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Reproductive anatomy of three Mediterranean species of Coralliophilidae (Mollusca: Gastropoda: Neogastropoda)

Alexandra Richter* and A ¤ngel A. LuqueLaboratorio de Biolog| ¤a Marina, Departamento de Biolog| ¤a, Universidad Auto ¤noma de Madrid, 28049 Madrid, Spain.

*Corresponding author, e-mail: [email protected]

The functional reproductive system of three Mediterranean species of Coralliophilidae (Gastropoda:Prosobranchia), Coralliophila brevis, Coralliophila meyendor⁄i and Babelomurex cariniferus, was compared withthat of Coralliophila squamosa and three Leptoconchus species. Di¡erences chie£y in the pallial section of thefemale reproductive tract separate the Indo-Paci¢c genus Leptoconchus from the Mediterranean species, andsubdivide the latter into three di¡erent anatomical groups. Polyphyly of the genus Coralliophila is suggested.Comparison of the reproductive system of coralliophilids with that of the related Muricidae allows identi-fying characters of Coralliophila brevis, Coralliophila meyendor⁄i and Babelomurex cariniferus that are unknown inMuricidae. The comparison also reveals a closer similarity of Coralliophila squamosa with Ocenebrinae,suggesting that this species might represent a less derived evolutionary line within Coralliophilidae. Thereproductive system of some individuals of Coralliophila meyendor⁄i and Babelomurex cariniferus undergoingpenis reduction in the laboratory is also studied. It sheds some light in the ontogeny of the female pallialreproductive tract, and provides direct evidence for the existence of protandry in these species.

INTRODUCTION

The family Coralliophilidae (Gastropoda: Muricoidea)comprises about 200 marine tropical and subtropical,littoral to deep water neogastropod species that feed exclu-

sively on anthozoans. However, life style and feedinghabits vary widely. Some species are euryphagous andmobile, living ectobiotically and feeding on various ordersof anthozoans. Others are stenophagous and sessile withmodi¢ed shells and feed on a single coral order clinging¢rmly on the surface of their hosts, sometimes even beingovergrown by it. Still others live embedded within holesbored in the skeleton of their host.

The most characteristic features of the family includethe lack of jaws and radula and brood care inside thepallial cavity. Species with planktotrophic larval develop-ment also have a characteristic multispiral protoconchwith keeled whorls, axial sculpture and a well de¢ned

sinusigera. This type of protoconch is apparently wide-spread in known living species from all biogeographicareas, and can be traced back in the fossil record to theMiddle Eocene. However, paucispiral and smooth proto-conchs indicating non-planktotrophic development havealso been reported in Paci¢c species.

Present knowledge of the feeding and reproductivebiology, larval development and protoconch of corallio-philids derives from studies on a few tropical shallowwater Indo-Paci¢c and Caribbean species, and has beenreviewed by Richter & Luque (2002).

Current knowledge of the anatomy of coralliophilidsis very limited. Gross anatomy, feeding system and

reproductive system are known in three Leptoconchusspecies from the Red Sea (Gohar & Soliman, 1963). Ward(1965) described the anatomy of the digestive system of

1816) and Kantor (1995) that of two Babelomurex species.Oehlmann (1994, as Coralliophila lamellosa) studied thereproductive system of the Mediterranean speciesCoralliophila squamosa (Bivona, 1838).

The scarce information on the biology and the anatomy

of coralliophilids, the usually high intraspeci¢c shell varia-bility, the absence of radula and the fact that the proto-conch is often eroded or broken in adults and even inyoung specimens, has made the classi¢cation of thespecies di⁄cult, which is based to date only on shell andopercular characters. It has also led to a controversialsystematic placement of this group within the neogastro-pods. Kantor (1995, 1996) considers Coralliophilidae andMuricidae two independent but closely related families onthe basis of anatomical di¡erences in the feeding appa-ratus. By contrast, Ponder & Ware ¤n (1988), withoutdiscussion, and Oliverio & Mariottini (2001a), based on aphylogenetic analysis using 12S rDNA sequences, propose

ranking Coralliophilinae as a subfamily of Muricidae.Here, we treat the group as an independent family inaccordance with a recent preliminary phylogenetic studyusing characters of the reproductive strategy, larval devel-opment, gross anatomy and anatomy of the feeding andreproductive apparatus that separates Coralliophilidaeand Muricidae into two monophyletic clades (Richter &Luque, 2002).

Within the frame of a study focusing on the reproductivebiology of Mediterranean coralliophilids, the present workaddresses the anatomy of the reproductive system of Coralliophila meyendor⁄i (Calcara, 1845), Coralliophila brevis(Blainville, 1832) and Babelomurex cariniferus (G.B.

Sowerby I, 1834). Coralliophila meyendor⁄i is a fairlycommon Mediterranean infralittoral coralliophilid, whileC. brevis and B. cariniferus are uncommon infralittoral

J. Mar. Biol. Ass. U.K. (2003), 83, 1029^1045Printed in the United Kingdom



species is lacking. Knowledge of their reproductive biologyis limited to some notes on the egg-capsules, breedingbehaviour and breeding season of B. cariniferus (Spada,1968; Ghisotti & Spada, 1970), and to sexual sizedimorphism with males smaller than females and ecolo-gical variability in shell size of mature females of C. meyendor⁄i (Oliverio & Mariottini, 2001b). A study

dealing with sexual size dimorphism and sex change inC. meyendor⁄i and B. cariniferus will be published elsewhere(Richter & Luque, in press).

Characters of the functional reproductive system haverecently been used in phylogenetic analysis in Neogastro-poda (Harasewych, 1984; Kool, 1993a,b; deMaintenon,1999). The preliminary phylogenetic study mentionedabove (Richter & Luque, 2002) has also highlighted theimportance of the functional reproductive apparatus forunravelling relationships within coralliophilids andamong coralliophilids and other neogastropods. Inaddition, the anatomical study of the reproductivesystem should provide direct evidences for protandry in

coralliophilids, previously proposed on the basis of indirect evidences (penis reduction) for the Indo-Paci¢cCoralliophila neritoidea (Chen et al., 1998).

MATERIALS AND METHODSFor the anatomical study, 36 specimens of Coralliophila

meyendor⁄i , 34 of Babelomurex cariniferus and six of Coralliophila brevis were dissected. Specimens werehand collected from the sublittoral of the SpanishMediterranean by SCUBA diving. Date of collection,sampling sites, prey and number of specimens collectedfor the anatomical study are summarized inTable1.

Specimens of C. meyendor⁄i and B. cariniferus used for theanatomical study were brought alive to the laboratoryafter collection, and maintained with their natural prey

in marine aquaria for observation. Before installing them,they were measured, sexed and marked di¡erentlyaccording to their sex. If both, a well-developed curvedpenis and the absence of egg capsules were observed, thespecimen was identi¢ed as male, and if absence of a penis,presence of a reduced penis ( ¼ pseudopenis) and/orpresence of egg capsules were observed, the specimen was

identi¢ed as female. During the laboratory observation,the pallial cavity of the marked individuals was regularlyinspected to detect the presence of egg-capsules andchanges in the size of their penes. All individuals of C. brevis used for the anatomical study were ¢xed immedi-ately after collection.

Of the 36 individuals of C. meyendor⁄i dissected, 17 wereobserved breeding at least once in the laboratory or in the¢eld, 15 having a well developed penis and one having apseudopenis were never observed breeding, and threewere identi¢ed as males when collected and were ¢xed assoon as penis reduction was observed. Of the 34 indivi-duals of B. cariniferus dissected, 21 were observed breeding

at least once, and 11 having a well-developed penis andtwo reducing the penis in the laboratory were neverobserved breeding.

Specimens were relaxed in MgCl 2 isotonic withseawater, ¢xed in Bouin or 10% formaldehyde for one dayand dehydrated in an ascending series of graded ethanol.Then they were submersed in bencilbenzoate for one daymaximal, embedded in Paraplast, serially sectioned at7 ^ 10 mm and stained with standard haematoxylin andeosin or Azan. Shell length and aperture length of dissected individuals were measured with a calliper to thenearest 0.05mm, and penis and pseudopenis length weremeasured on relaxed and ¢xed specimens using a stereo-

microscope with ocular micrometer. Voucher material hasbeen deposited in the Museo Nacional de CienciasNaturales of Madrid.

1030 A. Richter and A.A. Luque Reproduction of Mediterranean Coralliophilidae

Table 1. Number of specimens in each sample, sampling localities, depth, prey and date of sample collection.

Species N Locality Depth (m) Prey Date

Coralliophila meyendor⁄i 4 Cape Gata 0 ^ 2 Actinia equina 10 ^ 19939 Cape Gata 0 ^ 2 Actinia equina 6 ^ 19941 El Calo ¤n 0 ^ 2 Actinia equina 10 ^ 19953 Escombreras ^ ^ 11 ^ 1995

12 Cape Gata 0 ^ 2 Actinia equina 6 ^ 19961 Cala Cerrada 0 ^ 2 Actinia equina 7 ^ 19961 Cala Cerrada 1 ^ 2 Anemonia sulcata 7 ^ 19961 El Playazo 1 ^ 3 Anemonia sulcata 9 ^ 19963 Los Escullos 3 ^ 4 Balanophyllia europaea 9 ^ 19961 Los Escullos 1 ^ 2 Anemonia sulcata 10 ^ 1996

Coralliophila brevis 1 Cabo de Palos ^ Eunicella sp. 7 ^ 19971 Cabo de Palos ^ Eunicella sp. 9 ^ 19981 Punta de la Mona 13 Leptogorgia squamosa 3 ^ 19941 Columbretes Island 38 ^ 10 ^ 19982 Bleda Island, Ibiza 45 ^ 6 ^ 1994

Babelomurex cariniferus 11 Punta de la Mona 10 ^ 20 Astroides calycularis 9 ^ 199310 Calahonda 10 ^ 20 Astroides calycularis 8 ^ 1994

1 Calahonda 10 ^ 20 Astroides calycularis 5 ^ 19952 Punta de la Mona 10 ^ 20 Astroides calycularis 5 ^ 1996

8 Punta de la Mona 10 ^ 20 Astroides calycularis 2 ^ 19972 Calahonda 10 ^ 20 Astroides calycularis 7 ^ 1997



proximal end, and pale orange to white colour in ¢xedspecimens. The subepithelial glandular tissue was homo-geneous, and produced a ¢ne globular secretion staining

turquoiseblue with Azan. A narrow strip of smooth epithe-lial cells running along the left lateroventral side of theprostate indicated the line of fusion of an originally opensperm groove (Figure 2C). Beyond the anus, the pallialsperm duct lost the subepithelial glandular tissue andcontinued as a shallow rib running from the £oor of themantle cavity upwards along the right £ank of the head-foot to the penis forming the cephalic sperm duct, a non-glandular closed ciliated duct (Figure 2D). The cephalicsperm duct continued along the penis as a closed eccentri-cally placed ciliated penis duct surrounded by circularmuscle ¢bres. As in the prostate, the line of fusion of anoriginally open sperm gutter was still visible as a double

sheeted epithelial strip connecting the penis duct to theepithelium lining externally the penis (Figure 2E).The penis was curved, laterally compressed and club

(Figure 1B). When relaxed, the penis was folded back-wards against the body wall, with the tip pointingupwards. The penis had a well developed external circularand internal longitudinal muscle sheet and dorsoventralmuscle ¢bres running across the blood sinus. Its externalsurface was densely folded and lined by a ciliated epithe-lium with mucous glandular cells (Figure 2F). Average

length of the penis and its papilla were 3.33 0.87mm(range: 2.15 ^ 5.24 mm; N ¼ 9) and 0.27 0.11mm (range:0.16 ^ 0.48 mm; N ¼ 9), respectively.

Female reproductive systemFemales measured between 10.50 and 28.00 mm in shell

length (average 19.70 4.46 mm; N ¼ 18). Their reproduc-tive tract consisted of an ovary, a coelomic or posterioroviduct and a closed pallial oviduct. In the latter, a prox-imal glandular region, divided into a posterior albumengland and an anterior capsule gland, and a distal nonglandular region, the vestibule and the muscular vagina,could be distinguished. The pallial oviduct was also

connected proximally through a short narrow duct to aseminal receptacle, situated between the albumen and thecapsule gland, and distally to a large muscular lateraldiverticulum, the bursa copulatrix (Figure 1C).

The ovary extended along the right side of the visceralmass from the kidney to its posterior tip, encompassing thedorsal surface of the coiled visceral mass. It was racemous,consisting of numerous branched tubules lined by a £atepithelium. Its colour and volume varied depending onthe stage of the reproductive cycle and on the actinianspecies upon which females had been feeding during thevitellogenic phase of the oogenesis. During the breedingseason, when the oocytes were ripe, the ovary occupied

from one-third to half of the visceral mass. It was intensepink if the female had been feeding on Actinia equina anddi¡ered clearly from the digestive gland, which was deepred. If the female had been feeding on Anemonia sulcata, theovary was pale yellow to golden brown in colour. In thelatter case, it could not be distinguished externally fromthe golden brown digestive gland. In the ripe ovary, theunderlying connective tissue has been completely reab-sorbed, and the lumina of the follicles were completelyinvaded by mature oocytes, ¢lled with large yolk granules.Previtellogenic oocytes were very scarce (Figure 3A). Dueto a spawning event, a few empty follicles with scatteredyolk granules appeared among ripe ones.

During the postreproductive period, the ovary waspartially reabsorbed, and encompassed only a ¢fth or lessof the total volume of the visceral mass. The colour wasgreyish green, and black waste products externally delim-ited the border of the follicles. The walls of the follicleswere collapsed, and the empty lumen contained remainsof yolk granules from degenerating oocytes and small eosi-nophilic phagocytes (Figure 3B). The ovary of prerepro-ductive females was also greyish green and of smallvolume. The eosinophilic connective tissue surroundingthe ovarian follicles was more developed than in breedingfemales, and the lumina of the follicles were narrow whencompared to those of ripe follicles. The follicles were

roundish in cross section and small groups of premeioticand previtellogenic oocytes surrounded by follicular cellswere attached on the inner wall of the follicles (Figure


Figure 2. Coralliophila meyendor⁄i. Male reproductive system.(A) Section through the visceral mass in a plane perpendicularto the coiling axis, showing the seminal vesicle and testis of areproductively active male; (B) seminiferous tubule of a repro-ductively active male; (C) transverse section through the rightpallial complex showing the prostate gland; (D) transversesection through the head-foot behind the insertion of the penis,showing the cephalic sperm duct; (E) transverse sectionthrough the penis; (F) longitudinal section of the penis close toits base. bs, blood sinus; csd, cephalic sperm duct; ct, connec-tive tissue, dg, digestive gland, epd, epithelial cells of the penisduct, eps, early growth phases of paraspermatozoa; esp,euspermatocytes; gc, glandular cells of the outer epithelium of the penis; hf, head-foot; hg, hypobranchial gland; lf, line of fusion of the sperm duct; lps, late growth phase of parasper-matozoa; msh, muscle sheet; msp, bunch of heads of matureeuspermatozoa; pd, penis duct; pg, prostate gland; r, rectum;sv, seminal vesicle; ts, testis. Scale bars: A, C ^ F, 100 mm; B,50 mm.



Reproduction of Mediterranean Coralliophilidae A. Richter and A.A. Luque 1033

Figure 3. Coralliophila meyendor⁄i. (A ^ H ) Female reproductive system. (A) Ripe ovary during the reproductive season; (B) spentovary during the postreproductive season; (C) immature ovary during the prereproductive season; (D) oblique section through thealbumen gland; (E) transverse section approximately through the middle of the capsule gland; (F) detail of the internal epitheliumof the bursa copulatrix; (G) transverse section of the pallial oviduct at the level of the vestibule; (H) detail of the ventral channel atthe level of the centre of the capsule gland. ( I ^ L ) Reproductive system of transitional females. (I) Oblique section through thevisceral mass showing kidney, digestive gland, atrophied seminal vesicle and immature ovary; (J) cross section through theposterior region of the visceral mass showing digestive gland, atrophied seminal vesicle and peripheral ovarian follicles; (K) detailof the atrophied seminal vesicle showing remains of euspermatozoa; (L) detail of the peripheral ovarian follicle showing premeioticoocytes. aag, ascending (proximal) branch of the albumen gland; bc, bursa copulatrix; cf, ciliated fold of the ventral channel; dag,descending (distal) branch of the albumen gland; dg, digestive gland; dl, dorsal lobe of the capsule gland; ds, degenerating sperminside digestive vacuole; dsr, duct of the seminal receptacle; ec, cubical epithelial cells of the atrophied seminal vesicle; es, mid-

dorsal epithelial strip of the capsule gland; fvc, £oor of the ventral channel; ki, kidney; lbc, lumen of the bursa copulatrix; mcl,main central lobe of the capsule gland; msp, heads of euspermatozoa; nec, nucleus of the epithelial cell; of, ovarian follicles; phc,phagocytes; pmo, premeiotic oocytes; pod, pallial oviduct; pvo, previtellogenic oocyte; vc, ventral channel; vs, vestibule. Scaleb A ^E G H I ^L 100 F 50



The ovarian follicles led to a straight thin walled, non-ciliated coelomic oviduct, which ran along the ventral sideof the visceral mass from the posterior to the anteriorregion. In ¢ve of eight females whose coelomic oviduct wasthoroughly studied, it was straight throughout its wholelength and whitish, while in the three remaining females itbecame slightly folded and turned reddish brown close to

the kidney. Two of the latter females had been identi¢ed asmales when collected and reduced their penis during theperiod they were kept in the marine aquaria.

The pallial section of the oviduct in all the femalesdissected, except for one, consisted of a closed duct linedat its inner surface by a columnar ciliated epithelium. Itwas surrounded externally by subepithelial glandular cellsgrouped in clusters at the level of the albumen gland andthe capsule gland. The albumen gland was an U-shapedloop with the convex side oriented dorsally. The proximalbranch of the loop was more developed than the distal one,with the base of the former bulging out and extending overthe tubular tract of the pallial oviduct.The albumen gland

produced two di¡erent types of secretion. The glandularcells of the left lateral wall secreted minute granules, andtheir cytoplasm stained very slightly with Azan, while atthe right lateral wall, they produced large secretory gran-ules, which stained deep blue after Azan (Figure 3D).Occasionally, small amounts of eusperm could be foundin the lumen of the albumen gland.

The capsule gland was more or less oval in outline andlarger than the albumen gland. It was formed by twolateral lobes, left and right, separated dorsally by a rela-tively broad longitudinal strip of a highly folded cubicalciliated epithelium (Figure 3E). At the anterior half of the capsule gland, the right lobe was deeply cleft close to

its base. Each lateral lobe was divided into four clearlyvisible secretory areas, an anterior or cephalic lobe, acentral main lobe (corresponding to the left or right lobeaccording to the terminology of Fioroni et al., 1991, andOehlmann, 1994), a dorsal lobe and a posterior or caudalone, the latter next to the seminal receptacle. Theposterior lobe was the smallest one, pale pink, greyish orbrown in ¢xed specimens, and produced a globular secre-tion, consisting of large granules that stained heavily bluewith Azan. The main central lobe was pale yellow or whitein colour and produced large secretory granules, whichcompletely ¢lled the cytoplasm and stained orange withAzan. The dorsal lobe, translucent greyish in ¢xed speci-

mens, produced very ¢ne secretory granules, and the cyto-plasm of its glandular cells stained lightly pale blue withAzan (Figure 3E). The anterior lobe of the capsule glandwas a short transitory region, where the glandular sheetbecame gradually thinner until it disappeared at the levelof the vestibule. The latter was a non-glandular, more orless tubular extension of the capsule gland leading to thevaginal opening and occupying from one-third to half of the pallial oviduct. The glandular cells of the transitoryregion produced the same type of secretion as the dorsallobe.

The seminal receptacle lay between the albumen andthe capsule gland. It was round to oval, and consisted of a

single cavity, lined by a single layer of smooth epithelialcells with vacuolized cytoplasm. It was deep brown,except for one breeding female, in which it was yellowish.

lumen of the seminal receptacle was stu¡ed witheusperm, while in the postreproductive period it was¢lled with eusperm or empty. A narrow duct, lined by acubical ciliated epithelium and crossed by a longitudinalciliated fold, led from the posterior lobe of the capsulegland to the seminal receptacle, and opened at its ventralregion. No oriented eusperm appeared attached to the

inner wall of this duct, which represented a projection of the ventral channel of the capsule gland. Whether theepithelial cells lining the seminal receptacle were able tophagocytose sperm stored within the cavity was di⁄cultto assess, because sectioning generally disrupted theepithelium of the seminal receptacle. Nevertheless, basedon the absence of phagocytic vacuoles in the luminalborder of the epithelial cells of the seminal receptacle,which on the contrary occurred in the bursa copulatrix(see below), the seminal receptacle seemed not to phagocy-tose sperm.

The bursa copulatrix was a muscular blind sac of thepallial oviduct extending ¢rst dorsal to the vestibule and

then parallel and to the left of the capsule gland. Itslumen communicated with that of the vestibule at thelevel of the vaginal ori¢ce, a single round genital porebordered by swollen lips, which opened to the pallialcavity slightly subdistally at a strongly muscular regionof the distal part of the non-glandular vestibule, thevagina. In breeding females, the bursa copulatrix washypertrophied, and bulged out under the mantle skirtowing to the large amount of stored unoriented eusperm,parasperm and loose cells embedded in an amorphousmatrix. Its function was the receipt, storage and digestionof sperm. The inner wall of the bursa copulatrix washeavily folded and lined by tall columnar glandular cells

with basal nuclei and granulated cytoplasm. At theluminal surface of the epithelial cells, the cytoplasmpresented small phagocytic vacuoles with degradingeusperm inside (Figure 3F).

Sperm coming from the bursa copulatrix wasconveyed posteriorly toward the seminal receptaclethrough the ventral channel, whose £oor was lined by asmooth epithelium. At the level of the vestibule, theventral channel ran dorsally, and was delimited by twonarrow left folds and a large dorso-median ciliated fold,with three narrow crests on its inner surface (Figure3G). At the level of the capsule gland, it ran ventrally£anked by a single curved left ciliated fold, which arose

at the junction of the £oor of the ventral channel andthe base of the left lobe of the capsule gland and wascontinuous with the dorso-median fold of the vestibule(Figure 3H). The ventral channel was connected to thelumen of the capsule gland throughout its whole length,except at its proximal end. There it submerged downinto the glandular tissue and was closed o¡ from thelumen of the posterior lobe of the capsule gland. Asmentioned before, the pallial oviduct of one femaledi¡ered from this general structure. In the smallestfemale dissected (shell length 10.50 mm), it was notcompletely developed. A deep gap separated theposterior lobe of the capsule gland from the central

main lobe. In contrast to the other females, which wereeither collected with egg-capsules or observed breedingin the laboratory, this female was not breeding when




Most functional females presented male secondarysexual characters. Sixteen out of 19 females dissectedhad a pseudopenis in the same position as the malepenis and/or traces of the male cephalic sperm duct.The pseudopenis looked like a little wart or a tiny uncini-form penis, and its tip was usually pigmented. In a singlefemale (shell length 24.50mm) it had a distal papilla,thus resembling closely a male penis. Average femalepseudopenis length was 0.47 0.18 mm (range: 0.24 ^ 0.83;

N¼

10).Typically, the foot of functional females lacked a ventralpedal gland for moulding and ¢xation of egg-capsules to

Intermediate sexual stages

Transitional maleOne of the individuals dissected that had a well-devel-

oped penis was a transitional male (shell length:14.70 mm). The posterior or coelomic gonoduct of thisindividual consisted of a mature testis and a functionalseminal vesicle ¢lled with sperm. The anterior section of the reproductive tract, by contrast, shared female and

male secondary sexual characters. In addition to a gland-ular region similar in appearance to a prostate gland, anon-glandular cephalic sperm duct and a well developed


Figure 4. (A&B ) Coralliophila meyendor⁄i. Schemes of the reproductive system of transitional females in di¡erent stages of sexchange. ( C ^ E ) Coralliophila brevis. Reproductive system. (C) Male penis; (D) pallial section of the female reproductive system; (E)female pseudopenis. ( F) Babelomurex cariniferus. Male penis. ag, albumen gland; al, anterior lobe of the capsule gland; asv, atrophiedseminal vesicle; bc, bursa copulatrix; cod, coelomic oviduct; csd, cephalic sperm duct; dl, dorsal lobe of the capsule gland; dsr, ductof seminal receptacle; isr, incipient seminal receptacle; mcl, main central lobe of the capsule gland; ov, ovary; pa, papilla; pg,

prostate gland; pl, posterior lobe of the capsule gland; pp, female pseudopenis; sr, seminal receptacle; vc, ventral channel; vo,vaginal ori¢ce; vs, vestibule. Scale bars: 0.31 mm.



4B). The penis of these individuals was smaller than themale penis (average 1.40 0.23 mm; range: 1.15 ^ 1.60 mm;N ¼ 3) and lacked a distal papilla, except for one indivi-dual of 17.40 mm in shell length, whose penis bore asmall papilla.

Coralliophila brevis

Male reproductive systemOnly the anterior section of the sperm duct of a singlel f 10 60 i h ll l h (f l d l d bi

Balearic Islands) could be examined. It followed the samebasic organization as that of Coralliophila meyendor⁄i, andconsisted of a prostate gland, a non glandular cephalicsperm duct, appearing as a narrow ridge running from the£oorof the pallial cavity tothebaseof the penis, and apenis.Whether the prostate opened or not to the pallial cavitythrough a slit placed proximally could not be determined,since the lateral lobes of the prostate gland split open along

the ventral side when the specimen was manipulated. Thepenis was curved, club-shaped, with a distal ventralpapilla (Figure 4C), and crossed by an eccentrically placedl d i d


Figure 7. Babelomurex cariniferus. Individuals in transitional sexual phases. (A) Gonad of an individual in transitional male phase;(B) gonad of an individual in transitional female phase; (C ^ E) schemes of the pallial reproductive tract of transitional females indi¡erent stages of sex change. ag, albumen gland; al, anterior lobe of the capsule gland; bc, bursa copulatrix; dg, digestive gland;dl, dorsal lobe of the capsule gland; dsr, duct of the seminal receptacle; esp, primary euspermatocytes; fc, follicular cells; icg,incipient capsule gland; isr, incipient seminal receptacle; mcl, main central lobe of the capsule gland; mf, membranous fold; mp,

muscular pouch; msp, remains of mature eusperm; opg, ori¢ce of the pallial gonoduct; pbc, posterior portion of the bursa copula-trix; phc, phagocytes; pl, posterior lobe of the capsule gland; pmo, premeiotic oocytes; pvo, previtellogenic oocytes. sr, seminalreceptacle; vc, ventral channel; vo, vaginal opening; vs, vestibule. Scale bars: A, 50 mm; B, 100 mm.



Female reproductive systemThe structure of the female reproductive system of

Coralliophila brevis was essentially like that of Coralliophilameyendor⁄i (Figure 4D).

The ovary occupied the dorsal surface of the coiled visc-eral mass, and consisted of branching tubules. The naturalcolour of a ripe ovary, observed only in one female

collected in September 1998 (Cabo de Palos, shell length:12.40 mm), was deep yellow and easily distinguishablefrom the pale pink digestive gland. The pallial section of the oviduct closely resembled that of C. meyendor⁄i. Thealbumen gland was a single U-shaped loop, with theconcave side facing downwards, and the proximal branchof the loop was more developed than the distal one, andhad a dilated base. The round seminal receptacle laybetween the albumen and the capsule gland, and wasconnected to the pallial oviduct through a narrow lateralduct. In the female collected in September 1998, theseminal receptacle was empty and its wall was translucentand very thin, while in the remaining females (shell

length: 14.00 ^ 19.95 mm) the wall of the seminal receptaclewas relatively thick, had a glandular appearance, and itscolour was purple, brown or yellow. In the latter females,except for one collected in March 1994 (shell length:14.00 mm), the seminal receptacle was stu¡ed with irides-cent eusperm.

The oval capsule gland was divided into the same secre-tory areas as in C. meyendor⁄i, and beyond the anterior lobeof the capsule gland the pallial oviduct continued as a longnon glandular vestibule, which connected anteriorly at thelevel of a slightly subdistally placed slit, the vaginalopening, with the bursa copulatrix. The latter was propor-tionally smaller than in C. meyendor⁄i, was as high as the

vestibule and a little wider and more muscular than thelatter, and ran dorsal to it. All the dissected females borea small penis behind the right ocular tentacle. In twofemales (12.40 and 19.95 mm in shell length) that alsopresented a completely developed non-glandular cephalicsperm duct running in the form of a ridge from the base of the penis to the £oor of the pallial cavity, the penis wassimilar to the male penis, slightly curved, club-shaped,with a distal ventral papilla and a closed duct (Figure 4E).

Only one of all the females studied (shell length:15.65 mm) was brooding egg-capsules when collected in June 1994 together with a male (Bleda Island, Ibiza,Balearic Islands).

As in C. meyendor⁄i, females lacked a ventral pedalgland.

Babelomurex cariniferus

Male reproductive systemOf the 11 individuals dissected that had a well-developed

penis, eight were males that measured between 21.00 and29.00 mm in shell length (average 24.93 2.93 mm; N ¼ 8).Their reproductive system followed the same basic struc-ture as that of C. meyendor⁄i, and consisted of a testis, acoelomic or posterior sperm duct, a seminal vesicle, aprostate gland, a non-glandular cephalic sperm duct anda functional penis.

During the reproductive season the seminal vesicle washypertrophied and amber coloured and the testis, whichexpanded over the dorsal surface of the coiled visceral

contrasted with the orange digestive gland. As inC. meyendor⁄i, inside the seminiferous tubules developedeusperm and parasperm simultaneously. The early stagesof the gametes were close to the walls of the follicles,while spermatids and mature sperm di¡erentiated towardthe centre of the lumen (Figure 5A). In the postrepro-ductive season, the seminal vesicle was reduced and

reddish brown and the testis was brown. The seminiferoustubules showed wide, almost empty lumina with remainsof eusperm inside and were invaded by eosinophilicphagocytes.

As in C. meyendor⁄i, the prostate extended from thebottom of the pallial cavity up to the anus, surpassing itslightly. It was surrounded by a sheet of subepithelialgland cells producing a homogeneous secretion, andopened to the pallial cavity through a small ventral slitplaced proximally. In cross section and viewed from thefrontal side, the prostate lay lateral-ventrally to therectum being separated from it by connective tissue(Figure 5B,C). Its lumen appeared as a dorsoventral slit

£anked by the left and right lateral glandular lobe. Alongthe prostate a narrow medial strip of epithelium randorsally, and lateroventrally, a band of two layers of smooth epithelial cells representing the line of fusion of the originally open sperm duct (Figure 5C). At its surfacefacing the pallial cavity, this band formed narrow ridges(crests), which were continuous with the epithelium liningthe pallial cavity (Figure 5D).

Beyond the anus, the prostate projected into a narrownon-glandular cephalic sperm duct, which led to the baseof the penis. Inside the penis the sperm duct continued as aclosed ciliated eccentrically placed penis duct that stillkept the line of fusion of an originally open sperm groove.

The penis was curved, gradually tapering toward the tip,lacked a distal papilla and measured between 2.25 and5.42 mm in length (average 3.75 1.12 mm; N ¼ 7) (Figure4F). It was muscular, with the muscle ¢bres arranged inthe same manner as in C. meyendor⁄i. It also had bloodsinuses and was coated with a ciliated epithelium bearingglandular cells, which were absent at the distal region of the penis.

Female reproductive systemFemales measured between 25.35 and 39.00 mm in shell

length (average 31.52 4.02 mm; N ¼ 22). One of them wasidenti¢ed as male when collected due to its well-developed

penis.The anatomical organization and histology of thefemale reproductive system of B. cariniferus was verysimilar to that of C. meyendor⁄i, thus it will be only brie£ydescribed, with special emphasis on the main di¡erences.

The ovary was built up by branching tubules, whichunited in a single coelomic oviduct running ventrally tothe visceral mass and parallel to the columellar muscle.The coelomic oviduct was whitish and straight throughoutmost of its length, but in most females (nine out of tenstudied) it turned dark red and was more or less heavilytwisted close to the kidney resembling an atrophiedseminal vesicle (Figure 6A).

In breeding females, the ovary occupied about one-third to half of the visceral mass, and its colour was deepred. It could be clearly distinguished from the digestive




ingested polyps of Astroides calycularis. The connective tissuewas completely reabsorbed, and the follicles were occludedby mature oocytes ¢lled with large yolk granules (Figure6B). During the postreproductive season the ovary wasdark reddish brown, the walls of the follicles werecollapsed, and eosinophilic phagocytes surrounded thefollicles and invaded their empty lumen, where remains of

degenerated yolk granules (residual bodies) from the lastspawning event were retained (Figure 6C). In prerepro-ductive females, the connective tissue surrounding thefollicles was more developed, and the lumina of the latterwere small when compared to those of ripe follicles.Groups of premeiotic and previtellogenic oocytessurrounded by small nurse cells adhered to the inner wallof the follicles (Figure 6D). In some follicles, small goldenbrown granules, representing degenerating oocytes from aprevious breeding season, could also be observed.

The pallial section of B. cariniferus showed the samebasic structure as in C. meyendor⁄i. The albumen glandwas an U-shaped loop, with the convex side oriented

dorsally and with equally developed branches, andproduced a blue globular secretion. The bilaterallysymmetrical capsule gland was also divided into aposterior lobe, a central main lobe, a reduced dorsal lobewith a medial band of cubical epithelium (Figure 6E) andan anterior lobe, each of them producing the same type of secretion as C. meyendor⁄i. The anterior lobe of the capsulegland projected also into a long non glandular vestibule,which connected anteriorly with the bursa copulatrix atthe level of the vaginal opening (Figure 6H). The latterlay in a relatively short furrow running parallel to the

vestibule and £anked by a ciliated fold (Figure 6I). Incross section the vestibule showed numerous longitudinalciliated folds (Figure 6F), which reduced in numberposteriorly until they completely disappeared. Along thedorsal wall of the vestibule ran the ventral channel, whichwas £anked by a large curved dorso-median fold withnarrow ridges and a left bilobed fold (Figure 6F).

Between these two folds ran smaller ciliated crests alongthe ventral channel that disappeared at the level of thecapsule gland. At this level, only a large left fold and oneor two reduced right folds £anking the ventral channelpersisted (Figure 6G).The ventral channel was continuouswith the lumen of the capsule gland throughout its wholelength.

The seminal receptacle, also round and with a singlecavity lined by a smooth vacuolized columnar epithelium,was situated between the posterior lobe of the capsulegland and the albumen gland. It was usually brown incolour, and ¢lled with unoriented packed eusperm. Theduct leading from the oviduct to the seminal receptacle

was covered by a cubical ciliated epithelium from whichemanated longitudinal folds. The bursa copulatrix repre-sented a large muscular lateral diverticulum of the pallialoviduct, histologically and functionally similar to that of C. meyendor⁄i, running ¢rst dorsal to the vestibule andthen parallel and to the left of the capsule gland.

As a rule, females of B. cariniferus also presented malesecondary sexual characters. Except for two females thatlacked any male secondary sexual character, theremaining 20 females of 22 dissected had a small penis orshowed at least a short tract of the cephalic sperm duct.


Table 2. Distribution of characters of the reproductive system in Coralliophilidae and Muricidae.

mgpd psd po csd pd alg cg psp bc fgo

Babelomurex cariniferus ^ with pr + nonmuscular

closed withline of fusion

+ + + long blind sacof vs

one common

Coralliophila brevis ^ with pr ? nonmuscular

closed + + + long blind sacof vs

one common

Coralliophila meyendor⁄i ^ with pr + nonmuscular



one common

Coralliophila squamosa ^ with pr + nonmuscular



one common

Leptoconchus ^ ? ^ ? closed withline of fusion

* * ^ small sacseparatedfrom pod

two independent

Ocenebrinae ^ with pr + nonmuscular


+ + +/ 7 long or smallblind sac of vs

one common

Muricinae ^ nongland-

ular

+ nonmuscular


+ + + long blind sacof vs or

continuouswith cg

one common

Rapaninae ^ with pr ^ nonmuscular

closed ductwithin duct

+ + +/ 7 continuouswith cg

one common

Trophoninae ^ with pr + muscular open/closedwithout line

of fusion

+ + ^ small blind sacof vs or

continuouswith cg

one common

alg, albumen gland; bc, bursa copulatrix; cg, capsule gland; csd, cephalic sperm duct; fgo, female genital ori¢ce; mgpd, malegonopericardial duct; pd, penis duct; po, proximal ori¢ce of the pallial sperm duct; pod, pallial oviduct; pr, prostate gland; psd, pallialsperm duct; psp, proximal sperm pouch; vs, vestibule; +, present; ^ , absent; ?, state unknown; *, pallial oviduct is glandular, but whetherdivided into albumen and capsule gland is uncertain. Own observations and data extracted from Fretter (1941), Gohar & Soliman (1963),



The female penis was between 0.12 and 0.80 mm long(average 0.51 0.25; N ¼ 10), looking like a wart or like amale penis.

As in the preceding species, females lacked a ventral

pedal gland.

Intermediate sexual stages

Transitional malesOne individual (shell length: 27.15 mm) with a well-

developed penis was a transitional male. The pallial andcephalic sperm ducts of this individual did not di¡er fromthose of functional males. The gonad was in the spentstage. The gonadic follicles showed wide empty luminainvaded by phagocytes and small groups of undi¡eren-tiated gonocytes, and small groups of previtellogenic andpremeiotic oocytes appeared attached to the inner surface

of their walls. In the lumen of some follicles remains of eusperm were observed (Figure 7A).

Transitional femalesThree individuals identi¢ed as a male when collected

and kept in the laboratory for a period of between 10 and38 months were transitional females in an advanced stageof sex change. Each of these individuals bore a developedpenis, had an ovary with immature oocytes (Figure 7B),an atrophied convoluted seminal vesicle, and a completenon-glandular cephalic sperm duct.

The pallial section of the reproductive tract runningalong the rectum, however, di¡ered markedly among

them. One individual that reduced its penis in the labora-tory and was ¢xed the following year at the end of thereproductive season (shell length: 30.00mm; aperture

that of functional females, an incipient capsule gland and ayellowish seminal receptacle ¢lled with sperm andconnected to the pallial oviduct through a duct. The inci-pient capsule gland did not show any external glandular

division and appeared externally very similar to a prostategland. It di¡ered only from the latter in that its glandulartissue was more developed than that of the prostate at theproximal region reducing in height and thickness gradu-ally toward the distal end. This transitional female alsohad two longitudinal membranous folds running alongthe ventral side of the incipient capsule gland (Figure7C). The penis of this individual looked like a wart andwas 0.45mm long.

The pallial reproductive tract of an individual (shelllength: 30.00; aperture length: 13.00 mm) that underwentpenis reduction close to onset of the reproductive seasonand was ¢xed as soon as penis reduction was detected,

was very similar to that of functional females. It di¡eredonly from that of a mature female in that the duct of theseminal receptacle was lacking, and the empty andyellowish seminal receptacle was a sac like dorsal expan-sion of the oviduct between the albumen and the capsulegland (Figure 7D). The penis of this female was relativelylong measuring 2.10 mm in length.

The pallial section of the reproductive tract of an indi-vidual that did not su¡er a visible penis reduction and was¢xed before onset of the breeding season (shell length:31.70mm; aperture height: 14.20 mm) consisted of aglandular gonoduct without an apparent external gland-ular di¡erentiation extending toward the anus, similar to

the prostate gland, but with the glandular sheet graduallythinning close to the anterior end of the duct. In theposterior end of this pallial gonoduct, an incipient


Table 3. Distribution among Mediterranean coralliophilids of characters of the reproductive system with probably systematic

Babelomurex cariniferus Coralliophila brevis Coralliophila meyendor⁄i Coralliophila squamosa

p curved and gradually tapering club shaped club shaped broad base with long flpp ^ + + ^ alg inverted U-loop with equal

branchesinverted U-loop with

unequal branchesinverted U-loop with

unequal branches?

ecr + ? ^ ?crs of pr slit like ? crescent shape ?r relative to pr dorso-laterally to pr ? at upper left corner of pr ?fgpd ^ ^ ^ +psp sr sr sr igd psp ciliated ? ciliated ?vc continuous with cg ? closed o¡ from cg

proximally?

f of vs 4 2 ? 2 ?f of vc 2; l and r ? 1; l 2; l and ravl ^ ^ ^ +vs long long long ?dl red red red ?vpg ^ ^ ^ ?

alg, albumen gland; avl, anterior-ventral lobe of the capsule gland; crs, cross section; d, duct; dl, dorsal lobe of the capsule gland; ecr,epithelial crests of the prostate; f, fold(s); fgpd, female gonopericardial duct; p, penis; pp, penis papilla; £, £agellum; ig, ingestinggland; l, left; pr, prostate gland; psp, proximal sperm pouch; r, right; red, reduced; sr, seminal receptacle; vc, ventral channel; vpg,ventral pedal gland; vs, vestibule; +, present; ^ , absent; ?, unknown. Characters absent in Muricidae jut out in pale grey; characterswith probably systematic value at generic level jut out in dark grey. Own observations and data from Oehlmann (1994).



empty and lacking the connecting duct. Parallel to the leftof this glandular pallial gonoduct ran a long blind sac, theposterior part of the functional bursa copulatrix, with alongitudinally folded internal wall and ¢lled witheusperm. The individual also had a single fold runningparallel to the posterior part of the bursa copulatrix andgiving rise anteriorly to a small muscular pouch in front of

the ori¢ce of the glandular pallial gonoduct (Figure 7E).

DISCUSSIONFunctional reproductive system

Based on characters of the reproductive system, withinCoralliophilidae two main anatomical groups might bedistinguished. These groups correspond to speciesdi¡ering in ecology and biogeographical distribution; oneis represented by the ectobiotic Mediterranean speciesCoralliophila meyendor⁄i, Coralliophila brevis, Coralliophilasquamosa and Babelomurex cariniferus, and the other by the

Indo-Paci¢c endobiotic boring species Leptoconchuscumingii, Leptoconchus globosus (¼ L. peronii) and Magilopsislamarckii, and hence by the genus Leptoconchus, sinceMassin (1982) included Magilopsis in Leptoconchus.

The reproductive system of the Mediterranean coral-liophilids follows the basic anatomical organization of the female and male neogastropod reproductive systemsoutlined in Ponder (1973, ¢gures 5 & 6; 1998, ¢gures15.155), Fretter (1984, ¢gure 1F&M) and deMaintenon(1999, ¢gures 11A&12A). In addition to this commonbasic structure, the reproductive system of theMediterranean coralliophilids shows the followingcharacteristic features: (1) complete absence of the male

gonopericardial duct; (2) a prostate gland formed by acompact sheet of subepithelial homogeneous glandulartissue; (3) a small ventral slit at the proximal region of the prostate; (4) a closed non muscular cephalic spermduct lacking glandular cells; (5) a muscular penis withan eccentrically placed closed ciliated penis duct stillretaining the line of fusion of an initially open spermgroove; (6) a bursa copulatrix arising as a long distalblind sac of the vestibule; and (7) a single femalegenital ori¢ce leading to the vestibule.

All of these traits occur simultaneously in Babelomurexcariniferus, Coralliophila meyendor⁄i (present study) and inCoralliophila squamosa (Oehlmann, 1994 as C. lamellosa)

(Table 2). In Coralliophila brevis, the ¢ne structure of thepenial sperm duct is unknown, and the absence of themale gonopericardial duct has still to be veri¢ed. Never-theless, di¡erences with the remaining Mediterraneanspecies are not expected, because in Leptoconchus the histo-logical structure of the penial duct is similar to that of theMediterranean species and the gonopericardial duct isalso absent (Gohar & Soliman, 1963). The proximalori¢ce of the prostate gland, however, has still to becon¢rmed in C. brevis, since Leptoconchus lacks it (Gohar& Soliman, 1963). Within the related Muricidae, a repro-ductive system following the basic neogastropod designand presenting this set of traits has been described in a

few Ocenebrinae. Other muricid subfamilies may presentsome of the traits indicated, but they never present all of them simultaneously and the basic design of their repro-

The reproductive system of the Indo-Paci¢c genusLeptoconchus described by Gohar & Soliman (1963) di¡ersfrom that of the former group in a few aspects. InLeptoconchus, the pallial section of the anterior sperm duct isfused throughout its whole length, and a spermpouch at theproximal region of the glandular pallial oviduct acting as aseminal receptacle or as a sperm ingesting gland is appar-

ently lacking. The genus Leptoconchus also di¡ers from theMediterranean species in the structure of the bursa copula-trix and in the shape of the penis. In Leptoconchus, the bursacopulatrix, referred to as sperm sac by Gohar & Soliman(1963), consists of a small pouch dorsal and anterior to theglandular pallial oviduct, and opens independently to thepallial cavity close from the ori¢ce of the latter. In addition,the penis is similar to that of B. cariniferus, curved, graduallytapering toward the tip, lacking a distal papilla but propor-tionally longer and slender than in the latter species. Asimilar penis is only observed in Reliquiaecava robillardi(Massin, 1987), also an Indo-Paci¢c coral-boring species. Abursa copulatrix with an independent ori¢ce to the pallial

cavity is unknown in Muricidae, while a proximal spermpouch ( ¼ sperm ingesting gland) is consistently absent inTrophoninae (Harasewych,1984; Pastorino & Harasewych,2000; but see Kool, 1993b), and sporadically inOcenebrinae and Rapaninae (Kool, 1993a). Since in thisfamily presence/absence of a sperm ingesting gland hasbeen shown to have systematic value (Harasewych, 1984),its phylogenetic implication in Coralliophilidae should bestudied.

Despite the uniformity in the basic anatomicalorganization and in the histology of certain organs, theMediterranean coralliophilids studied di¡er also incertain morphological, histological and anatomical

aspects. These aspects are: (a) the shape of the penis; (b)the shape of the albumen gland; (c) the cross section of the prostate gland; (d) the relative position of the latter tothe rectum; (e) the grade of development of the femalegonopericardial duct; (f) the grade of closure andnumber of ciliated folds of the ventral channel; (g) thenumber of folds of the vestibule; (h) the presence/absenceof an anteroventral lobe in the capsule gland; and (i) thefunction of the posterior sperm sac placed betweenthe albumen and the capsule gland (Table 3).

In Muricidae, the shape of the albumen gland and penisand the position of the prostate relative to the rectumare phylogenetically important at subfamilial level

(Harasewych, 1984; Kool, 1993a,b). The cross section of the prostate and the structure of the capsule gland andventral channel have also been considered as a goodsystematic criterion in Muricidae (Wu, 1973), but thishas still to be con¢rmed by a phylogenetic study. InCoralliophilidae, at least the shape of the penis, the gradeof development of the female gonopericardial duct, thepresence/absence of an anteroventral lobe in the capsulegland, and the function of the posterior sperm sac placedbetween the albumen and the capsule gland might havesystematic value and separate genera. Based on these char-acters Mediterranean coralliophilids can be divided intothe following anatomical groups: (A) Coralliophila squamosa;

(B) C. meyendor⁄i and C. brevis; and (C) Babelomurexcariniferus.In Coralliophila squamosa, the penis is laterally £attened,




relatively long and thin distal £agellum or pseudopapilla(Oehlmann,1994, ¢gure 28A), the female gonopericardialduct is completely developed, the posterior sperm sacfunctions as a sperm ingesting gland, and the capsulegland presents an anteroventral lobe (Fioroni et al., 1991;Oehlmann, 1994).

In Groups B and C, the capsule gland lacks an antero-

ventral lobe, the female gonopericardial duct is absent andthe posterior sperm pouch functions as a seminal recep-tacle (present study). Groups B and C di¡er from eachother in the shape of the penis. In C. meyendor⁄i andC. brevis the penis is curved, club-shaped and with aminute ventral papilla, while in B. cariniferus the penislacks a papilla, is laterally £attened, curved and graduallybut slightly tapering toward the tip. In Babelomurexnaskensis, the penis is also compressed and lacks a papilla(Kantor, 1995); whether it is curved or not was not stated.

The division of the genus Coralliophila into two markedlydi¡erent anatomical groups, A and B, that might representdi¡erent evolutionary lines is in agreement with the results

of a preliminary phylogenetic study using fragments of 12SrDNA revealing that the genus Coralliophila is polyphyletic(Oliverio & Mariottini, 2000, 2001a). The reproductivesystem of C. squamosa resembles more closely that of certain Ocenebrinae than that of any other Mediterraneancoralliophilid studied, since in some Ocenebrinae a femalegonopericardial duct, a long bursa copulatrix, a capsulegland with an anteroventral lobe and a ventral channel£anked by a left and a right fold has been reported(Fretter, 1941; Fretter & Graham, 1994; Oehlmann, 1994).Taking this into account, C. squamosa probably belongs to aless derived evolutionary line within Coralliophilidae thatshares plesiomorphic characters with Ocenebrinae. This is

also supported by a preliminary phylogenetic analysis thatsplits C. squamosa very early from the basis of a cladegrouping coralliophilids (Richter & Luque, 2002).

There are a few traits of the female reproductive systemshared at least by two of the Mediterranean coralliophilidsstudied here that deserve special attention, since thesetraits are lacking in the related family Muricidae. Thesetraits are: (i) a reduced dorsal lobe of the capsule glandwith partial substitution by a medial band of foldedcubical epithelium; (ii) a long non-glandular tubularvestibule occupying between one-third to half of thepallial oviduct; (iii) the presence of cilia and longitudinalfolds in the lateral duct leading to the seminal receptacle,

and, ¢nally, although not strictly pertaining to the repro-ductive tract; (iv) the absence of a ventral pedal gland formoulding egg-capsules. The distribution of these charac-ters among the Mediterranean coralliophilids studiedhere is represented in Table 3.

In Muricidae, the vestibule is either a relatively shortnon-glandular muscular region of the pallial oviduct infront of the capsule gland leading directly to the vaginalori¢ce (Fretter, 1941; Fretter & Graham,1994; Oehlmann,1994) or it does not exist, since the lumen of the bursacopulatrix is continuous with the lumen of the capsulegland and the ventral channel. This occurs in Rapaninae(Kool, 1988, 1993a,b) and in Trophoninae ( Xymenopsis

muriciformis; Pastorino & Harasewych, 2000). However,whether the bursa copulatrix in Rapaninae andX. muriciformis rather represents a functionally modi¢ed

a long tubular vestibule has been described in Mangelia(Turridae) (Smith, 1967), Costellariidae (Ponder, 1972 asVexillidae), Columbellidae (Marcus & Marcus, 1962b;deMaintenon, 1999) and in the fasciolariid Leucozonianassa (Marcus & Marcus,1962a).

The glandular tissue of the dorsal lobe is equally devel-oped at its central part in Muricidae (Fretter, 1941; Kool,

1988, ¢gure 4A; Gibbs et al., 1990, ¢gure 2b; Fretter &Graham, 1994; Pastorino & Harasewych, 2000, ¢gure92). Outside Coralliophilidae, a reduced dorsal lobe witha broad medial epithelial band has been reported inStrigatella paupercula (Mitridae) (Ponder, 1972).

In the only muricids where the duct leading to thesperm ingesting gland has been studied (Fretter, 1941;Kool, 1988; Fretter & Graham, 1994), it is lined by asmooth epithelium and lacks valves. OutsideCoralliophilidae, ciliated ducts leading to the seminalreceptacle or sperm ingesting glands has been describedin Costellariidae, Volutomitridae and Mitridae (Ponder,1972), Marginellidae (Ponder, 1973), in the nassariid

Nassarius vibex (deMaintenon, 2001a), in the fasciolariidLeucozonia nassa (Marcus & Marcus, 1962a) and in theconid Conus mediterraneus (Martoja-Pierson, 1958). InCostellariidae, the duct even bears longitudinal ciliatedfolds (Ponder, 1972). In the Mediterranean coralliophilids,the duct leading to the seminal receptacle seems to derivefrom the ventral channel of the pallial oviduct as indicatedby longitudinal ciliated folds emanating from its internalwall. If this is true, the lateral ducts of Nassarius vibex andcoralliophilids are not homologous. In Nassarius vibex, theduct leading to the sperm ingesting gland arises as atubular outgrowth of the dorsal lumen of the glandularpallial oviduct (deMaintenon, 2001a). Study of the onto-

geny of the lateral ducts leading to the seminal receptaclesor sperm ingesting glands in coralliophilids and otherneogastropods will reveal whether these ducts are homo-logous or might have evolved convergently from di¡erentstructures.

A ventral pedal gland used for moulding and ¢xing egg-capsules to the substratum is always present in muricids(Fretter, 1941; Harasewych, 1984; Martoja-Bouquegneu,1988; Kool, 1993a,b; Fretter & Graham, 1994; Pastorino& Harasewych, 2000). Outside Coralliophilidae andwithin Neogastropoda, the absence of a ventral pedalmoulding gland has been only reported in Costellariidaeand Volutomitridae (Ponder, 1972). Since most neogas-

tropod families have this gland, it is rather likely thatit has been lost independently in Coralliophilidae,Costellariidae and Volutomitridae.

The occurrence of these traits in other coralliophilidsespecially in Coralliophila squamosa should be determined.In a preliminary phylogenetic analysis based on anato-mical characters of the gross anatomy, reproductive andalimentary system, the reproductive strategy and larvaldevelopment, the absence of the ventral pedal gland, thereduced dorsal lobe and the long vestibule have beenrevealed as potential synapomorphies of a clade groupingLeptoconchus, Babelomurex cariniferus, Coralliophila meyendor⁄iand Coralliophila brevis (Richter & Luque, 2002). This clade

appears within the monophyletic Coralliophilidae, whichthe analysis separates from Muricidae. If the occurrence of these traits in other coralliophilids, including C. squamosa,




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Submitted 26 January 2003. Accepted 1 August 2003.




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