Some Aspects of the Anatomy, Reproduction, and Early Development of Cerithium Nodulosum (Bruguiere) (Gastropoda, Prosobranchia)1 JOSEPH R

Some Aspects of the Anatomy, Reproduction, and Early Development of Cerithium nodulosum (Bruguiere) (Gastropoda, Prosobranchia)1 JOSEPH R. HOUBRICK2

ALTHOUGH MEMBERS of the prosobranch genus reef shelves, occurring subtidally on rocky, sandy Cerithium occur in abundance throughout the substrates just shoreward of the reef edge. A warm, shallow, tropical waters of the world, total of 16 specimens collected from Japtan little is known of their general ecology or life Reef had a mean length of 101 mm; the popu histories (Anderson, 1960). For the most part, lation consisted of 14 females and two males only brief reports or notes have been published with no sexual dimorphism evident in radulae, on the reproduction and early development of shell size, or sculpture. Cerithium species, namely C. vulgatum (Lo Although Risbec (1943) discussed the gen Bianco, 1888), C. ferrugineum (Lebour, 1945), eral anatomy of C. nodulosum, he did not ex C. obeliscus (Ostergaard, 1950), C. morus (Na amine the pallial genital ducts in detail nor did tarajan, 1958), C. atratum (Marcus and Marcus, he observe any males. Freshly dissected males 1964), C. algicola (Davis, 1967), C. variabile which I examined had bright orange testes and (RaeiWe, 1968), C. stercusmuscarum (Wolf their sperm ducts were packed with both eu son, 1969), and C. litteratum and C. auricoma pyrene and apyrene sperm. The pallial genital (D'Asaro, 1970). ducts were open and consisted of lateral (left) The evidence at hand (Sunderbrink, 1929; and medial (right) laminae which were fused Risbec, 1943; Johansson, 1947, 1953, 1956; dorsally to each other and to the mantle. The Marcus and Marcus, 1964) indicates that mem dosed sperm duct terminated in the pocketlike bers of this genus are aphallic; have open, pal proximal portion of the pallial genital groove. lial, genital ducts; lay their eggs, either as a This area was thick and glandular and probably tangled mass or a flattened coil, in gelatinous functioned as a prostate. Beyond the prostate strings or filaments attached to a substratum; area the genital groove extended forward as a and hatch out as planktotrophic veligers. slitlike channel open to the mantle cavity. The I wish to express my appreciation to Dr. epithelial lining of the inner walls of the lam Philip Helfrich of the Hawaii Institute of inae was thrown into small folds extending Marine Biology for his suggestion to use the distally. These folds appeared to be somewhat Eniwetok Marine Biological Laboratory for this glandular but not as highly developed as those work. of the proximal portion of the genital groove. Ripe females had bright yellow ,ovaries which ANATOMY were filled with ova and ooeytes. The oviduct (0, Fig. 1)' was a closed tube leading into the C. nodulosum is the largest species in the proximal portion of the open pallial duct. The genus and occurs throughout the Indo-Pacific general morphology of the female pallial re region, but not in Southern Japan or Hawaii productive tract was found to be similar to that (Demond, 1957). I studied it at Eniwetok described for males except that the laminae Atoll, Marshall Islands, during August 1970, were larger and more glandular with a thinner where it is moderately common on the windward nonglandular portion along the edge of the 1 Support for this work was provided by the U.S. medial lamina. The proximal end of the ovidu Atomic Energy Commission through the University of cal groove (og, Fig. 1) which constitutes the Hawaii and the Eniwetok Marine Biological Labora albumen gland (ag, Fig. 1) was thick and the tory. Manuscript received March 11, 1971. epithelial lining of the inner walls of the 2 Smithsonian Institution, Smithsonian Oceano graphic Sorting Center, Washington, D.C. 20560. laminae was somewhat flat, with little evidence 560 Some Aspects of Cerithi11m nodulosum-HouBRlcK 561 of folds. Distal to this was a glandular medial impossible. Moreover, there were strong ciliary portion of the open duct which probably func currents leading from the proximal to the distal tions as the capsule gland (cg, Fig. 1); here portion of the groove and it would seem impos the inner walls of the laminae were glandular sible for the sperm to swim against such a and folded. At the distal end of the oviducal current if they were to move from the recep groove on the edge of the nonglandular portion taculum up to the site of fertilization. Perhaps of the lamina was a short slit (scg, Fig. 1), the sperm stored in the bursa are moved out of the sperm-collecting gutter of Johansson (1953), aperture into the lumen and down the groove which measured about 5 mm in length and led to the distal receptaculum seminis where they into the opening of a long, ciliated, flattened are stored. Subsequently they may leave the re tube (ct, Fig. 1). This tube ran inside the ceptaculum seminis, be drawn into the ciliated entire length of the medial lamina (ml, Fig. 1) slit, and move up into the bursa again prior to and enlarged into a chamber (bc, Fig. 1) lo fertilization and oviposition. Thus the bursa cated at its proximal end. Within this chamber may function as an intermediary receptaculum were found eupyrene sperm mixed with a yel seminis because the sperm could then move lowish mucus and thin jellylike strands of un through the aperture and fertilize the eggs be known function. Johansson (1947) called this fore they passed through the albumen and cap area in C. vulgatum the bursa copulatrix. Within sule glands. the bursa, embedded in the wall of the inner portion of the medial lamina, was a pink glan REPRODUCTION AND DEVELOPMENT dular area (ga, Fig. 1) resembling a warty Pairing was observed in the field, but the flap. Under this area a tiny opening led mechanism of sperm transferral was not seen. through the wall of the lamina into the lumen It is no doubt similar to that process described of the proximal oviducal groove (og, Fig. 1). by Fretter (1951) for Cerithiopsis in which Ciliary currents led from the bursa through the sperm, liberated with prostatic fluid, are im glandular area and its opening into the lumen. mediately drawn into the inhalent siphon of The unfertilized eggs left the closed oviduct the female and thence into her mantle cavity. in this portion of the lumen. I believe that this One female, measuring 110 mm long and must be the site of fertilization, and that sperm 50 mm wide, was observed depositing her egg stored in the chamber are transported through mass. She was partially buried in the thin sand the glandular aperture into the proximal open covering a limestone shelf. The crescent-shaped part of the duct where they fertilize the eggs egg mass was attached to the rocky substrate as the latter move into the open portion of the and was also partially covered with sand. The oviduct. As the fertilized eggs continue to move egg mass of Cerithium nodulosum (Fig. 2a) down the open groove, albumen and the hyaline proved to be quite distinctive in contrast to membrane are laid down around them. At the those described for other cerithiids. This egg distal end of the oviducal groove, opposite the mass consisted of a thick, ribbonlike, axial base slit on the medial lamina where the lateral which was of jellylike consistency. To this base lamina (11, Fig. 1) was fused to the dorsal were attached clusters of many coiled strings or body wall of the animal, was situated a pink filaments folded about themselves. The filaments glandular area within which was an opening were also jellylike and were covered with sand leading to a thin tube measuring 16 mm long grains. The whole mass was crescent shaped and 3 mm wide. This tube was also filled with and, in many respects, closely resembled that sperm and was called the receptaculum seminis described for Strombus (Robertson, 1959; by Johansson (1947) in C. vulgatum. It was D'Asaro, 1965). Detached from the substrate, found just beneath the epithelium. It is difficult the basal axial position of one egg mass mea to understand the function of a receptaculum sured 55 mm long and 6 mm wide. Each seminis located in the distal portion of the geni cluster of filaments attached to this basal axial tal duct. Eggs reaching this area would already portion averaged 12 mm in length, and 33 clus have been encapsulated, making fertilization ters of filaments were attached to this axis. The 562 PACIFIC SCIENCE, Volume 25, October 1971 ga

ml---"1l cg

scg

so Some Aspects ,of Cerithium IZodulosum-HouBRIcK 563

b , I -''Ytr<~'\'\ '.; ,\ st elm he

:\:1 M m

FIG. 2. a, Egg mass of Cerithium nodulosum detached from substrate and stretched to full length; b, portion of filament with sand grains removed to show zygotes; c, newly hatched veliger partially retracted in shelL SYMBOLS: elm, external limiting membrane; he, hyaline capsule; z, zygote; da, digestive anlage; f, foot; op, operculum; st, statocyst; v, velum.

individual filaments (Fig. 2b) were cylindrical, zygotes (z, Fig. 2b), .138 mm in diameter. covered with an external limiting membrane There were approximately 500 egg capsules per (elm, Fig. 2b) and measured 1 mm in diam centimeter of filament and the whole egg mass eter. Within this diameter, four to, five egg was estimated to. contain 66,000 eggs. Egg capsules were found. Egg capsules. (he, Fig. 2b) capsules did not appear to touch each other measured about .280 mm in diameter and the and there were thin membranous transparent

, FIG. 1. 'Diagrammatic representation of pallial portion of female genital duct in Cerithium nodulosum. ag, albumen gland; ars, aperture of receptaculum seminis; be, bursa copulatrix; cg, capsule gland; em, colu mellar .muscle; ct, ciliated tube; ga, glandular area; 11, latterallamina; me, mantle edge; ml, medial lamina; 0, oviduct; og, oviducal groove; rs, receptaculum seminis; scg, sperm collecting gutter; sn, snout; t, tentacle. Arrows represent ciliary currents. 564 PACIFIC SCIENCE, Volume 25, October 1971

strands which often appeared between them. ter, 1951), and Tympanotonus (Johnansson, The eggs and zygotes were moderately telole 1954). They also resemble those described for cithal and cleavage was unequal. Blastulation pleurocerids by Dazo (1965). Johansson's occurred rapidly within 5 hours of deposition. (1954) interpretation of the function of the Depending upon their position in the egg mass, chamber located in the outer portion of the some zygotes were already undergoing cleavage medial lamina as a bursa copulatrix is probably and blastulation by the time oviposition had correct; however, the glandular area and its ceased. Gastrulation was also rapid and ap opening in the wall of the bursa were not men peared to occur by epiboly. Within 24 hours tioned by him. I have found it in all members early larval stages were present and revolving of the genus that I have examined. It may serve within their individual hyaline capsules. A day as an auxiliary receptaculum seminis prior to later larvae attained a recognizable veliger stage. fertilization. The location of the receptaculum Veligers have a well-defined bilobed velum cov seminis near the distal portion of the gonadal ered with compound cilia (v, Fig. 2c). The duct is puzzling. Sperm leaving the bursa may shell is tan colored, caplike and large, and travel down the gonadal duct and be initially covers the digestive anlage (da, Fig. 2c). A stored there. Then, during oviposition, they prominent ciliated foot (f, Fig. 2c) and oper may leave it and again enter the sperm-collect culum (op, Fig. 2c) were also evident, and the ing gutter, ciliated tube, and bursa, to be eventu veligers continued to revolve in their capsules. ally stored in the glandular area of the bursa At the end of two days, eye spots and statocysts prior to fertilization. Oriented sperm have been (st, Fig. 2c) were seen and the shell had a seen in this glandular area, but no sectioning definite coil to it. Hatching took place in 3 days was done and such a function remains uncon but varied according to the position of the egg firmed. in the egg mass. The egg capsule appeared to The egg mass of Cerithium nodulosum differs collapse due to the ciliary beat of the velum from other cerithiid spawns in the thick axial and the emerging free-swimming veligers ap base by which it is attached to the substrate. peared to have lost their compound cilia; they Otherwise the filaments of the mass are quite were rapid swimmers and darted about quickly. typical for the group. Development is also simi The embryonic shells were brown and lightly lar to that described for other species of Ceri pitted. The operculum was unusually large in thium which have planktonic life stages. comparison to observations made on opercula of other Cerithium species. Free-swimming veli gers were maintained in aquaria for 3 days LITERATURE CITED after hatching but died thereafter. The length ANDERSON, D. T. 1960. The life histories of of their planktonic life remains unknown. marine prosobranch gastropods. Journal of the Malacological Society of Australia, no. DISCUSSION 4, pp. 16-29. The anatomy of the reproductive tract of C. D'AsARo, C. 1965. Development of Strombtls nodulosum is similar to other Cerithium species gigas. Bulletin of Marine Science, vol. 15, no. examined from Eniwetok and appears to be 2, pp. 359-416. representative of the cerithiids as a group. My --- 1970. Egg capsules of prosobranch present work on the genus in Florida and the mollusks from South Florida and the Ba Caribbean generally confirms the fact that both hamas and notes on spawning in the labora male and female reproductive tracts are open tory. Bulletin of Marine Science, vol. 20, in the pallial region and follow the general no.2,pp.414-440. pattern described by Johansson (1954) for the DAVIS, C. C. 1967. Emergence of veliger larvae Cerithiaceae. The open gonadal ducts of Ceri from eggs in gelatinous masses laid by some thium are similar to those described for the Jamaican marine gastropods. Malacologia, closely related genera Bittium (Johansson, 1947; vol. 5, no. 2, pp. 299-308. Fretter and Graham, 1961), Cerithiopsis (Fret- DAZO, B. C. 1965. The morphology and natural Some Aspects of Cerithittm nodttlosttm-HouBRlcK 565

history of Plettrocera amta and Goniobasis Mittheilungen an der Zoologischen Station livescens (Gastropoda: Cerithiacea: Pleuro zu Neapel (Leipzig), vol. 8, pp. 385-440. ceridae). Malacologia, vol. 3, no. 1, pp. 1-80. MARcus, E., and E. MARCUS. 1964. On Ceri DEMOND, J. 1957. Micronesian reef-associated thium atratum (Born 1778) (Gastropoda: gastropods. Pacific Science, vol. 11, no. 3, Prosobranchia). Bulletin of Marine Science pp. 275-341. of the Gulf and Caribbean, vol. 14, no. 3, FRETTER, V. 1951. Observations on the life pp. 494-510. history and functional morphology of Ceri NATARA]AN, A. V. 1958. Studies on the egg thiopsis tttbercttlaris and Triphora perversa. masses and larval development of some Journal of the Marine Biological Association prosobranchs from the Gulf of Mannar and of the United Kingdom, vol. 29, pp. 567 the Palk Bay. Proceedings of the Indian 586. Academy of Sciences, vol. 46, pp. 170-228. FRETTER, V., and A. GRAHAM. 1962. British OSTERGAARD, J. M. 1950. Spawning and de prosobranch mollusks. Ray Society, London. velopment of some Hawaiian marine gas 755 pp. tropods. Pacific Science, vol. 4, no. 2, pp. JOHANNSON, J. 1947. Dber den offenen Uterus 75-115. bei einigen Monotocardiern ohne Kopula RAEIHLE, D. 1968. Notes on captive Cerithium tionsorgan. Zoologiska bidrag fron Uppsala, variabile and Mitra fioridana. Annual Re vol. 25, pp. 102-110. port of the American Malacological Union, --- 1953. On the genital organs of some Inc. for 1968, pp. 35-36. mesogastropods: Cerithium vulgatum, Brug., RrSBEC, J. 1943. Recherches anatomiques sur Triphora perversa (1.) and Melanella (Eu les prosobranches de Nouvelle-Caledonie. lima) intermedia (Cantr.). Contributions to Annales des Sciences Naturelles, Zoologie, the phylogeny of the pallial gonoducts of series 11, vol. 5, pp. 89-112. the prosobranchia. Zoologiska bidrag fron ROBERTSON, R. 1959. Observations on the Uppsala, vol. 30, pp. 1-23. spawn and veligers of conchs (Strombus) in ---1954. On the anatomy of Tympanotonus the Bahamas. Proceedings of the Malacologi fuscatus including a survey of the open pallial cal Society of London, vol. 33, no. 4, pp. oviducts of the Cerithiaceae. Atlantidae Re 164-172. port, vol. 4, pp. 149-166. SUNDERBRINK, O. 1929. Zur Frage der Ver LEBOUR, M. V. 1945. The eggs and larvae of wandtschaft zwischen Melaniiden und Cer some prosobranchs from Bermuda. Proceed ithiiden. Zeitschrift fUr Morphologie und ings of the Zoological Society of London, mikroskopische Anatomie, vol. 14, pp. 261 vol. 114, pp. 462-489. 337. LoBIANCO, S. 1888. Notizie biologiche rigu WOLFSON, F. H. 1969. Spawning notes IV: ardanti specialmente il periodo di maturita Cerithium stercusmuscamm. Veliger, vol. 11, sessuale degli animali del golfo di Napoli. no. 4, pp. 441-442.