ON CERITHIU1'\,f ATRA TUM (BORN, 1778) (: PROSOBRANCHIA)

EVELINE AND ERNST MARCUS Caixa Postal 6994, Siio Paulo, Brazil

ABSTRACT The shell, anatomy, and habits of the mesogastropod atratum (Born) are described from collected intertidally at the Research Station of the Oceanographic Institute, near Ubatuba, Brazil. The has been reported from Florida and the West Indies, southward to Argentina, but is not described in the recent literature. Its relationship with allied species, such as C. algicola C. B. Adams, C. ehurneum Brugiere, and C. striatissimum Sowerby, is discussed but not settled.

INTRODUCTION Cerithium atratum (Born, 1778) is said to occur among the Florida Keys and in the West Indies. Along the coast of South America from Brazil to Argentina, however, it is frequently recorded. Near Ubatuba, Brazil (230 57' S, 45° 06' W), it was found burrowing superficially in coarse sand in the tidal zone. As the species is not described in modern shell books, its relationship with allied species, such as Cerithium algicola C. B. Adams, C. eburneum Brugiere, and C. striatissimwn Sower by, re- mains in question. We are grateful to Professor Dr. Frederick M. Bayer for revising the language of our manuscript and for reading the proofs.

EXPLANATION OF LETTERING a-accessory pedal ganglia lb-thickening of labial nerve am-albumen gland m-mantle skirt an-anterior foot glands rna-major typhlosole ar-anus mc--capsule gland b--subintestinal ganglion me-mantle edge bu-cerebrobuccal connective mo-mouth c-cerebral ganglion n-nerve co-columellar nerve na-anterior border of foot cs-crystalline style o--oesophagealopening eu-cuticularized area oi-oviduct d-liver opening om-operculum e-testis duct oo-slit of pallial oviduct en-cephalic tentacle or-ovipositor ex-exhalant strip ov-pallial oviduct j-epipodial furrow p-pedal ganglion g-gastric shield pi-left pleural ganglion h--testis pr--right pleural ganglion i-intestine q--pallial male duct is-labial disc r-·-right mantIe nerves j-pallial tentacles ro-aperture of receptaculum seminis k--kidney rs-receptaculum seminis I-left mantle nerve s-blood sinus 1964] Marcus & Marcus: On Cerithium Atratum 495 sa-sorting area /lo-aperture of bursa sh-subintestinallimb of v-epipodial ridge visceral loop ve-ventral fold in stomach so-pallial sperm groove w-tip of tail sp-supra-intestinal limb of x--exhalant fold visceral loop y-communication of style sac and t-statocyst intestine Ii-bursa copulatrix

OCCURRENCE In February 1964 we found a species of Cerithium at the beach of the Research Station of the Oceanographic Institute, 14 km SW of Ubatuba (230 57' S, 450 06' W). The snails burrowed in rather coarse, slightly silty sand in the intertidal zone, between the levels of mean and spring low tide. The tracks of the ploughing snails, which consist of mucus fasten- ing the sand grains along their path, were seen on the bottom during mean tides and in calm weather. Most of the tracks were rather straight, and the animals could be taken at the end of the trail. Sometimes part of the shell was visible, and progress of the animals through the sand could be seen. Risbec (1943:89) described a sand-dwelling Cerithium, C. obelis- CllS, and its track, from New Caledonia. It is probable that the snails we collected at the Station had been re- leased there a few days before by Dr. Liliana Forneris, who, together with Dr. Edmundo Nonato, had dredged a great number of Cerithium on shelly bottom (4-12 m) in front of Anchieta Island (previously called Ilha dos Porcos), 12 km south of Ubatuba. Shells, opercula, and radulae of her dredged material, which she kindly showed us, cannot be distinguished fmm ours. The largest shells from Anchieta Island (38 mm) were bigger than ours (up to 28 mm). Our description of shell, operculum, and radula refers to our specimens and to those dredged at Anchieta Island, while the anatomy was studied only of the former material, which was observed alive. In the laboratory, in diffuse light, our snails were slow and shy. They came out gradually, but withdrew rapidly at the slightest movement of the dish, or when shadowed. Put on sand in normal position they buried under its surface immediately; without sand they moved for a certain time by jerks and then quieted down with the head-foot scarcely extended between aperture and operculum. Turned onto the back and held in this position by a loop of wire, the snails, observed for over an hour, did not come out completely, though inhalant and exhalant currents were seen with help of carbon powder. On sand the snail lying on its back rights itself by extending the foot over the inner or outer lip of the aperture, but does not always at its first attempt attain normal position. Hastula cinerea and the olivids (Olivella and Lintricula), which have a large foot, burrow incomparably much better than our Cerithium. When a 496 Bulletin of Marine Science of the Gulf and Caribbean [14(3) snail was removed from its track and placed on its back, half a minute or more passed until it began to right. The just mentioned neogastropods live in fine, dense sand which is usually not deeply stirred up by the waves. Cerithium atratum inhabits a more unstable, coarse sand in the tidal zone, but the place where we found the specimens is well sheltered, so that their passivity toward mechanical disturbance does not hinder their activity during calm weather. NOMENCLATURE We call these shells Cerithium atratum Born, 1778, upon the basis of Kobelt's detailed description (1898:192-193, PI. 35, Figs. 4,5), Reeve's account (1865, species 32), and specimens identified by various concholo- gists and kept in the Department of Zoology (Secretary of Agriculture) and the Oceanographic Institute, Sao Paulo. D'Orbigny's description (1841: 444) is inexplicit; our not having Tryon's Manual is to a certain degree compensated by Kobelt, who acquaints us with Tryon's concepts of specific limits and synonyms. C. atratum is common along the entire coast of Brazil (Souza Lopes and Alvarenga, 1957: 166) to Argentina (Kobelt). Moreover. it is recorded from the Florida Keys and the West Indies (Smith, 1890:492; Kobelt, 1898; Johnson, 1934: 109; Coomans, 1958: 70), but is not described in the modern shell-books dealing with this region. Since Reeve, the light C. caudatum Sowerby has been considered to be a synonym of C. atratum (see Smith). Brazilian localities of C. atratwn are: Fernando de Noronha; Pernambuco (Smith); Rio de Janeiro (d'Orbigny; Smith; Oliveira, 1950: 372; Buckup, 1957: 23); Sao Paulo, Island of Sao Sebastiao (v. Ihering, 1897: 170; Buckup); Parana (Lange de Morretes, 1949: 79; Gofferje, 1950: 234). We found it difficult to distinguish several other species from atratum. C. subatratum Kobelt (1898: 193, PI. 35, Fig. 6, 7), separated for geo- graphic reasons, agrees perfectly with our material. Also, the following figures of C. eburneum Bruguiere, 1792, correspond to various specimens among our material: Warmke and Abbott (1961, PI. 13, n), Reeve (1865: PI.6, Fig. 35 b, c), Reeve (1865: PI. 10, Fig. 63: algicola), and Reeve (1865: PI. 12, Fig. 8'0: versicolor). The latter is a synonym of eburneum (Abbott, 1955: 154). C. algicola C. B. Adams, 1848, is described as "longitudinal iter plicata," and hence is similar to our ribbed shells. According to Reeve, algicola has been referred to eburneum long ago, and also now Abbott (1955: 154; 1958: 40) says that algicola may be merely a form of eburneum. Also, other ribbed shells belong to eburneum (Warmke & Abbott, 1961: 73); they were described from Puerto Rico by Dall & Simpson (1901: 425), though under the name uncinatum Gmelin, which to-day is applied to a species from tropical west America (Keen, 1958: 303, n° 216). 1964] Marcus & Marcus: On Cerithium Atratum 497 Cerithium striatissimwn Sowerby (Reeve, 1865: PI. 5, Fig. 31) has been recorded from the coasts of Sta. Catarina (Kobelt) and Parana (Lange de Morretes; Gofferje). In the collection of the Oceanographic Institute there are shells identified as striatissimum from the coast of Sao Paulo, Island of Sao Sebastiao. They are very similar to the snails we call atratllm. According to Tryon (Kobelt, 1898: 120), striatissimum is ebllrnellm, and Kobelt himself (1898:] 93) thinks that striatissimum can hardly be separated from atratum. Pending the examination of more ma- terial, however, we feel justified in suggesting only the following tentative synonymy. Cerithillm atratum (Born, 1778) Mllrex atratus Born, 1778, p. 324, pI. II, figs. 17-18. Cerithillm caudatum Sowerby, 1855, p. 856, figs. 71-72. ? Cerithium striatissimum Sowerby, 1855, p. 856, figs. 86-87.-Reeve, 1865, pI. 5, fig. 31. Cerithium a/ratum. Reeve, 1865, sp. 32.-Kobelt, 1898, p. 192, pI. 35, figs. 4-5.-Johnson, 1934, p. 109.-Coomans, 1958, p. 70. ? Cerithium suhatratutn Kobelt, 1898, p. 193, pI. 35, figs. 6-7.

SHELL AND OPERCULUM Length up to 38 mm; average proportion of length to breadth 2.3: 1; young shells 2: 1; adults up to 2.64: 1. Apex acute, though often damaged. Whorls 12-15, of which three are smooth and belong to the larval shell. Axial ribs 9-20, more distinct in posterior than in anterior whorls. In young shells all post-larval whorls ribbed. Unequal spiral cords, often broadened over ribs, up to 20 in penultimate whorl. In anterior whorls ribs often obscured by regular superposed outgrowths in 2-3 spiral series; those of the middle (peripheral) series generally largest. Outgrowths may be very small knobs or high points (algicola-like specimens). Moreover, some of the spiral cords can be more or less beaded. Base of shell with 2-3 rows of numerous fine beads. Sutures covered by following whorls, hence indistinct. Sometimes only 2 but generally more (up to 12) varices, especially in the posterior whorls; frequently also a varix on the outer lip, which is convex, crenulate when a varix. is developed; aperture ovate. Anterior and posterior canals short, the former oblique, the latter set off from parietal wall by a fold on upper part of columella. This fold is thick when the varix on the outer lip is strong, absent when the varix is not developed. Protoconch brown, translucent; following 5-7 whorls often white, with- out dark marks; later whorls greyish, with cloudlike dark blotches and light specks; ribs generally dark, spiral cords white, varices light. Shell be- tween cords often brown or blackish. When the outer lip bears a varix, the interior of the aperture ("Gaumen," Kobelt) may be bluish. Among 498 Bulletin of Marine Science of the Gulf and Caribbean [14(3) 150 shells, a single creamy white specimen was seen, but no quite black ones. Periostracum colorless, rather strong. Operculum smaller than the aperture, hence deeply retractable. Nucleus situated near the anterior, columellar side, surrounded by a conspicuous ridge for muscle insertion. There are a number of slightly pigmented whorls within the conchiolin of the operculum, behind the nucleus. This description does not refer to all the C. atratum that we have seen in collections in Sao Paulo, but only to those of the area of Ubatuba, An- chieta Island, and the Research Base of the Oceanographic Institute.

HEAD, FOOT, AND MANTLE CAVITY Figs. 1,2 The rounded head has a broad and flat snout with subterminal labial discs (is); its dorsal skin is streaked with black. The tapering tentacles (en) are highly contractile and bear rather large eyes in a basal bulge. Head and foot are separated by a light ciliary furrow (f) extending back- ward to the operculigerous disc (om). Farther behind, there is an epipo- dial ridge (v) as in Bittium varium (Marcus, 1963: Fig. 80, em). On the right side a gutter (ex) comes from the mantle cavity and ends short behind the anterior corner of the foot. In the female it leads the eggs out and is described together with the reproductive organs. The foot is relatively small, hardly as long as the shell aperture, hence minute in comparison with one of the burrowing species described by Risbec (1943: Fig. 7). Its deep anterior furrow extends over the whole breadth; the glands (an) of the upper lip stain reddish, those of the lower lip blue with haematoxylin-eosin. These glands have separate openings; there is no common median duct. The whole lower lip bears cilia, but only the lower side of the upper lip is ciliated. The sale is provided with a great number of groups of subepithelial ~land cells secreting mucus. Ventral and lateral surfaces of the foot bear cilia. Also, the epipodial fur- rows (f) are ciliated, but the epipodial ridges are not. Numerous nerves (n) are seen in sections of the anterior border and also in other regions of the foot. In C. atratum, the edge of the mantle skirt bears a row of short tenta- cles (j) in front and on both sides as in C. vul.l?otum (Bouvier, 1887: 132) and C. dialeucum (Risbec, 1943: 91). They are about '0.35 mm long and simple, not pinnate as in Turritella communis (Fretter & Graham, 1962: Fig. 57, 108), which lives in mud. The inhalant current enters the mantle cavity of C. atratum through a short siphon, a vaulted fold of the mantle edge. The latter is provided with many secondary ganglia of the pallial nerve. The lateral walls of the siphon can be closely approximated forming a nearly closed tube. The inhalant current seems to be filtered ef- ficiently, since siphon, osphradium, and gill are free from coarse particles. ] 9641 Marcus & Marcus: On Cerithium Atratum 499 1 m

w

2

om s n

FIGURES 1-5. Anatomy of Cerithium atratum: 1, Head-foot of preserved c;> seen from right side.-2, Horizontal section of foot, c;> .-3, Central nervous system. -4, Young testis.-5, Half row of radula. See p. 494 for explanation of lettering. 500 Bulletin of Marine Science of the Gulf and Caribbean [14(3) Therefore, most of the water drawn into the deep and narrow pallial cavity by the branchial cilia can be used for removing the sandy faeces. These are expelled from the right anterior corner of the mantle edge by the exhalant current along a ciliated strip (Fig. 1, ex), overlain by a fold (x) of the mantle skirt. The color of the soft parts of C. vulgatum varies according to the locality where the snails live (Joannis, 1834). Risbec (1943) has indi- cated the anatomical colors of his species, and so we give those of living C. atratum for comparison: mantle edge transparent with white tentacles, mantle skirt with brown longitudinal streaks, floor of pallial cavity with patches of black pigment, osphradium a white bulge with pigmented leaf- lets, gilI yellowish with more black pigment in front than behind, hypo- branchial gland light greyish green, rectum brownish black, pallial oviduct orange, bursa often with brownish, receptaculum with silky contents, liver brown, testis bright golden yellow, and ovary creamy white. The osphradium is a bulge about 11 mm long and 0,2-0,3 mm broad, to the left of the gill. It extends along the mantle skirt from the region of the heart to the insertion of the siphon. Here the bulge curves to the left, exposing its bend to the inhalant current. This flexure occurs also in C. vulgatum (Bouvier, 1887: 132) and C. obeliscus (Risbec, 1943: Fig 12, os). The bulge is supported by a basal cord of vesicular cells and contains a thick nerve along its entire length. This nerve has multiple connections to nerves in the mantle skirt, and by way of these with the supra-intestinal ganglion. On either side of the base the osphradial epithelium forms a sharply limited cushion of high ciliated cells along the whole length of the bulge. These are evidently the sensory areas whose nerve fibres join the axial nerve. Near its crest the central bulge grows out into lateral leaflets about 140 JJ. long, narrower and less slanting than those in C. vulgatum (Bernard, 1890: Fig. 22 A), and alternate as in that species. As Bernard (p. 197) already has described, nerve fibres from the leaflets pass to the axial nerve. Behind and in front the osphradial leaflets shorten until they disappear in the foremost region and the fundus of the mantle cavity. Both males and females have about 190 gill filaments whose length de- creases inwards. Folds connecting the filaments with the hypobranchial gland, as in Littorina angulifera (Marcus, 1963: 12-13), were described for C. vulgatum (Bouvier, 1887: 132), but are not developed in C. atra- tum. Mucous gland cells are concentrated on the afferent (abfrontal) border of the leaflet; the strong supporting rods are restricted to the front- al area and do not extend to the region under the lateral cilia. Bittium varium has thin endoskeletal elements (Marcus, 1963: 79); other cerithi- ids have none (Johansson, 1956: 150). The large hypobranchial gland is compact, with a smooth surface, not folded transversely as is that of C. vulgatum (Bouvier, 1887: Fig. 34; 1964] Marcus & Marcus: On Cerithium Atratum 501 Bernard, 1890: 335). The anal papilla lies nearer to the mantle edge than the end of the female pallial duct.

NERVOUS SYSTEM Fig. 3 This system of Cerithium has been studied well by Bouvier (1887: 132 ff.); Sunderbrink (1929) has copied some of Bouvier"s figures erroneous- ly. The cerebral (c) and pleural (pi, pr) ganglia lie quite near to one an- other, and also the subintestinal ganglion (b) belongs to the central mass, as it is apposed to the left pleural ganglion (pi). The pedal ganglia (p) are a little smaller than the cerebral ones and located ventrally to and in front of the dorsal complex. The cerebra-pedal connectives run over the pleura-pedal ones, and both pairs are rather long. The statocysts (t) are in contact with the posterior border of the pedal ganglia and contain many small statocones and one bigger statolith. The buccal ganglia receive the cerebra-buccal connectives from the front, because these connectives (bu) run, as in C. vulgatum (Bouvier: 137), beyond the buccal mass and then turn backwards running on the sides and over the buccal mass. This course recalls the archaeogastropod an indirect connection of buccal to cerebral ganglia by way of the labial com- missure. The labial nerves are much thickened (lb) to the sides of the jaws, but are not gangliate. The anterior borders of the pedal ganglia (p) bear each a pair of accessory ganglia (a) from which groups of nerves arise. These form branches with secondary ganglia in the anterior part of the foot, as Brock (1889: 71) observed. He was puzzled (p. 76) by the rich nervous supply of the propodium in several burrowing prosobranchs. But in carnivores such as naticids and olivids, which grip their prey with the forefoot, a plentiful innervation can be easily understood by such locomotor and sensory activity. The same holds for Hastula cinerea (Marcus, 196'0: 35), whose very short tentacles may be compensated by the pedal sensory cells. The correlation between neuro-sensorial equipment of the foot and mode of life is really not so obvious in Cerithium atratum. Possibly the anterior pedal border, together with the tentacular papillae on the mantle edge, prevents the entrance of sand grains into the pallial cavity as in Natica (Fretter & Graham, 1962: 574). The morphologically right limb of the visceral loop begins with a long connection (sp) of the right pleural (pr) to the supra-intestinal ganglion, which is the osphradial and branchial centre. Outside the body cavity the left mantle nerve (I) which arises in the left pleural ganglion (pi) is linked with the anterior branchial nerve. The left pallial organs are possibly co- ordinated by this dialyneury. The fusion of the right mantle nerves (r) 502 Bulletin of Marine Science of the Gulf and Caribbean [14(3) emanating from the subintestinal (b) and the right pleural ganglion (pr) is less peripheral, but still lies within the body cavity. An impulse given to the columellar nerve (co) which carnes out of the subintestinal ganglion might be transmitted to the right side of the mantIe by way of this right dialyneury.

ALIMENTARY TRACT Figs. 5-7 Cerithium atratum is herbivorous. We observed it browsing upon the short growth on its own shell and saw the nibbling movements of the muzzle on the floor of a glass dish with a mirror. Together with detritus of plant origin, sand grains are ingested. Also foraminifers, eggs of turbellarians, copepods, and other matter were found in the gut. Ciliary feeding (Marcus, 1963: 78) was not seen. The jaws are strong plates, 0.5 mm broad, 0.27 mm long; their anterior part is covered with pegs 45 IL high and 6 IL thick. Of the two burrowing species studied by Risbec (1943: 93), one has strong mandibles, but in the other there is merely a hint of these structures, and also their buccal bulbs (Figs. 16, 39, 40) are of very different sizes. The biology of thcse species, C. obeliscus and C. fasciatum, is not known, so no comments can be made upon the anatomical differences of these two sand-dwellers. The buccal mass of C. atratum is haemoglobin red; the cartilages are black. The radula (Fig. 5) has up to 75 rows, and the general aspect of the teeth is, as in other lower Taenioglossa, "adapted for a variety of tasks: picking up particles, cutting and shredding, as well as sweeping and grazing" (Morton, 1958: 90). The rhachidian tooth is broader than high, has a prominent median cusp underlain by a smaller one and flanked by two pairs of broad denticles. The base is triangular in the middle and provided with lateral expansions. These are not easily seen and perhaps therefore not drawn in Troschel's figure of the otherwise similar radula of C. vulgatum (Fischer, 1887: Fig. 444; Sunderbrink, 1929: Fig. 49). The cutting edge of the lateral (intermediate) tooth has one strong cusp, one inner and 2-4 outer denticles; under the cusp there is a broad outgrowth. The base is elongated to the outer side and inserts near the bases of the narrow mar~inal teeth. These are high and have one principal prominence and 3-4 inner denticles. Furthermore the inner marginal tooth has 1-2 outer denticles, evidently absent in C. vulgatum. The radulae of Risbec"s species (1943: Figs. 18-19, 42-44) are less similar to the radula of C. atratum than that of C. vulgatum. The salivary glands are tightly winding thin tubes. Their fundi are coiled; the ducts pass through the nerve ring and their openings lie on the folds that bound the dorsal food-channel of the anterior oesophagus. The 1964] Marcus & Marcus: On Cerithium Atratum 503

7

12 me m

u rs

UO FIGURES 6-12. Anatomy of Cerithium atratum: 6, Stomach, opened from dorsal side.-7, Epithelial ridges of initial intestine.-8, Diagram of male organs.-9, Diagram of female organs.-IO, Transverse section of female organs at level shown by line 10 in Fig. 9.-11, Transverse section of female organs at level shown by line 11 in Fig. 9.-12, Newly hatched veliger. 504 Bulletin of Marine Science of the Gulf and Caribbean [14(3) epithelial cells of the glands are stuffed with blue-staining granules of secretion, evidently mucus. According to Bouvier (1887: 133) and Risbec (1943: 94), the salivary glands are different in the various species of Cerithium; the blind tubes of C. gemmulatum seem to be similar to the glands of atratum. The supra-intestinal branch of the visceral loop marks, as in other snails (Graham, 1939: 77), the anterior limit of the twisted part of the alimentary tract. In this part the densely ciliated food-channel is ventral; its epithelium contains mucus cells. Its bounding folds bear especially long cilia. The originally ventral, now dorsal, wall of the oesophagus forms two lateral pouches with many transverse folds as in Patella; their epithelium is pigmented and its secretion is predominantly spherical, as in Turritella communis (Graham, 1939: 95). The pouches are open ventrally along their whole length. Apart from this broad communication with the food-channel, the pouches allow for a comparison with the gland of Leiblein (Risbec, 1955: 48) in higher prosobranchs, thought to be stripped from the oesophagus pulled through the nerve ring (Graham, 1941: 13, 16). The dorsal pouches of the mid-oesophagus are Risbec's "jabot" (1943: 94); evidently they differ widely in size among the various species (ibid.: Figs. 39, 45, J). The posterior oesophagus has about 10 longitudinal folds, a small lumen, and ciliated epithelium with mucus cells. The oesophagus runs alongside the columella and enters (Fig. 6, 0) the ventral wall of the stomach, well in front of the digestive gland (d). Also in Cerithium vulgatum (Sunderbrink, 1929: Fig. 58), in the Cerithium species studied by Risbec (1943: Figs. 94-96), in Tympanotonus fuscatus (Johansson, 1956: Fig. 10), and in Bittium varium (Marcus, 1963: Fig. 83), the cardia lies in front of the liver opening. In the area between these apertures the wall bears transverse ciliated folds which attain the longitudinal fold bordering the intestinal groove. To the left of this groove extends the densely folded sorting area (sa). The apical region of the stomach behind the entrance of the liver duct, functionally the fundus, is formed by a smooth pouch, evidently without even the vestigial function of a spiral caecum. Also the intestinal groove does not begin in this pouch, but in front of a folded sub-apical belt. The dorsal wall of the stomach is occupied by a large cuticularized field (cu) supported by a high cushion of the gastric wall. The edges of this cuticular field are free; anteriorly it is continuous with the rather long gastric shield (g). Often a food string embedded in mucus adheres to the sticky surface of the cuticularized area, against which the head of the crystalline style bears. The longitudinal ventral fold (ve) is continuous with the major typhlosole (ma); the minor typhlosole begins in front of the sorting area. Both typhlosoles border the communication (y) of the intestine and the 1964] Marcus & Marcus: On Cerithium Atratum 505 sac containing the long crystalline style (cs) as high folds. For Cerithium the style was first described by Sunderbrink (1929: 306), and later on, independently, by Risbec (1943: 94 fl.); in an earlier study (Berkeley & Hoffman, 1835: Pl. 21, Fig. 10) the crystalline style of Telescopium telescopillm was seen, but not understood (Johansson, 1956: 158; with further references to styles of cerithiids). The sponge feeders among the Cerithiacea studied by Fretter (1951) have no style. The initial region of the intestine bears ridges, partly continuous, in part interrupted ones; the latter are rows of tubercles (Fig. 7). In Aporrhais pespelecani (Yonge, ]937; Fig. 5, R) and Bittillm varium (Marcus, 1963: 86) ridges in this region were described. In the surrounding connective tissue of this pyloric region accumulations of amoebocytes co-operating in digestion (references: Marcus, 1963: 87) are located. The major typhlosole (rna) is continued into the intestine (i) along the beginning of the loops around the style-sac. The faecal pellets are compacted in the part of the hind-gut that runs along the roof of the pallial cavity. They are placed obliquely (Fig. 9). In some cases the quantity of sand is too great to be divided into pellets sheathed with mucus. Such masses of sand can be removed from the pallial cavity by repeated retractions of the body into the shell, whereby jets of water are driven out of the mantle cavity, carrying the sand with them.

REPRODUCTIVE ORGANS (Figs. 4, 8-11) Of 20 measured adult snails from the Research Base, the females attain a greater size (28 mm) than the males (22 mm), but the measurements overlap. With a length of 15 mm, males and females can be distinguished by the bright golden yellow male and creamy white female gonads. The testis (h) is the uppermost organ of the visceral hump. Its ramified follicles are initially separate from one another (Fig. 4), subsequently becoming entwined (Fig. 8). They open into the common testis duct (e). The phase of separate testicular lobules was described also for C. fascia tum (Risbec, 1943: 98, Fig. 49). The testis duct runs coiled on the columellar side; farther in front it accompanies the oesophagus. Near the compound visceral ganglion, as already observed by Risbec (1943: 97), the male duct attains the mantle cavity. In the suture of the mantle the pallial efferent duct forms an open, deep, folded and glandular pouch (q) which belongs half to the roof and half to the bottom of the cavity, due to its position in the suture. Outwards the pouch flattens. This open sperm gro~)Ve(so) leaves the floor and runs along the roof beside the hind gut (i). Most of its glands have red granular secretion as is typical in prostates, but in the deep part of the pouch, in the suture, there are many blue- 5'06 Bulletin of Marine Science of the Gulf and Caribbean [14(3) staining glands, and some occur also among the red ones. In the outermost part, where the pouch narrows, there are only mucous glands. Opposite to the dorsal glandular groove the floor of the mantle cavity is ciliated. The pallial male duct ends with a small fold entally to the anus (or), near to the entrance of the right pallial nerve into the mantle skirt. The cilia on the floor of the cavity continue beyond the end of the sperm groove and in a furrow between two small folds on the right side of the head-foot. An organ corresponding to the glandular ovipositor is not developed in the male. The ovary lies outside the digestive gland and apically to it. The tubular oviduct (oi) runs along the stomach on the columellar side. The oesopha- gus is parallel to the intestine, and the oviduct lies between them. It opens into the red-staining albumen gland (Fig. 9, am). The following capsule gland (mc) together with the sperm-storing vesicles is a flat tube with a horizontal lumen (ov) lined with a ciliated epithelium. The pallial oviduct curves so that its concavity faces the columella, its convexity the hind-gut. A slit (ov) along the concave side extends over the ectal half or two thirds of this organ. The lumen separates a thinner upper part which lies within the mantle skirt and a thicker under portion projecting into the mantle cavity. The upper part contains mucous gland cells which in the innermost region of the pallial oviduct pass also onto the ventral side. The lower part consists principally of a roomy sperm-storing organ (u). It may be called a bursa copulatrix (Johansson, 1953: 11-12), though there is no true copulation. The bursa canal begins with a rather wide opening (uo) and extends backwards to the albumen gland. Its muscular wall is thick, its lining epithelium ciliated, its contents are sperms if.) whorls and strands, in the outer part orientated ones with heads fastened to the wall, and brown masses, evidently prostatic secretion. Powdered carbon is drawn into the slit of the oviduct by ciliary action, and thence also enters the bursa whose ental vesicle becomes filled with the black particles. To the wall of the bursa that faces the oviducal lumen (ov) the recep- taculum seminis (rs) lies tightly apposed. The receptaculum begins with a wide opening (ra) situated in the ental third of the oviduct. The organ is a flat tube dilating entally. Its contents have a silky aspect and consist of orientated sperms fastened to dorsal and lateral walls of the organ. The ciliated floor is free from sperm. Prostatic secretion is absent in the receptaculum. The principal amount of the ejaculated masses is evidently stored in the bursa, whose muscles may later on drive out smaIIer portions. A lump of sperm was found in front of the opening of the bursa canal and another halfway to the receptaculum. In a species without penis, spacious sperm-storing organs appear to be necessary in order to accumu- 1964] Marcus & Marcus: On Cerithium Atratum 507 late as much as possible of the material that is gained with the inhalant current. In Bittium reticulatum (Johansson, 1947: Fig. 1-6) and B. varium (Marcus, 1963: Fig. 87), species with two sperm-storing organs in the same position as in the present species, there is a third pouch in the dorsal part of the pallial oviduct; in Cerithium vulgatum there are only two as in C. atratwn, but they are located one in the dorsal and one in the ventral fold (Johansson, 1953: 2). A ciliated gutter (ex) on the floor of the mantle cavity runs down the right side. A little behind the fore end of the foot there is a glandular knob (or) which divides this gutter into a dorsal and a ventral branch. The action of this organ was seen in a spawning snail whose emerging eggs paused over the knob. Thus, we can call it an ovipositor, the secretion of which probably attaches the band of eggs to the substratum. In Littorina (Linke, 1933: 37-38; Marcus, 1963: 22-24) and Bittium varium (Marcus, 1963: 90), similar ovipositors occur. The largest egg mass was 8.5 em long and 2 mm broad; it was deposited by a snail 25 mm long and contained about 25,000 eggs. The bands consist of a string 0.4 mm wide, looping to and fro with about 4 eggs, 80 IL in diameter, to one level. The egg mass comes forth in batches, not continu- ously; in one hour about 1 em of the band is produced (29°C). The observed masses were fastened to the wall of the glass dish very firmly, a few millimeters above the surface of the sand. The first veligers came free 66 hours after spawning (24-29°C). Within the egg capsule their cilia move as slowly as the movements of the adult snails. The veliger (Fig. 12) hatches without tentacles and eyes; the outer lip of its shell is pointed.

DISCUSSION Cerithium atratum is a typical representative of the lower Mesogastro- poda: it is herbivorous and has a crystalline style, its central nervous system is concentrated, but primitive by dialyneury on both sides, and accessory pedal ganglia. Pouches of the mid-oesophagus, rather anterior entrance of the oesophagus into the stomach, absence of caecum, and elaborate ridges and tubercles in the pyloric region of the intestine are specialized features. The pallial genital ducts are open as in several other meso gastropods without penis, with tightly coiled spiral shell, narrow and deep mantle cavity, and large gill toward the left side (Fretter, 1953: 222). From the standpoint of functional morphology, however, the open condition of the pallial gonoducts cannot be explained (Johansson, 1953: 15-17): Trivia has a broad mantle cavity, a penis and an open oviduct, Melanella a penis and an open oviduct, Nassopsis and 2 species of Melania combine lack of 508 Bulletin of Marine Science of the Gulf and Caribbean [14(3) a penis with a closed oviduct. Open pallial gonoducts appear to be ancestral recurrences of primitive grooves rather than adaptive characters.

SUMARIO

Cerithiurn atraturn (BORN, 1778) (GASTER6PODA: PROSOBRANCHIA) El gaster6podo Cerithiurn atraturn (Born), reportado en los Cayos de la Florida y las Indias Occidentales, se encuentra comunmente a 10 largo de las costas de la America del Sur, desde Brasil hasta la Argentina. En la investigaci6n de la anatomia de esta especie se han usado ejemplares recogidos en fondos de arena gruesa, en la zona de la marea, cerca de Ubatuba, Brasil. Se observaron ejemplares mantenidos vivos en el labora- torio y se encontr6 que son de movimientos lentos y tlmidos. Se describe en detalle la concha, que alcanza un largo de 38 mm, con 9-20 costillas axiales. La cabeza, que dorsalmente tiene lineas negras, es redondeada y tiene un hocico ancho y aplastado. El pie es pequeno, no tan largo como la abertura de la concha, con un surco anterior profundo. Sus superficies ventral y lateral son ciliadas como 10 son tam bien sus surcos epipodiales pero no las crestas epipodiales. EI borde del manto tiene una hilera de cortos tentaculos a 10 largo del frente y de los dos costados como se ha descrito en algunas otras especies de Cerithium. El sif6n es corto. Se describe la circulaci6n de la corriente de agua. Se investigan el osphra- dium y las branquias. El sistema nervioso, descrito ya para el genero Cerithiurn por otros autores, se discute brevemente y se compara con el de otras especies. Se describe el conducto digestivo de C. atratum, que es herbivoro, incluyendo las mandibulas, radula, glandulas salivales, rotaci6n visceral, es6fago, est6mago, tifosoles e intestinos. Se investig6 el con due to reproductivo en ambos sexos: testiculos, conducto palial masculino, ovario, oviducto, glandula de la capsula, bolsa de la esperma y estructuras acceso- rias, y se menciona brevemente el desove y las caracteristicas de la mas a de huevos y de las larvas. LITERATURE CITED

ABBOTT, R. TUCKER 1955. American seashells. New York, D. van Nostrand, xiv + 541 pp., 40 pIs. . . . 1958. The marine mollusks of Grand Cayman Island, BntIsh West Indies. Monogr. Acad. Nat. Sci. Philadelphia, 11.. 1-138. BERNARD, FELIX 1890. Recherches sur les organes palleaux des Gasteropodes prosobranches. Ann. Sci. nat. ZooL, ser. 7, 9: 89-404. BERKELEY, M. J. AND G. H. HOFFMAN 1835. A description of the anatomical structure of Cerithium telescopium. ZooL J., 5: 431-439. BOUVIER, E. L. 1887. Systeme nerveux, morphologie generale et classification des Gaste- ropodes prosobranches. Ann. Sci. nat. Zool., ser. 7,3: 1-510. 1964] Marcus & Marcus: On Cerithium Atratum 509 BROCK, J. 1889. Zur Neurologie der Prosobranchier. Zeitschr. wiss. Zoo!., 48 (1): 67-83. BucKuP, LUDWIG AND ERICA HELENA BUCKUP 1957. Catalogo dos moluscos do museu Riograndense ... Iheringia, 1: ]-40. COOMANS, H. E. 1958. A survey of the littoral Gastropoda of the Netherlands Antilles and other Caribbean islands. Stud. Fauna Cura<;;ao,8 (3]): 42-111. DALL, W. H. AND C. T. SIMPSON ]901. The of Porto Rico. Bull. U.S. Fish Comm., 20 (Part 1): 351-524. FISCHER, PAUL 1887. Manuel de Conchyliologie. F. Savy, Paris, xxiv + ]369 pp., 23 pIs. FRETTER, VERA 1951. Observations on the life history and functional morphology of Cerithiopsis tubercu/ata (Montagu) and Triphora perversa (L.). J. mar. Bio!. Ass. U. K., 29: 567-586, 6 figs. 1953. The transference of sperm from male to female prosobranch, with reference, also, to pyramidellids. Proc. Linn. Soc. London, session 164 (2): 217-244. FRETTER, VERA AND ALASTAffi GRAHAM 1962. British prosobranch molluscs. Ray Society, London, xvi + 755 pp., 3] 7 figs. GOFFERJE, CARLOS N. ]950. Contribui<;;ao a zoogeografia da malacofauna do litoral do Estado do Parana. Arq. Mus. Paran., 8: 221-282, pIs. 31-35. GRAHAM, ALASTAIR 1939. On the structure of the alimentary canal of style-bearing proso- branchs. Proc. zool. Soc. London, ser. B, 109: 75-112. 1941. The oesophagus of the stenoglossan prosobranchs. Proc. R. Soc. Edinb., 61 (1): 1-23. IHERING, HERMANN V. 1897. A ilha de Sao Sebastiao. Rev. Mus. Paulista, 2: 129-171. JOANNIS, L. DE 1834. Sur l'animal de Cerithium vulgatum. Mag. Zoo!., 4: Classe Y, PI. 52, 1 page. JOHANSSON, JOHAN 1947. Vber den offenen Uterus bei einigen Monotocardiern ohne Kopula- tionsorgane. Zoo!. Bidr., 25: 102-110. 1953. On the genital organs of some mesogastropods ... Zool. Bidr., 30: 1-23. 1956. On the anatomy of Tympanotonus fuscatus ... Atlantide Rep., 4: 149-166. JOHNSON, C. W. ]934. List of marine Mollusca of the Atlantic coast from Labrador to Texas. Proc. Boston Soc. Hist. Nat., 40 (1): 1-204. KEEN, A. MYRA 1958. Sea shells of tropical West America. Stanford University Press, Stanford, California, viii + 626 pp.; 10 pIs. KOBELT, WILHELM 1898. Die Gattung Cerithium. Martini-Chemnitz, Conch. Cab., 2nd ed., 1 (26): 1-297. 510 Bulletin of Marine Science of the Gulf and Caribbean [14(3)

LANGE DE MORRETES, FREDERICO 1949. Ensaio de cat{t1ogo dos moluscos do Brasil. Arq. Mus. Paran., 7 (l) : 5-216. LINKE, OTTO 1933. Morphologie und Physiologie der Nordseelittorinen. Wiss. Meeresun- tersuch. Abt. Helgoland, 19, fasc. 2 (5): 1-60. MARCUS, EVELINE AND ERNST ]960. On Haslula cinerea. Bol. Fac. Fil. Univ. S. Paulo. Zoologia, 23: 25-66. 1962. On Leucozonia nassa. Bol. Fac. Fil. Univ. S. Paulo, Zoologia, 24: 11-30. ]963. Mesogastropoden von der Kliste Sao Paulos. Abhandl. Akad. Wiss. Mainz, Math. Nat. KI., Jahrg. 1963,1: 1-105. MORTON, J. E. 1958. Molluscs. Hutchinson University Library, London, 232 pp., 23 fig5. OLIVEIRA, LEJEUNE P. H. DE ]950. Levantamento biogeognifico da baia de Guanabara. Mem. Inst. Os- waldo Cruz, 48: 364-391. ORBIGNY, ALCIDE D' 1841. Mollusques. Voyage dans l'Amerique Meridionale, 5 (3): 409-488. PERRIER, REMY 1889. Recherches sur l'anatomie et l'histologie des Gastcropodes proso- branches. Ann. Sci. nat. Zool., ser. 7, 8: 61-3]5. PERRY. LOUISE M. AND JEANNE S. SCHWENGEL 1955. Marine shells of the western coast of Florida. Paleontological Re- search Institution, Ithaca, New York, 3 I 8 pp., 55 pIs. REEVE, LOWELL AUGUSTUS 1865. Monograph of the genus Cerithium. Conchol. Icon., 15, spec. 1-149. RISBEC, JEAN 1943. Recherches anatomiques sur ]es prosobranches de Nouvelle Caledo- nie, pt. 4. Ann. Sci. nat. Zool., ser. 11, 5: 89-112. ]955. Observations sur l'anatomie comparee et la classification des Gastero- podes prosobranches. J. ConchylioI., 95: 45-82. SMITH, EDGAR A. 1890. Mollusca. In: H. N. Rid]ey, Notes on the Zoology of Fernando Noronha. J. Linn. Soc. London, Zool., 20: 483-503. SOUZA LOPES, HUGO DE AND MOACIR ALVARENGA 1957. Contribuic;ao as conhecimento dos moluscos da ilha Fernando de Noronha, Brasil. Bol. Inst. Oceanogr. S. Paulo, 6 (1-2) (1955): 157-196. SUNDER BRINK, OTTO 1929. Zur Frage der Verwandtschaft von Melaniiden und Cerithiiden. Z. Morph. bkol. Tiere, 14 (2): 216-337. YONGE, C. M. 1937. The biology of Aporrhais pes-pelecani and A. serresiana. J. mar. BioI. Ass. U. K.. n. ser., 21 (2): 687-703.