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Epitonium Millecostatum and Coralliophila Clathrata: Two Prosobranch Gastropods Symbiotic with Indo-Pacific Palythoa (Coelenterata: Zoanthidae)L

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Epitonium Millecostatum and Coralliophila Clathrata: Two Prosobranch Gastropods Symbiotic with Indo-Pacific Palythoa (Coelenterata: Zoanthidae)L Pacific Science (1980), vol. 34, no. 1 © 1981 by The University Press of Hawaii. All rights reserved Epitonium millecostatum and Coralliophila clathrata: Two Prosobranch Gastropods Symbiotic with Indo-Pacific Palythoa (Coelenterata: Zoanthidae)l ROBERT ROBERTSON2 ABSTRACT: Two little known prosobraneh gastropods, the wentletrap Epitonium millecostatum (Pease 1860-1861) and the muricacean Coralliophila clathrata (A. Adams 1854), are both obligate symbionts of the colonial zoanthid sea anemone Palythoa. Data are given on the taxonomy of both gastropods, and on their symbioses in the Maldive Islands, Sri Lanka (Ceylon), and the Great Barrier Reef, Australia. Neither species had been reported previously from any of these regions, and the known range of C. clathrata is also extended to Zanzibar and the Marquesas Islands. Coralliophila sugimotonis Kuroda 1930 is shown definitely to be a synonym of C. clathrata. Palythoa sloughs off nematocysts and zooxanthellae in its mucus, and both gastropods ingest this;·they do not ingest the Palythoa tissue or polyps, which contain sand grains. The feces of the Epitonium consist chiefly of discharged nematocysts; while those of the Coralliophila consist chiefly of remnafits of zooxanthellae. Both species presumably digest the mucus. The Epitonium also digests the zooxanthellae, thereby being in part herbivorous, and the Coralliophila apparently also digests the nematocysts. Both species have small eggs and a planktotrophic larval stage lasting about a morith or more. The larvae of the two species must have well-developed settl~ment responses to Palythoa, which is sparsely and patchily dispersed in shallow water. Frequencies of the adult gastropods with Palythoa are low, DESPITE THEIR NEMATOCYSTS, many kinds of when injected into mammals (Moore and coelenterates are host to symbiotic pros­ Scheuer 1971). obranch and opisthobranch gastropods that three kinds of gastropods have been re­ feed on their tissues or mucus. One such host ported as symbionts with Palythoa: a nudi­ is the colonial toanthiniarian sea anemone branch, a group of architectonicids, and or soft coral Palythoa (family Zoanthidae). various coralliophilids (muricaceans). The Palythoa is a tropical genus that. occurs nudibranch is the specialized eolid Aeolidiop­ around the wotid in shallow water; Iorming sis ransoni Pruvot-Fol (i956), reptmed only small to large incrustations on hard sub­ from the Tuamotu archipelago (Polynesia). strates. Palythoa has zooxanthellae, sand According to Pruv'OtoFol (1956) it feeds on grains, and three kinds of nematocysts the tissues of Palyihoa and has sand grains (Hyman 1940) embedded in its tissues, and in its gut. extracts from som~ species are highly toxic the architectonicid genus Heliacus is obil.gately symbiotic with zoanthiniarians (Robertson 1967). A Heliacus feeds by evert­ 1 This work was partially supported by United States ing its long acrembolic proboscis and National Science Foundation grant no. DEB 76-18835. makihg a deep hole in its host. Heliacus feces Manuscript accepted 15 March 1980. conHtin zooxanthellae and sand grains. 2 Academy of Natural Sciences, Department of Malacology, Nineteenth and the Parkway, Philadelphia, Their larvae are planktotrophic. Pennsylvania 19103. The first gastropod reported to have been 2 PACIFIC SCIENCE, Volume 34, January 1980 FIGURE I. Specimen 29 and specimen 30 (arrow) of Epitonium millecostatum with egg capsules on underside of edge of incrustation of Palythoa. Great Barrier Reef, Australia. found with Palythoa (as Corticifera, a syn­ 1850) is another Palythoa symbiont (Men­ onym) was Coralliophila sugimotonis Kuroda donl;a de Oliveira 1971; ANSP collection). (1930, 1931) [=c. clathrata (A. Adams In an abstract, Robertson (1966) lists 1854)], described from Japan. The associa­ "Epitonium sp." and "Coralliophila cf. C. tion apparently is a true symbiosis, i.e., sugimotonis Kuroda, 1930-31" as symbiotic the occurrence of this Coralliophila with with Palythoa in Ceylon and the Maldives. Palythoa is consistent (Sugimoto 1929). The The present paper treats the taxonomy, same seems to be true of C. squamosissima zoogeography, and some aspects of the (E. A. Smith 1876), the synonymy of which ecology and life history of two prosobranch was treated by Kilburn (1977). Kuroda symbionts of Palythoa in the Indo-Pacific: (1931) recorded this second Coralliophila the wentletrap Epitonium millecostatum with Corticifera (=Palythoa) in Japan (as (Pease 1860-1861) (Figure I) and the muri­ C. stearnsii Pilsbry 1895), and Kilburn cacean Coralliophila clathrata. (1972) recorded it with Palythoa in South Africa [as C. meyendorffi (Calcara)]. Also, the Academy of Natural Sciences of Phil­ MATERIALS AND METHODS adelphia has two specimens of C. squamosis­ sima (ANSP 302792) embedded in a piece of Palythoa was torn up in search for proso­ Palythoa from Okinawa. In the tropical branchs when general collections of mollusks western Atlantic, C. aberrans (C. B. Adams were made in Sri Lanka and the Maldive Prosobranch Symbionts of Palythoa-RoBERTSON 3 Islands during the International Indian Island host or hosts to species. More than Ocean Expedition in 1964. More intensive one species may be present. Thus, the two investigations were made during a visit to gastropods associated with Palythoa at the Lizard Island Research Station, Great Lizard Island mayor may not be host­ Barrier Reef, northern Queensland, Aus­ specific. The Palythoa specimens range in tralia, from 30 May to 13 June 1979. At color from reddish or yellowish brown Lizard Island the epitoniums were at depths through tan, sometimes with a greenish between about 0.5 and 2 m below mean low tinge. 3 The polyps do not project much water, except for specimen 42, which was an above the coenenchyme. The septa per empty shell embedded in Palythoa, found by average-sized polyp range from 40 to 46 Ian Loch while scuba diving at a depth of 5 (four counts; mean 42). The Indian Ocean m. Loch also found the single Lizard Island species possibly is the same species as that at specimen of Coralliophila clathrata while Lizard ·Island. scuba diving at a depth of 10m. Palythoa ranges from the lower intertidal The Indian Ocean prosobranchs were zone down to at least 15-16 m off North dropped unrelaxed into 70 percent ethyl al­ Point, Lizard Island (fide Ian Loch). Most cohol. The Great Barrier Reef prosobranchs of the Palythoa torn up was in 0.5-2 m of were relaxed with MgClz and then pre­ water. No large incrustations such as occur served. Three of the epitoniums were fixed in Sri Lanka and the Maldives were seen. in Bouin's solution, which dissolved the Old colonies split up into clusters of daugh­ shells and enabled me to sex the specimens. ter colonies about 5-10 cm in diameter. The (Epitoniid spermatozeugmata and oocytes prosobranchs seemed mainly to be with can readily be distinguished in the gonads small, isolated colonies of the anemones. even with a dissecting microscope.) Other specimens, preserved in alcohol, were sexed either by crushing the shells or by boiling them to loosen the attachment of the col­ SUPERFAMILY EPITONIACEA (= PTENOGLOSSA) umellar muscle and removing the body with FAMILY EPITONIIDAE a pin. Radulae were extracted (or in the case of the Coralliophila, searched for) from Epitonium millecostatum (Pease 1860-1861) whole bodies with Clorox (5.25 percent SYNONYMY: sodium hypochlorite). Eggs and veligers were studied, measured, and drawn with the Scalaria millecostata Pease (1860-1861: 400, unfigured [Sandwich (Hawaiian) aid of a compound microscope. Feces of Islands]). Holotype (BMNH) discussed and both species were collected from the outer edge of the operculum. illustrated by Kay (1965: 42-43, pI. 6, Sample specimens of Palythoa are retained figs. 5-6). Scala millecostata (Pease). E. A. Smith along with the gastropods in the malacology (1901: 109, pI. I, fig. 5). collections of the Academy of Natural Epitonium millecostatum (Pease). Pilsbry Sciences of Philadelphia and the Australian (1921:377) and Kay (1979:155, fig. Museum, Sydney, Australia. Museum abbre­ 54H). viations used in the text are: AMS, Australian Museum; ANSP, Academy of Natural Sci­ SHELL (Figure 2): An all-white Epitonium ences of Philadelphia; BMNH, British Museum attaining a length of 9.7 mm and an (excep­ (Natural History); SDSNH, San Diego Society tional) width of 7.1 mm, with about 6~ of Natural History. teleoconch whorls. Thin and fragile. Pro- PALYTHOA 'The same or a similar Great Barrier Reef Palythoa Palythoa taxonomy is in such chaos that it has been well illustrated in color (as P. mesial by Gillett is presently impossible to identify the Lizard and McNeill (1959); the polyps are shown closed. 4 PACIFIC SCIENCE, Volume 34, January 1980 50 f1 m ~ 3 FIGURE 3. Representative radular tooth of Epitonium mi//ecostatum. ally also on later whorls of large shells. Axial ribs not prominent at shoulder. No basal spiral cord. Aperture round; umbilicus small. The shells of Epitonium millecostatum have far more axial ribs than any other epitoniid; the rolled over axial ribs are also characteristic. APPEARANCE AND HABITS: Coloration of body contrasts with that of Palythoa: trans­ lucent yellowish cream, with yellowish white superficial mottling on the dorsal front end of the foot; subsurface white granules medial and posterior to each eye; pigmented mantle 2mm organ purple-red with a little orange-yellow. Large individuals crawl with difficulty, the FIGURE 2. Shell of Epitonium mi//ecostatum (speci­ foot being folded transversely. A mucous
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