Argonauta, IX (10- 12): 3- 10
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A coral-associatedepitoniid, new to the Red Sea
(Prosobranchia, Ptenoglossa)*
Marco Oliverio**
Marco Taviani
Dip. Biologia Animale e dell'Uomo, Istituto di Geologia Marina C.N.R., "La Sapienza" Rome University, Via Gobetti 101, 1-40129, V.le dell'Università 32, 1-00185 Rome, Italy. Bologna, Italy e-mail: rnoliverio@axrrna.~inirornal.it e-mail: taviania boigrn2.igrn.bo.cnr.it
Renato Chemeiio Istituto d i Zoologia, Via Archirafi 9, Palermo, Italy. e-mail:
[email protected]
* Received 20.V.1996: accepted l l .XI. 1996 ** Present address: Dip. Biologia, "Roma Tre" University. V.le G. Marconi 446, 1 - 00146 Rome, Italy.
KEY WORDS: Mollusca, Castropoda, Epitonium hilleeanum, Cnidaria, Scleractinia, Tithasfraea coccinea, ecto-parasitism, ecology, first record, Red Se:i, Madagascar.
Epironium hilleeanum (DuShane & Bratcher, 1965) has been observed feeding and spawning on the scleractinian T~rhaslraeacoccinea (Ehrenberg, 1864) in the Sudanese Red Sea. This is the westernmost record for the species, and with finding at Madagascar extends its range to the entire Indo-Pacific region. Egg-mass rnorphology and embryonic, larval and adult shells are briefiy describerl. The species has a planktotrophic larval development. It belongs to a species group with very close shell morphology, possibly monophyletic, al1 associated with scleractinians belonging to the families Caryophylliidae and Ralanophylliidae.
INTRODUCTION Epitoniids are obligatory parasites/micropredators of cnidarians (Robertson, 1970). The life habits of most species are still unknown, in spite of many members being distributed in shallow waters. Severa1 Epitoniinae have been documented in association with solitary fungiid corals, in tropical coral reefs (e.g.: Bosch, 1965; Sabelli & Taviani, 1984; DuShane, 1989; Yamashiro, 1990). Other species are known to occur in association to s e a - a n e m o n e s a n d z o a n t h i d s (e.g. Fretter CL Graham, 1962; Robertson, 1963, 1981). A list of epitoniids species associated with scleractinians in some localities is reported by Bouchet & Warén (1986). We have observed the recurrent presence of an epitoniid (Fig. 1) feeding a n d s p a w n i n g o n t h e scleractinian Tubastraea coccinea (Ehrenberg, 1864) in some coral reefs of the Sudanese Red Sea during two biologica1 surveys carried out aboard the M/S Felicidad in March/April 1993 (FEL '93 cruise) and August/September 1993 (REDSED-5 cruise) respectively (Fig. 22). The same species
h a s b e e n o b s e r v e d at Madagascar (TESTREEF expedition) and Philippines. Robertson & Schutt (1984) recorded a very similar entity, t h e g o l d e n w e n t l e t r a p 'Epitonium' billeeanum ( D u S h a n e & Bratcher, 1965), a s living o n b o t h Tu bastraea and Dendrophyllia scleractinians in the Pacific Ocean. Page & Willan (1988) described in this species ontogenetic changes in radular morphology, possibly associated with sex change. We report here the ecological and morphological observations on Red Sea specimens and discuss the possible taxonomic relationships with implications on the biogeography of the species.
Epitonium billeeanum D u S h a n e & Bratcher, 1965 Scalina (Ferminoscala) billeeana DuShane CL Bratcher, 1965: 160-161, pl. 24, figs 1-4 The species has been dealt with in few works since the origina1 description. We report here the list of relevant literature (mostly after Page & Willan, 1988):
Copyright byA.M.1. (1997)- ISSN 0394 - 3399
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M. Oliverio, M. Taviani & R. Chemello
Dushane & Poorman, 1967: 424; Dushane, 1967: 87; Dushane & McLean, 1968: 1, 2, fig. 1; Robertson, 1970: 45; Keen, 1971: 424, fig. 612; MacLeish, 1973: 755; Dushane, 1974:9, 10, fi s 13, 15, 155a, 155b; Coleman, 1978: 11 ; Coleman 1981: 13, 44; Endean, 1982: 138, fig. 137; Loch, 1982: 5; Robertson & Shutt, 1984: 1 , 4; Rudman, 1984: 172.
t
MATERIAI., EXAMINED.
Red Sea: RS5.192 (Sanganeb Reef, North Point, -3/9 m depth, 9.IX.1993, M . 0 & M.T. legg.: 2 specimens); RS5.2#2 (Sanganeb Reef, South Point, -3/12 m depth, .IX.1993, M . 0 & M.T. legg.: 18 specimens); RS5.1#2 (Wingate Reef, -5/8 m depth, air-pump sample from overhangs with abundant red algae and Tubastraea l.v.1993, M.0 & M.T. legg.: 4 specimens); FEL93.6#6 (Sanganeb Reef, South East Point, -3/8 m d e p t h , 31.iii.1993, M.O. leg., 1 specimen). Madagascar: MAD95 Expedition, Nosy Vé Is., -5 m on Tubastraea (24.x.1995, M.O. & R.Villa legg., 2 specimens). Maldive Islands: Bodu Finolu, -5 m (R. Ardovini leg., 1993). Philippines Islands: Pescador Island (Cebu), -6 m o n Tubastraea (15-18.vi.1996, M.O. leg., 2 specimens).
Head-joot - The anima1 is semitransparent, yellow, with lighter yellow ('lime') minute specking on the whole body. The eyes are black. (based o n field observation under stereomicroscope of living specimens during the Red Sea cruises). Sbell (Figs 2-8) - The shell is ovate-pyramidal, fragile, translucent amber/yellowish, with brown light periostracum. Protoconch conical, multispiral, of about 3.5 whorls. T h e e m b r y o n i c shell of 0.5 whorls is smooth. The larva1 shell consists of about 2.8 whorls, with a sculpture of sigmoid axial lines, and n o spira1 threads. At the protoconch-teleoconch boundary, the sigmoid outer lip is evident. The teleoconch whorls (5-8 in the specimens studied) are convex. Suture rather d e e p , umbilical chink present. Peristome continuous, slightly expanded at the anterior end. Sculpture reticulated (sometimes described as latticelike). Axial ribs thin, spaced, low, not reflexed, straight, not spiny at the upper
end. Spira1 ribs nearly equa1 in size, resulting in a clathrate pattern, with quadrate interstices. E@-rnasses and ernbryos (Figs 9-21) - The egg capsules are less than 1 mm long, 600 pm in width, subspherical or ellipsoidal. A net of crests, ca 50 pm in height, over the whole surface of the capsule determine polygonal fields of 200-250 pm width. The capsules are yellow, semitransparent, the crests are light yellow. The eggs inside are orange-purplish, like the host coral. Al1 capsules are connected by robust, coiled threads, of ca. 20 pm diameter. Within each capsule, al1 embryos are nearly at the same developmental stage. Nevertheless, in the same capsule-mass we have observed different capsules with eggs at different developmental stage. We d o not k n o w whether they originated from different females, or from subsequent depositions by the same female. Still cleaving embryos of 50-60 pm diameter are seemingly shellfree. In other capsules, pre-hatching specimens of 150-160 pm have the smooth, 0.20.3 whorled embryonic shell already completely calcified.
The specimens herein described are certainly closely allied to the populations described as E. billeeanurn (DuShane & Bratcher, 1965) from Western Mexico and we are inclined to consider them as conspecific. Some slight differences between the Red Sea and Madagascar specimens o n the one hand, and other populations investigated by us or recorded in the literature (e.g. light yellow Vs orange colour of the animal) can be the result of intraspecific variation. E. billeeanurn was s o far known (Robertson & Schutt, 1984) from W. Mexico, Galapagos, Australia, Philippines, Maldives. The present record significantly extends its range to the entire Indo-Pacific region, including eastern Africa (Madagascar) and Red Sea. It appears strange that such a common and widespread spec i e ~remained undescribed unti1 the nineteen sixties. It is possible that it was described by s o m e of t h e old malacologists working o n the Indo-Pacific fauna (e.g. Jousseaume, 191l), and only carefu1 revision of the relative type materia1 will allow its identification. Systematics of the Epitoniidae are
Epitonium bilieeanum frorn the Red Sea
still in a state of great confusion. The sole subdivision into two families (Epitoniinae and Nystiellinae) is self-evident (Bouchet & Warén, 1986). Supraspecific groups have been based mainly o n similarity in shell characters and no reliable attempt for the reconstruction of epitoniid phylogeny is recorded in the literature. We agree with Dushane (1967) and Page & Willan (1988) that confident supraspecific placement of the present species must await a phylogenetic reconstruction of the family. A few monophyletic group of species are probably identifiable on the base of certain shell characters, but need to be tested according to a wider set of data. Epitonium billeeanum belongs to a group of species including taxa of very close shell morphology (lattice like sculpture, fragile shell), for which often the generic taxa Amaea and Scalina have been employed, but such genera refer probably to other lineages in the family. Species of this group whose ecology is known, al1 are associated to scleractinians belonging to the closely relat e d families Caryophylliidae a n d Balanophylliidae. We suspect that they belong to a monophyletic unit (genus) to which at least the following taxa pertain: E. striatissimum NE Atlantic (including the Mediterranean) and SE USA from N Carolina to Florida (rushii Dall, 1889: 313 s e e Clench & Turner, 1952: 296 pl. 136) E. d e n d r o p h y l l a e E Atlantic a n d W Mediterranean o n Dendrophyllia ramea (L., 1758), Balanophyllia cellulosa Duncan, 1878, Dendrophyllia sp. (anastomozonas sensu Monod, 1954) [Bouchet & Warén, 1986, and pers. obs.] E. bille'eanum Pacific Ocean (from W. Mexico to Philippines) and Indian Ocean (Maldives, Madagascar and Red Sea), o n Dendrophyllia and Tu bastraea. E. sp. B (INVESTIGATOR: 06'01'N 81°16'E, -60 m; BMNH) o n Balanophyllia stimpsoni (Verril, 1865) [Bouchet & Warén, 19861 ECOLOGY
E. billeeanum has been observed (see Robertson & Schutt, 1984 and Page &
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Willan, 1988) o n both Tubastraea a n d Dendrophyllia corals. I n o u r records, Epitonium sp. apparently occurs only o n Tubastraea, while al1 Dendrophyllia and Dendroph-yllia-like colonies investigated by us in the Red Sea (iii/iv and viii/ix. 1993), Madagascar (x.1995) and the Philippines (vi.1996) were not colonised by the wentletraps. Tubastraea coccinea (Ehrenberg, 1834) is a pink-red coral, normally cushion shaped, occasionally forming low bushy groups of corallites. The corallites reach 3 cm in length and up to 12 cm in width. T. coccinea is a relatively common element of semi-sciaphylic reef communities, a n d likewise most species of the genus, has strongly coloured tissues a n d is often exposed daytime (Sheppard & Sheppard, 1991). In the Red Sea it is found under overhangs and in crevices regardless of depth and we recorded its presence in the surveyed a r e a d o w n t o 45 m d e p t h (RS5.12#1: Wingate Reef, off Port Sudan, 8ix-93), but with a decise preference for shaded area in shallow waters (2-10 m depth). The same holds true for the associated epitoniid: we recorded living specimens on the corals down to 21 m depth, but the highest concentration was in the shallow waters. Most common associated organisms in this area include red algae, sponges, Tubastraea micranthus (Ehrenberg, 1834), Balanophyllia s p p . (mostly yellow species), etc. Noteworthy, it was never observed o n the yellow scleractinians sometimes situated at a very short d i s t a n c e (5-10 cm) f r o m t h e Tubastraea/Epitonium complex. Striking differences in the colour b e t w e e n the corals (pink-orange) and the epitoniids (light yellow) d o not support the hypothesis (for E. billeeanum: Robertson & Schutt, 1984) that the pigments of the snails directly originate from t h e Cnidarians. Moreover, neither the soft parts nor the egg-capsules colour (light yellow) is cryptic o n the Tubastraea, while the eggs insid e the capsules have the same colour of the corals. Epitoniids are often thought to b e associated with cnidarians for feeding aims only. Few are the records of spawning activity, though it seems likely that corals play an important role also in this aspect of their biology. Taviani & Sabelli (1984) reported E. cfr. ulu with egg masses and juveniles under Fungia paumotensis (Red Sea).
M. Oliverio, M. Taviani & R. Chemello Very few specimens of Epitonium billeeanum w e r e observed in Red Sea during Spring (March/April). In late Summer (September), a much higher density was observed, u p to hundreds of specimens scored per dive, with concentrations ranging from 2/m2 to 6/m2 (density of corallites of 30-100/m2). During the MarcWApril survey we did not record any egg-mass nor scored any clue of oviposition. It is possible that timing of oviposition is linked to the temperature of the water. A water tempera-
ture of 31 "C was measured in September vs. 25 OC measured during the MarcWApril survey. ACKNOWLEDGEMENTS
We are grateful to captain, crew and colleagues aboard M/S Felicidad during FEL93 and REDSED5 cruises. R. Robertson (NAS, Philadelphia) and H. DuShane (Whittier, California) provided valuable comments. This is BIORES contribution n.2.
Fig. 1. E. billeeanum. Sanganeb Reef, South Point, -3/12 m depth, .D(.1993. Length 7 mm. Fig. 2. E. billeeanum. Sanganeb Reef, South Point, 3/12 m depth, .M.1993. Length 7 mm. Figs 9,lO. E. billeeanum. Sanganeb Reef, South Point, 3/12 m depth, .M.1993. Egg capsules with embryos visible in transparency. Length 2 mm.
Epitonium billeeanum from the Red Sea
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Figs 3-8. E. billeeanum. Sanganeb Reef, South Point, 3 / 1 2 m depth, .IX.1993. Scale bars: 500 pn1(3), 200 pm (51, 100 pm ( 4 , 7 ) ,50 pm (6) a n d 20 pm (8).
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M. Oliverio, M. Taviani & R. Chemello
Figs 11-21. E. billeeanum. Sanganeb Reef, South Point, -3/12 m depth, .IX.1993. 11-13: egg capsules (13, particular of the surface). 14, 15: coiled wires connecting the capsules. 16-20: embryos at different developmental stages from a dissected capsule (19, pre-hatching veliger) 21: pre-hatching veliger shell. Scale bars: 500 pm (11, 12), 200 pm (16, 17), 100 pm (13151, 50 pm (19-21) and 20 Fim (18).
Epitonium billeeanum frorn the Red Sea
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Fig. 22. Geographical distribution'of E. billeeanum. Open circles: previous records. Closed circles: present records.
REFERENCES Bosch H.F., 1965. A gastropod parasite of solitary corals in Hawaii. Pacific Science, 19(2): 267-268. Bouchet P. & Warén A,, 1986. Revision of the northeast Atlantic bathyal and abyssal Aclididae, Eulimidae, Epitoniidae. Bollettino Malacologico, Suppl. 2. Coleman N., 1978. A look at the wildlve of the Great Barrier Reef Bay Books, Sydney, 128 PP Coleman N., 1981. Shells alive. Rigby, Sydney, 94 pp. DuShane H., 1967. Epitonium (Asperiscala) billeeana (DuShane & Bratcher, 1965) non Scalina billeeana DuShane & Bratcher, 1965. Veliger 10: 87-88. DuShane H., 1974. The Panamic-Galapagan Epitoniidae. Veliger lG(Supp1.): 1-84. DuShane H., 1979. The family Epitoniidae (Mollusca: Gastropoda) in the northeastern Pacific. Veliger 22: 91-134. DuShane H. & Bratcher T., 1965. A new Scalina from the Gulf of California. Veliger 8(2): 160-161. Dushane H. & McLean J.H., 1968. Three new epitoniid gastropods from the Panamic province. Contributions to Science (Los Angeles), 145: 1-6. D u s h a n e H. & P o o r m a n R., 1967. A check-list of mollusks from Guaymas, Sonora, Mexico. Veliger 9: 413-440. Endean R., 1982. Australia's Great Barrier Reef University of Queensland Press, St. Lucia, 348 pp. Guinther E., 1970. Biology of some Hawaiian Epitoniidae. In "The Biology of Mollusca" University of Hawaii, Hawaii Institute of Marine Biology Techn. Rep., 1: 10-11. Jousseaume F., 1911. Faune malacologique d e la Mer Rouge. Scalidae. Memoires de la Societè Zoologique de France, 24: 108-246. Keen A.M., 1971. Sea shells of tropical west America. Stanford University Press, Stanford, 1064 pp. Loch I., 1982. Queensland epitoniids. Austalian. Shell News 39: 3-6. MacLeish K., 1973. Exploring Australia's coral jungle. National Geographic Magazine 143: 743-778. Page A.J. & Willan R.C., 1988. Ontogenetic change in the radula of the gastropod Epitonium billeeana (Prosobranchia: Epitoniidae). Veliger 30(2): 222-229.
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R o b e r t s o n R., 1963. Wentletraps (Epitoniidae) feeding o n sea anemones a n d corals. Proceedings o the Malacological Society London, 35: 5 1-63. Robertson R., 196 American Malacological Union Reports, 1965: 6-8. Robertson R., 1970. Review of the Predators and Parasites of Stony Corals, with special references to Symbiotic Prosobranch Gastropods. Pacijìic Science, 24: 43-54. Robertson R., 1981. Epitonium rnillecostaturn and Coralliophila clathrata: two prosobranch gastropods symbiotic with Indo-Pacific Palythoa. Pacifzc Science, 34: 1-17. Robertson R. & Shutt P., 1984. Golden wentletraps o n Golden Corals. Hawaiian Shell News, 32(11): 1, 4. Rudman W.B., 1984. Molluscs. In Reader's Digest book of the Great barrier Reef. Reader's Digest, Sydney . Sabeili B. & Taviani M., 1984. Red Sea record of a Fungia-associated Epitonid [SICI. Bollettino Malacologico, 20: 91-94. S h e p p a r d C.R.C. & Sheppard A.L.S., 1991. Corals and Coral Communities of Arabia. Fauna of Saudi Arabia, 12: 1-170.
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