link with the functioning of the rhipidoglossan radula. The oesophageal region of the gut of P. midas and P. lucaya agrees with that of Mikadotrochus amabilis (Fretter, 1964). It is tied to the dorsal body wall by muscle strands, and at its entrance is a large oesophageal valve (Fig. 2,v) preventing regurgitation of the food at the forward stroke of the odontophore. At the oesophageal opening to the stomach is a long sphincter. Paired glands in the oesophageal region of the gut extend forward from the mid oesophagus to the posterior limit of the buccal cavity, their secreting surfaces being papillated. The stomach of P. midas is shown in Figure 3. It closely resembles that of Mikadotrochus beyrichi (Woodward, 1901), being bent sharply into a U-shape, the right half receiving the oesophagus, the left giving origin 610 Bulletin of Marine Science [16(3) to the intestine. The oesophageal aperture (oa) is surrounded by raised lips continuous with oesophageal folds and in its neighborhood is a small gastric shield (gs). The duct of the digestive gland opens to a groove lying between two folds which form the boundary between the two limbs of the U. The groove (gd leads in one direction to the opening (osc) of an elaborately helically coiled spiral caecum (sc) with four turns; in the other direction it leads to the style sac (ss) along the wall of which it runs for a short distance. The ridges which bound this groove must, by comparison with other prosobranchs, be the two typhlosoles (tl, t2). These details are also seen in the stomach of P. lucaya. The stomach in its general features is reminiscent of that of trochaceans. It is perhaps more like that of Monodonta or Calliostoma (Graham, 1949) than that of Cittarium (Graham, 1965) despite the greater similarity in size. It is more capacious than the stomach of any of these animals, more globular, less well provided with cuticularized surfaces, and lacks some of the features which are generally well marked in prosobranch stomachs. Thus, the intestinal groove (gd seems to end before reaching the intestinal end of the style sac and there is no trace of the sorting area commonly found alongside the gastric section of the intestinal groove. In the former of these points the animal differs from M. beyrichi; in the latter it resembles it. The gonad of P. midas (Fig. 1,0v) spreads over the digestive gland in the visceral coils, and deep septa covered by germinal epithelium subdivide the lumen. Many ova are free in the lumen, each embedded in a gelatinous sheath as thick as the diameter of the ovum. Sections of the ovary show that this covering is secreted by the ovum, as in other diotocardians (Fretter & Graham, 1962). A gonadal duct leaves the ovary and passes forward to a slit-like opening in the anterior thin-walled chamber of the right kidney which opens anteriorly to the glandular duct. This triple origin of the genital tract is in agreement with that of Calliostoma and is the general plan of the compound duct of higher gastropods. The spawn of pleurotomariids is unknown. It may be deduced that, as in Margarites and Calliostoma, a number of eggs, each in a gelatinous sheath, is embedded in secretion from the glandular section of the duct. The final form of the mass will depend on any manipulation it receives after leaving the urinogenital opening. The nervous systems agree essentially with that described by Woodward (1901) for M. beyrichi showing as a primitive feature a negligible degree of separation of ganglia from nerve trunks, with the exception of the branchials which are conspicuously large. The visceral loop is long, in accordance with the depth of the mantle cavity, giving off a number of nerves along its course. Bouvier & Fischer (1899) figure a large visceral ganglion for P. quoyanus, but this does not occur in these two new species 1966] Fretter: Anatomy of Perotrochus 611 of Perotrochus. The posterior part of the visceral loop passing through the basibranchial sinus gives nerves to the rectum, right and left kidneys, and remaining viscera. Other primitive features of the system are seen in the position of the cerebral ganglia low on the head, giving a long cerebral commissure, long pedal nerves with numerous transverse commissures, and the ventral position of the pleural ganglia. In all these features, with the exception of ganglia being ill defined, the nervous system agrees with that of Haliotis. However, pleurotomariids are more advanced and resemble trochaceans in having the labial ganglia fused with the cerebrals.

COMMENTS ON THE ARRANGEMENT OF ORGANS ASSOCIATED WITH THE MANTLE CAVITY The undamaged soft parts of Perotrochus midas and P. lucaya permitted an investigation of the visceral mass which was not possible for Mika- dotrochus amabilis, the most recently described pleurotomariid. This demonstrates further resemblances between pleurotomariid and trochacean organization than already listed (Fretter, 1964), namely in the stomach and female reproductive system. The anatomy is closest to that of the trochid Calliostoma zizyphinum. In fact it becomes increasingly obvious that the fundamental differences in the gross anatomy of these diotocardians are in the pallial complex. The mantle cavity of the pleurotomariid gastropod is proportionately longer than that of any other zeugobranch and is unique in being divisible into branchial and post-branchial regions of approximately equal length. The former, associated with the shell slit, contains paired gills, osphradia and hypobranchial glands, also the anus with exhalant streams of water converging on it from right and left. The latter contains the right and left kidney openings and accessory pallial glands; water movements in this part of the cavity must be comparatively slight. The right half of the pallial complex is reduced in length and breadth in accordance with the dextral coiling of the visceral mass. Trochids also have a long mantle cavity and a tightly wound spiral shell. In their soft parts they show trends towards monotocardian organization, especially in the loss of the right gill and osphradium. This results in the replacement of the primitively-double, lateral to median, water flow in the cavity by a single transverse current from left to right and obviates the necessity for a pallial slit. The ctenidium contrasts with that of the pleuro- tomariid in that it extends much closer to the posterior end of the mantle cavity, and the associated hypobranchial gland accompanies it. There are no accessory pallial glands. Blood flows to the ctenidium of the trochid by way of the transverse pallial vein which is homologous with the basi- branchial vein at the innermost end of the mantle cavity of pleurotomariids. The transverse pallial vein, however, has migrated into the roof of the 612 Bulletin of Marine Science [16(3) mantle cavity crossing it at more than a third its length from the innermost end in Calliostoma. On reaching the gill it divides into anterior and posterior branches which comprise the afferent pallial vein. The arrange- ment by which blood flows to this vein nearly halfway along its length increases the efficiency of the circulation in the ctenidium and compensates for its increased length. The migration of the vein may have become mechanically possible with the disappearance of the need to supply two ctenidia and in its new position is better placed for the collection of blood from the cephalopedal haemocoel. Support for the gill is met along the middle third of its length by the development of an afferent membrane which, together with the efferent membrane, ties the axis to the mantle skirt and leaves the anterior third free. In the posterior third the broad side of the axis fuses with the mantle and carries only a single row of leaflets; this approaches the condition of the gill in Monotocardia. Links between the afferent border of the ctenidial axis and the mantle skirt provide a pathway for such blood as has circulated through channels in the hypobranchial gland to reach the afferent branchial vein and increases the importance of the ctenidial circulation. In pleurotomariids there are no such links and the pallial blood flow bypasses the gills and enters the efferent branchial vessels along the length of their course. This condition is paralleled in the neritaceans (Fretter, 1965) and may be characteristic of a primitive ancestral form from which both pleurotomariids and neritaceans evolved. Nerita has exploited this arrangement of the pallial circulation so that it can withstand long periods of emersion when the single aspidobranch gill is contracted, its blood flow reduced, and the mantle cavity used as a lung. Blood flowing through the mantle skirt reaches the auricle by way of a special vessel peculiar to neritaceans, the parabranchial vein, which joins the efferent branchial vein near the heart. The glandular urinogenital duct in the female Calliostoma is anterior to the transverse pallial vein and the loss of the right gill allows it to spread forward in a position comparable to the pallial oviduct of monotocardians. In the pleurotomariid the duct bears the same relationship to the basi- branchial vein and is therefore accommodated in the posterior part of the mantle cavity posterior to the right gill. In both cases the duct may have originated from a closed-off portion of the mantle skirt, as may also be its origin in monotocardian gastropods, and contrasts with the pallial genital duct of neritids which develops within the anterior pallial vein as a forward growth from the visceral part of the genital duct.

SUMMARY The anatomy of two new species of Perotrochus is described from a single, preserved specimen of each: P. midas, a mature female, and P. lucaya, immature and the sex not determinable. Their external features 1966] Fretter: Anatomy of Perotrochus 613 agree with those described for P. quoyanus, including the pattern of radular structure. The jaws, however, are relatively larger and there is no well defined visceral ganglion. The arrangement of the organs and the blood vessels associated with the mantle cavity agree with those of Mikadotrochus, except that in P. lucaya there is no right accessory hypobranchial gland. Both new species have a large membraneous inner lip, with prominent dorsal papillae, which presumably help the radula in gathering food. The stomach, reminiscent of that of Monodonta or Calliostoma, has a helically coiled spiral caecum. It is similar to that of M. beyrichi, especially in the absence of a sorting area alongside the gastric section of the intestinal groove, but differs in that the intestinal groove appears to end before reaching the intestinal end of the style sac. The female reproductive system of P. midas agrees with that of Calliostoma; each ovum secretes a gelatinous sheath and there is a glandular pallial duct associated with the mantle skirt. The pallial duct of Perotrochus spreads through the post- branchial part of the mantle cavity, which is approximately equal in length to the branchial part. In Calliostoma it has migrated forward with the transverse pallial vein, and the loss of the right gill allows it to occupy a position comparable to the pallial oviduct of monotocardians.

SUMARIO OBSERVACIONES EN LA ANATOMIA DE Dos NUEVOS GASTEROPODOS PLEUROTOM ..\RIDOS DEL ATL.ANTICO OCCIDENTAL Se describe la anatomia de dos nuevos especies de Perotrochus bas{mdose en un solo ejemplar conservado de cada uno: P. midas, una hembra madura, y P. lucaya, no maduro y de sexo no determinable. Sus caracteres externos concuerdan con los descritos para P. quoyanus, incluyendo el patr6n de la estructura radular. Las mandibulas, sin embargo, son relativamente mayores y no hay ganglio visceral bien definido. La dispo- sici6n de los 6rganos y de los vasos sanguine os relacionados con la cavidad del manto concuerdan con los de Mikadotrochus, excepto que en P. lucaya no hay ghlndula hipobranquial accesoria derecha. Ambas especies tienen un gran labio interior membranoso, con papilas dorsales prominentes, que presumiblemente ayudan a la cadula a recoger el alimento. El est6mago, una reminiscencia del de Monodonta 0 Calliostoma, tiene un ciego espiral ellpticamente enrollado. Es similar al de M. beyrichi especialmente en la ausencia de un area de selecci6n a 10 largo de la secci6n gastrica del surco intestinal, pero difiere en que el surco intestinal parece terminar antes de alcanzar el extremo intestinal del saco del estilo. El sistema reproductor femenino de P. midas concuerda con el de Calliostoma: cada huevo secreta una cubierta gelatinosa y hay un conducto palial glandular asociado con el vuelo del manto. El conducto palial de Perotrochus se extiende por la parte post-branquial de la cavidad del manto, que es aproximadamente 614 Bulletin oj Marine Science [16(3) igual en longitud a la parte branquial. En Calliostoma ha migrado hacia adelante con la vena palial transversal y la perdida de la branquia derecha Ie permite ocupar una posicion comparable a la del oviducto palial de los monotocardios. REFERENCES BAYER,F. M. 1965. New pleurotomariid gastropods from the Western Atlantic, with a summary of the Recent species. Bull. Mar. Sci., 15 (4): 737-796. 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 mono- graphique des Pleurotomaires actuels. Bull. Mus. compo Zool., Harvard, 32: 193-249. DALL,W. H. 1889. Reports on the results of dredgings ... in the Gulf of Mexico (1877-78) and in the Caribbean Sea (1879-80) by the U. S. Coast Survey Steamer BLAKE ... 29. Reports on the . Part 2. and Scaphopoda. Bull. Mus. compo Zool., Harvard, 18: 1·492. FRETTER,V. 1964. Observations on the anatomy of Mikadotrochus amabilis Bayer. Bull. Mar. Sci. Gulf & Carib., 14 (1): 172-184. 1965. Functional studies of the anatomy of some neritid prosobranchs. J. Zool., 147: 46-74. FRETTER,V. ANDA. GRAHAM 1962. British prosobranch molluscs. Ray Society, London. xvi + 755 pp., 315 figs. GRAHAM,A. 1964. The molluscan stomach. Trans. roy. Soc. Edinb., 61: 737-778. 1965. Observations on the anatomy of some trochacean gastropods. Bull. Mar. Sci., 15 (1): 202-210. NISBET, R. H. 1953. The structure and function oE the buccal mass in some gastropod molluscs. 1. Monodonta lineata (da Costa). Ph.D. Thesis, Univer- sity of london. WOODWARD,M. F. 1901. The anatomy of Pleurotomaria beyrichi Hilg. Quart. J. micro Sci., 44: 215-26R.