Sistem Reproduksi Gastropoda Pesisir

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

Alexandra Richter* and A
ngel A. Luque
Laboratorio de Biolog| a Marina, Departamento de Biolog| a, Universidad Auto noma de Madrid, 28049 Madrid, Spain.
*Corresponding author, e-mail: alexandra.richter@uam.es
The functional reproductive system of three Mediterranean species of Coralliophilidae (Gastropoda:
Prosobranchia), Coralliophila brevis, Coralliophila meyendori and Babelomurex cariniferus, was compared with
that of Coralliophila squamosa and three Leptoconchus species. Dierences chiey in the pallial section of the
female reproductive tract separate the Indo-Pacic genus Leptoconchus from the Mediterranean species, and
subdivide the latter into three dierent 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 meyendori and Babelomurex cariniferus that are unknown in
Muricidae. 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. The
reproductive system of some individuals of Coralliophila meyendori and Babelomurex cariniferus undergoing
penis reduction in the laboratory is also studied. It sheds some light in the ontogeny of the female pallial
reproductive 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 feeding
habits vary widely. Some species are euryphagous and
mobile, living ectobiotically and feeding on various orders
of anthozoans. Others are stenophagous and sessile with
modied shells and feed on a single coral order clinging
rmly on the surface of their hosts, sometimes even being
overgrown by it. Still others live embedded within holes
bored in the skeleton of their host.
The most characteristic features of the family include
the lack of jaws and radula and brood care inside the
pallial cavity. Species with planktotrophic larval develop-
ment also have a characteristic multispiral protoconch
with keeled whorls, axial sculpture and a well dened
sinusigera. This type of protoconch is apparently wide-
spread in known living species from all biogeographic
areas, and can be traced back in the fossil record to the
Middle Eocene. However, paucispiral and smooth proto-
conchs indicating non-planktotrophic development have
also been reported in Pacic species.
Present knowledge of the feeding and reproductive
biology, larval development and protoconch of corallio-
philids derives from studies on a few tropical shallow
water Indo-Pacic and Caribbean species, and has been
reviewed by Richter & Luque (2002).
Current knowledge of the anatomy of coralliophilids
is very limited. Gross anatomy, feeding system and
reproductive system are known in three Leptoconchus
species from the Red Sea (Gohar & Soliman, 1963). Ward
(1965) described the anatomy of the digestive system of
the Caribbean species Coralliophila abbreviata (Lamarck,
1816) and Kantor (1995) that of two Babelomurex species.
Oehlmann (1994, as Coralliophila lamellosa) studied the
reproductive system of the Mediterranean species
Coralliophila squamosa (Bivona, 1838).
The scarce information on the biology and the anatomy
of coralliophilids, the usually high intraspecic shell varia-
bility, the absence of radula and the fact that the proto-
conch is often eroded or broken in adults and even in
young specimens, has made the classication of the
species dicult, which is based to date only on shell and
opercular characters. It has also led to a controversial
systematic placement of this group within the neogastro-
pods. Kantor (1995, 1996) considers Coralliophilidae and
Muricidae two independent but closely related families on
the basis of anatomical dierences in the feeding appa-
ratus. By contrast, Ponder & Ware n (1988), without
discussion, and Oliverio & Mariottini (2001a), based on a
phylogenetic analysis using 12S rDNA sequences, propose
ranking Coralliophilinae as a subfamily of Muricidae.
Here, we treat the group as an independent family in
accordance with a recent preliminary phylogenetic study
using characters of the reproductive strategy, larval devel-
opment, gross anatomy and anatomy of the feeding and
reproductive apparatus that separates Coralliophilidae
and Muricidae into two monophyletic clades (Richter &
Luque, 2002).
Within the frame of a study focusing on the reproductive
biology of Mediterranean coralliophilids, the present work
addresses the anatomy of the reproductive system of
Coralliophila meyendori (Calcara, 1845), Coralliophila brevis
(Blainville, 1832) and Babelomurex cariniferus (G.B.
Sowerby I, 1834). Coralliophila meyendori is a fairly
common Mediterranean infralittoral coralliophilid, while
C. brevis and B. cariniferus are uncommon infralittoral
species. Previous information on the anatomy of these
J. Mar. Biol. Ass. U.K. (2003), 83, 1029^1045
Printed in the United Kingdom
Journal of the Marine Biological Association of the United Kingdom (2003)
species is lacking. Knowledge of their reproductive biology
is limited to some notes on the egg-capsules, breeding
behaviour and breeding season of B. cariniferus (Spada,
1968; Ghisotti & Spada, 1970), and to sexual size
dimorphism with males smaller than females and ecolo-
gical variability in shell size of mature females of
C. meyendori (Oliverio & Mariottini, 2001b). A study
dealing with sexual size dimorphism and sex change in
C. meyendori and B. cariniferus will be published elsewhere
(Richter & Luque, in press).
Characters of the functional reproductive system have
recently been used in phylogenetic analysis in Neogastro-
poda (Harasewych, 1984; Kool, 1993a,b; deMaintenon,
1999). The preliminary phylogenetic study mentioned
above (Richter & Luque, 2002) has also highlighted the
importance of the functional reproductive apparatus for
unravelling relationships within coralliophilids and
among coralliophilids and other neogastropods. In
addition, the anatomical study of the reproductive
system should provide direct evidences for protandry in
coralliophilids, previously proposed on the basis of
indirect evidences (penis reduction) for the Indo-Pacic
Coralliophila neritoidea (Chen et al., 1998).
MATERIALS AND METHODS
For the anatomical study, 36 specimens of Coralliophila
meyendori, 34 of Babelomurex cariniferus and six of
Coralliophila brevis were dissected. Specimens were
hand collected from the sublittoral of the Spanish
Mediterranean by SCUBA diving. Date of collection,
sampling sites, prey and number of specimens collected
for the anatomical study are summarized inTable 1.
Specimens of C. meyendori and B. cariniferus used for the
anatomical study were brought alive to the laboratory
after collection, and maintained with their natural prey
in marine aquaria for observation. Before installing them,
they were measured, sexed and marked dierently
according to their sex. If both, a well-developed curved
penis and the absence of egg capsules were observed, the
specimen was identied as male, and if absence of a penis,
presence of a reduced penis (pseudopenis) and/or
presence of egg capsules were observed, the specimen was
identied as female. During the laboratory observation,
the pallial cavity of the marked individuals was regularly
inspected to detect the presence of egg-capsules and
changes 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. meyendori dissected, 17 were
observed breeding at least once in the laboratory or in the
eld, 15 having a well developed penis and one having a
pseudopenis were never observed breeding, and three
were identied as males when collected and were xed as
soon 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 and
two reducing the penis in the laboratory were never
observed breeding.
Specimens were relaxed in MgCl
2
isotonic with
seawater, xed in Bouin or 10% formaldehyde for one day
and dehydrated in an ascending series of graded ethanol.
Then they were submersed in bencilbenzoate for one day
maximal, embedded in Paraplast, serially sectioned at
7^10 mm and stained with standard haematoxylin and
eosin or Azan. Shell length and aperture length of
dissected individuals were measured with a calliper to the
nearest 0.05 mm, and penis and pseudopenis length were
measured on relaxed and xed specimens using a stereo-
microscope with ocular micrometer. Voucher material has
been deposited in the Museo Nacional de Ciencias
Naturales 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 meyendori 4 Cape Gata 0^2 Actinia equina 10^1993
9 Cape Gata 0^2 Actinia equina 6^1994
1 El Calo n 0^2 Actinia equina 10^1995
3 Escombreras ^ ^ 11^1995
12 Cape Gata 0^2 Actinia equina 6^1996
1 Cala Cerrada 0^2 Actinia equina 7^1996
1 Cala Cerrada 1^2 Anemonia sulcata 7^1996
1 El Playazo 1^3 Anemonia sulcata 9^1996
3 Los Escullos 3^4 Balanophyllia europaea 9^1996
1 Los Escullos 1^2 Anemonia sulcata 10^1996
Coralliophila brevis 1 Cabo de Palos ^ Eunicella sp. 7^1997
1 Cabo de Palos ^ Eunicella sp. 9^1998
1 Punta de la Mona 13 Leptogorgia squamosa 3^1994
1 Columbretes Island 38 ^ 10^1998
2 Bleda Island, Ibiza 45 ^ 6^1994
Babelomurex cariniferus 11 Punta de la Mona 10^20 Astroides calycularis 9^1993
10 Calahonda 10^20 Astroides calycularis 8^1994
2 Punta de la Mona 10^20 Astroides calycularis 5^1996
8 Punta de la Mona 10^20 Astroides calycularis 2^1997
N, number of specimens; ^, no data.
RESULTS
Anatomy and histology of the reproductive system
Coralliophila meyendori
Male reproductive system
All of the individuals with developed penis dissected,
except for one, were males. Males measured between
10.85 and 21.00 mm in shell length (average
16.70 3.39 mm; N14). Their reproductive system was
composed of testis, a coelomic or posterior sperm duct,
an anterior sperm duct and a penis. The pallial section of
the anterior sperm duct running parallel to the rectum
formed the prostate gland, which continued beyond the
anus in a narrow non-glandular cephalic sperm duct
(cephalic vas deferens or vas deferens) leading to the
penis (Figure 1A).
All the individuals with a developed penis studied
histologically had a mature testis formed by densely
packed and branched seminiferous tubules (Figure 2A).
Inside them, typical (eupyrenic) sperm and atypical
sperm (apyrenic and oligopyrenic sperm or parasperma-
tozoa) (Figure 2B) developed. Early growth phases of the
paraspermatozoa were spherical and oligopyrenic. They
could be distinguished from the primary and secondary
spermatocytes of the growth series of the eusperm by
their wider and eosinophilic cytoplasm containing minute
strongly basophilic granules that result from the degrada-
tion of the nucleus. Later growth phases were spindle-
shaped or worm-shaped and still had few basophilic
granules. Fully developed paraspermatozoa were also
spindle or worm-shaped and had the nucleus completely
reabsorbed, since no basophilic granules could be seen.
Small and slightly eosinophilic granules also appeared in
their cytoplasm.
The seminiferous tubules joined ventrally in a straight,
thin-walled and narrow, non-ciliated coelomic sperm duct
running from the posterior end of the visceral mass to the
anterior end. Close to the kidney, the sperm duct became a
very convoluted and turgid seminal vesicle, lled with
euspermatozoa and paraspermatozoa (Figure 2A). Under
the dissecting microscope, the walls of the seminal vesicle
appeared glossy and dark red or yellowish brown in
colour. The internal surface of the seminal vesicle was
lined by highly vacuolized columnar epithelial cells.
Beneath this inner epithelium lay a at epithelium
surrounded by a thin circular muscle sheet. A short, thin
and rather straight tract from the seminal vesicle ran
below the kidney and led to the pallial section of the
sperm duct, which ran ventrally and to the right side of
the rectum. It formed the prostate gland, an almost
completely closed ciliated duct surrounded by subepithelial
glandular tissue with a small slit-like opening at the
Reproduction of Mediterranean Coralliophilidae A. Richter and A.A. Luque 1031
Figure 1. Reproductive system of Coralliophila meyendori. (A) Scheme of the complete male reproductive system; (B) penis; (C)
scheme of the complete female reproductive system. ag, albumen gland; al, anterior lobe of the capsule gland; bc, bursa copulatrix;
cod, coelomic oviduct; csd, cephalic sperm duct; dl, dorsal lobe of the capsule gland; dsr, duct of the seminal receptacle; mcl, main
central lobe of the capsule gland; ov, ovary; pa, penis papilla; pe, penis; pg, prostate gland; pl, posterior lobe of the capsule gland;
po, posterior orice of the prostate gland; pod, pallial oviduct; pp, female pseudopenis; psd, posterior sperm duct; sr, seminal
receptacle; sv, seminal vesicle; ts: testis; vc, ventral channel; vo, vaginal opening; vs, vestibule. Scale bar: 0.31 mm.
proximal end, and pale orange to white colour in xed
specimens. The subepithelial glandular tissue was homo-
geneous, and produced a ne globular secretion staining
turquoise blue with Azan. A narrowstrip of smooth epithe-
lial cells running along the left lateroventral side of the
prostate indicated the line of fusion of an originally open
sperm groove (Figure 2C). Beyond the anus, the pallial
sperm duct lost the subepithelial glandular tissue and
continued as a shallow rib running from the oor of the
mantle 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 cephalic
sperm duct continued along the penis as a closed eccentri-
cally placed ciliated penis duct surrounded by circular
muscle bres. As in the prostate, the line of fusion of an
originally open sperm gutter was still visible as a double
sheeted epithelial strip connecting the penis duct to the
epithelium lining externally the penis (Figure 2E).
The penis was curved, laterally compressed and club
shaped, with a small distal papilla at its ventral side
(Figure 1B). When relaxed, the penis was folded back-
wards against the body wall, with the tip pointing
upwards. The penis had a well developed external circular
and internal longitudinal muscle sheet and dorsoventral
muscle bres running across the blood sinus. Its external
surface 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 0.87 mm
(range: 2.15^5.24 mm; N9) and 0.27 0.11mm (range:
0.16^0.48 mm; N9), respectively.
Female reproductive system
Females measured between 10.50 and 28.00 mm in shell
length (average 19.70 4.46 mm; N18). Their reproduc-
tive tract consisted of an ovary, a coelomic or posterior
oviduct and a closed pallial oviduct. In the latter, a prox-
imal glandular region, divided into a posterior albumen
gland and an anterior capsule gland, and a distal non
glandular region, the vestibule and the muscular vagina,
could be distinguished. The pallial oviduct was also
connected proximally through a short narrow duct to a
seminal receptacle, situated between the albumen and the
capsule gland, and distally to a large muscular lateral
diverticulum, the bursa copulatrix (Figure 1C).
The ovary extended along the right side of the visceral
mass from the kidney to its posterior tip, encompassing the
dorsal surface of the coiled visceral mass. It was racemous,
consisting of numerous branched tubules lined by a at
epithelium. Its colour and volume varied depending on
the stage of the reproductive cycle and on the actinian
species upon which females had been feeding during the
vitellogenic phase of the oogenesis. During the breeding
season, when the oocytes were ripe, the ovary occupied
from one-third to half of the visceral mass. It was intense
pink if the female had been feeding on Actinia equina and
diered clearly from the digestive gland, which was deep
red. If the female had been feeding on Anemonia sulcata, the
ovary was pale yellow to golden brown in colour. In the
latter case, it could not be distinguished externally from
the golden brown digestive gland. In the ripe ovary, the
underlying connective tissue has been completely reab-
sorbed, and the lumina of the follicles were completely
invaded by mature oocytes, lled with large yolk granules.
Previtellogenic oocytes were very scarce (Figure 3A). Due
to a spawning event, a few empty follicles with scattered
yolk granules appeared among ripe ones.
During the postreproductive period, the ovary was
partially reabsorbed, and encompassed only a fth or less
of the total volume of the visceral mass. The colour was
greyish green, and black waste products externally delim-
ited the border of the follicles. The walls of the follicles
were collapsed, and the empty lumen contained remains
of yolk granules from degenerating oocytes and small eosi-
nophilic phagocytes (Figure 3B). The ovary of prerepro-
ductive females was also greyish green and of small
volume. The eosinophilic connective tissue surrounding
the ovarian follicles was more developed than in breeding
females, and the lumina of the follicles were narrow when
compared to those of ripe follicles. The follicles were
roundish in cross section and small groups of premeiotic
and previtellogenic oocytes surrounded by follicular cells
were attached on the inner wall of the follicles (Figure
3C). Some oocytes had started vitellogenesis.
Figure 2. Coralliophila meyendori. Male reproductive system.
(A) Section through the visceral mass in a plane perpendicular
to the coiling axis, showing the seminal vesicle and testis of a
reproductively active male; (B) seminiferous tubule of a repro-
ductively active male; (C) transverse section through the right
pallial complex showing the prostate gland; (D) transverse
section through the head-foot behind the insertion of the penis,
showing the cephalic sperm duct; (E) transverse section
through the penis; (F) longitudinal section of the penis close to
its base. bs, blood sinus; csd, cephalic sperm duct; ct, connec-
tive tissue, dg, digestive gland, epd, epithelial cells of the penis
duct, 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 mature
euspermatozoa; pd, penis duct; pg, prostate gland; r, rectum;
sv, seminal vesicle; ts, testis. Scale bars: A, C^F, 100 mm; B,
50 mm.
Figure 3. Coralliophila meyendori. (A^H) Female reproductive system. (A) Ripe ovary during the reproductive season; (B) spent
ovary during the postreproductive season; (C) immature ovary during the prereproductive season; (D) oblique section through the
albumen gland; (E) transverse section approximately through the middle of the capsule gland; (F) detail of the internal epithelium
of the bursa copulatrix; (G) transverse section of the pallial oviduct at the level of the vestibule; (H) detail of the ventral channel at
the level of the centre of the capsule gland. (I^L) Reproductive system of transitional females. (I) Oblique section through the
visceral mass showing kidney, digestive gland, atrophied seminal vesicle and immature ovary; ( J) cross section through the
posterior region of the visceral mass showing digestive gland, atrophied seminal vesicle and peripheral ovarian follicles; (K) detail
of the atrophied seminal vesicle showing remains of euspermatozoa; (L) detail of the peripheral ovarian follicle showing premeiotic
oocytes. 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 sperm
inside 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. Scale
bars: AÊ, G, H, I^L, 100 mm; F, 50 mm.
The ovarian follicles led to a straight thin walled, non-
ciliated coelomic oviduct, which ran along the ventral side
of the visceral mass from the posterior to the anterior
region. In ve of eight females whose coelomic oviduct was
thoroughly studied, it was straight throughout its whole
length and whitish, while in the three remaining females it
became slightly folded and turned reddish brown close to
the kidney. Two of the latter females had been identied as
males when collected and reduced their penis during the
period they were kept in the marine aquaria.
The pallial section of the oviduct in all the females
dissected, except for one, consisted of a closed duct lined
at its inner surface by a columnar ciliated epithelium. It
was surrounded externally by subepithelial glandular cells
grouped in clusters at the level of the albumen gland and
the capsule gland. The albumen gland was an U-shaped
loop with the convex side oriented dorsally. The proximal
branch of the loop was more developed than the distal one,
with the base of the former bulging out and extending over
the tubular tract of the pallial oviduct. The albumen gland
produced two dierent types of secretion. The glandular
cells of the left lateral wall secreted minute granules, and
their cytoplasm stained very slightly with Azan, while at
the right lateral wall, they produced large secretory gran-
ules, which stained deep blue after Azan (Figure 3D).
Occasionally, small amounts of eusperm could be found
in the lumen of the albumen gland.
The capsule gland was more or less oval in outline and
larger than the albumen gland. It was formed by two
lateral lobes, left and right, separated dorsally by a rela-
tively broad longitudinal strip of a highly folded cubical
ciliated 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 clearly
visible secretory areas, an anterior or cephalic lobe, a
central main lobe (corresponding to the left or right lobe
according to the terminology of Fioroni et al., 1991, and
Oehlmann, 1994), a dorsal lobe and a posterior or caudal
one, the latter next to the seminal receptacle. The
posterior lobe was the smallest one, pale pink, greyish or
brown in xed specimens, and produced a globular secre-
tion, consisting of large granules that stained heavily blue
with Azan. The main central lobe was pale yellow or white
in colour and produced large secretory granules, which
completely lled the cytoplasm and stained orange with
Azan. 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 with
Azan (Figure 3E). The anterior lobe of the capsule gland
was a short transitory region, where the glandular sheet
became gradually thinner until it disappeared at the level
of the vestibule. The latter was a non-glandular, more or
less tubular extension of the capsule gland leading to the
vaginal opening and occupying from one-third to half of
the pallial oviduct. The glandular cells of the transitory
region produced the same type of secretion as the dorsal
lobe.
The seminal receptacle lay between the albumen and
the capsule gland. It was round to oval, and consisted of a
single cavity, lined by a single layer of smooth epithelial
cells with vacuolized cytoplasm. It was deep brown,
except for one breeding female, in which it was yellowish.
During the breeding and prereproductive seasons, the
lumen of the seminal receptacle was stued with
eusperm, while in the postreproductive period it was
lled with eusperm or empty. A narrow duct, lined by a
cubical ciliated epithelium and crossed by a longitudinal
ciliated fold, led from the posterior lobe of the capsule
gland to the seminal receptacle, and opened at its ventral
region. 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 the
epithelial cells lining the seminal receptacle were able to
phagocytose sperm stored within the cavity was dicult
to assess, because sectioning generally disrupted the
epithelium of the seminal receptacle. Nevertheless, based
on the absence of phagocytic vacuoles in the luminal
border 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 the
pallial oviduct extending rst dorsal to the vestibule and
then parallel and to the left of the capsule gland. Its
lumen communicated with that of the vestibule at the
level of the vaginal orice, a single round genital pore
bordered by swollen lips, which opened to the pallial
cavity slightly subdistally at a strongly muscular region
of the distal part of the non-glandular vestibule, the
vagina. In breeding females, the bursa copulatrix was
hypertrophied, and bulged out under the mantle skirt
owing to the large amount of stored unoriented eusperm,
parasperm and loose cells embedded in an amorphous
matrix. Its function was the receipt, storage and digestion
of sperm. The inner wall of the bursa copulatrix was
heavily folded and lined by tall columnar glandular cells
with basal nuclei and granulated cytoplasm. At the
luminal surface of the epithelial cells, the cytoplasm
presented small phagocytic vacuoles with degrading
eusperm inside (Figure 3F).
Sperm coming from the bursa copulatrix was
conveyed posteriorly toward the seminal receptacle
through the ventral channel, whose oor was lined by a
smooth epithelium. At the level of the vestibule, the
ventral channel ran dorsally, and was delimited by two
narrow left folds and a large dorso-median ciliated fold,
with three narrow crests on its inner surface (Figure
3G). 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 and
the base of the left lobe of the capsule gland and was
continuous with the dorso-median fold of the vestibule
(Figure 3H). The ventral channel was connected to the
lumen of the capsule gland throughout its whole length,
except at its proximal end. There it submerged down
into the glandular tissue and was closed o from the
lumen of the posterior lobe of the capsule gland. As
mentioned before, the pallial oviduct of one female
diered from this general structure. In the smallest
female dissected (shell length 10.50 mm), it was not
completely developed. A deep gap separated the
posterior lobe of the capsule gland from the central
main lobe. In contrast to the other females, which were
either collected with egg-capsules or observed breeding
in the laboratory, this female was not breeding when
collected and xed.
Most functional females presented male secondary
sexual characters. Sixteen out of 19 females dissected
had a pseudopenis in the same position as the male
penis 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 single
female (shell length 24.50 mm) it had a distal papilla,
thus resembling closely a male penis. Average female
pseudopenis length was 0.47 0.18 mm (range: 0.24^0.83;
N10).
Typically, the foot of functional females lacked a ventral
pedal gland for moulding and xation of egg-capsules to
the substrata.
Intermediate sexual stages
Transitional male
One 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 this
individual consisted of a mature testis and a functional
seminal 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, a
non-glandular cephalic sperm duct and a well developed
penis with papilla, this transitional male had a small
Figure 4. (A&B) Coralliophila meyendori. Schemes of the reproductive system of transitional females in dierent stages of sex
change. (CÊ) 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, atrophied
seminal vesicle; bc, bursa copulatrix; cod, coelomic oviduct; csd, cephalic sperm duct; dl, dorsal lobe of the capsule gland; dsr, duct
of 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 orice; vs, vestibule. Scale bars: 0.31 mm.
sac-like empty glandular organ next to the proximal end of
the prostate gland in homologous position of the female
seminal receptacle, probably representing an early ontoge-
netic stage of the latter.
Transitional females
Three individuals that were xed during the experi-
mental study as soon as their penis reduction was detected
were transitional females (shell length: 15.65^21.20 mm)
with atrophied but still folded seminal vesicle surrounded
and invaded by phagocytes (Figure 3I^K) and immature
ovaries (Figure 3J&L). In one of them (shell length:
17.40 mm), the degenerating seminal vesicle still retained
remains of euspermatozoa (Figure 3J,K). In the two
smallest individuals (shell length: 17.40 and 15.60 mm),
the anterior section of the reproductive tract consisted of
a prostate gland, a non-glandular cephalic sperm duct
and a penis (Figure 4A). In the largest individual
(21.20 mm), the reproductive tract showed almost the
same organization. It diered from that of the preceding
individuals in that the anterior end of the glandular
pallial gonoduct or prostate developed a sac-like side
pouch without lateral duct representing an incipient
seminal receptacle, like in the transitional male (Figure
Figure 5. Babelomurex cariniferus. Male reproductive system. (A) Seminiferous tubule of a reproductively active male; (B) trans-
verse section through the pallial complex showing prostate gland; (C) cross section through the prostate gland; (D) detail of the
crests of the ventral epithelial strip running along the prostate gland. ct, connective tissue; des, dorsal epithelial strip; ecr, epithelial
crests; eps, early growth phases of paraspermatozoa; esp, euspermatocytes; hg, hypobranchial gland; lf, line of fusion; lpg, left lobe
of prostate gland; lps, late growth phases of paraspermatozoa; msp, mature euspermatoza; pc, pallial cavity; pg, prostate gland;
r, rectum; rg, rectal gland; rpg, right lobe of prostate gland; st, spermatides. Scale bars: B, C, 100 mm; A, D, 50 mm.
Figure 6. (Opposite) Babelomurex cariniferus. Female reproductive system. (A) Cross section through the coelomic oviduct close to
the kidney; (B) ripe ovary during the reproductive season; (C) spent ovary during the postreproductive season; (D) immature
ovary during the prereproductive season; (E) transversal section through the centre of the capsule gland; (F) transversal section
through the vestibule behind the vaginal opening; (G) detail of the ventral channel at the level of the centre of the capsule gland.
(H&I) Semidiagrammatic cross sections through the pallial oviduct. (H) Section at the level of the vaginal opening and at the
point where the ventral channel, vestibule and bursa copulatrix are conuent; (I) section through the vestibule at a point in front of
the vaginal opening. bc, bursa copulatrix; cf, ciliated fold of the ventral channel; cod, coelomic oviduct; cr, ciliated crest of the
vestibule; ecf, at epithelial cells of the follicular wall; dg, digestive gland; dl, dorsal lobe of the capsule gland; dmf, dorso-median
fold of the vestibule; ef, epithelial fold; es, mid-dorsal epithelial strip of the capsule gland; foc, follicular cells; fu, furrow; hg,
hypobranchial gland; ki, kidney; lcf, left ciliated fold of the ventral channel; mcl, main central lobe of the capsule gland; nu,
nucleus of mature oocyte; phc, phagocytes; pvo, previtellogenic oocyte; rb, residual bodies; r, rectum; rcf, right ciliated fold of the
ventral channel; rg, rectal gland; vc, ventral channel; vi, vitellus; vs, vestibule, vo, vaginal opening. Scale bars: 100 mm.
4B). The penis of these individuals was smaller than the
male penis (average 1.40 0.23 mm; range: 1.15^1.60 mm;
N3) and lacked a distal papilla, except for one indivi-
dual of 17.40 mm in shell length, whose penis bore a
small papilla.
Coralliophila brevis
Only the anterior section of the sperm duct of a single
male of 10.60 mm in shell length (from Bleda Island, Ibiza,
Balearic Islands) could be examined. It followed the same
basic organization as that of Coralliophila meyendori, and
consisted of a prostate gland, a non glandular cephalic
sperm duct, appearing as a narrow ridge running from the
oor of the pallial cavity tothe base of the penis, andapenis.
Whether the prostate opened or not to the pallial cavity
through 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. The
penis was curved, club-shaped, with a distal ventral
papilla (Figure 4C), and crossed by an eccentrically placed
closed penis duct.
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; (CÊ) schemes of the pallial reproductive tract of transitional females in
dierent 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, orice 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, seminal
receptacle; vc, ventral channel; vo, vaginal opening; vs, vestibule. Scale bars: A, 50 mm; B, 100 mm.
The structure of the female reproductive system of
Coralliophila brevis was essentially like that of Coralliophila
meyendori (Figure 4D).
The ovary occupied the dorsal surface of the coiled visc-
eral mass, and consisted of branching tubules. The natural
colour 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 distinguishable
from the pale pink digestive gland. The pallial section of
the oviduct closely resembled that of C. meyendori. The
albumen gland was a single U-shaped loop, with the
concave side facing downwards, and the proximal branch
of the loop was more developed than the distal one, and
had a dilated base. The round seminal receptacle lay
between the albumen and the capsule gland, and was
connected to the pallial oviduct through a narrow lateral
duct. In the female collected in September 1998, the
seminal receptacle was empty and its wall was translucent
and very thin, while in the remaining females (shell
length: 14.00^19.95 mm) the wall of the seminal receptacle
was relatively thick, had a glandular appearance, and its
colour 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 stued with irides-
cent eusperm.
The oval capsule gland was divided into the same secre-
tory areas as in C. meyendori, and beyond the anterior lobe
of the capsule gland the pallial oviduct continued as a long
non glandular vestibule, which connected anteriorly at the
level of a slightly subdistally placed slit, the vaginal
opening, with the bursa copulatrix. The latter was propor-
tionally smaller than in C. meyendori, was as high as the
vestibule and a little wider and more muscular than the
latter, and ran dorsal to it. All the dissected females bore
a small penis behind the right ocular tentacle. In two
females (12.40 and 19.95 mm in shell length) that also
presented a completely developed non-glandular cephalic
sperm duct running in the form of a ridge from the base of
the penis to the oor of the pallial cavity, the penis was
similar 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. meyendori, females lacked a ventral pedal gland.
Babelomurex cariniferus
Of the 11individuals dissected that had a well-developed
penis, eight were males that measured between 21.00 and
29.00 mm in shell length (average 24.93 2.93 mm; N8).
Their reproductive system followed the same basic struc-
ture as that of C. meyendori, and consisted of a testis, a
coelomic or posterior sperm duct, a seminal vesicle, a
prostate gland, a non-glandular cephalic sperm duct and
a functional penis.
During the reproductive season the seminal vesicle was
hypertrophied and amber coloured and the testis, which
expanded over the dorsal surface of the coiled visceral
mass, was deep red like the ovary of ripe females, and
contrasted with the orange digestive gland. As in
C. meyendori, inside the seminiferous tubules developed
eusperm and parasperm simultaneously. The early stages
of the gametes were close to the walls of the follicles,
while spermatids and mature sperm dierentiated toward
the 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 seminiferous
tubules showed wide, almost empty lumina with remains
of eusperm inside and were invaded by eosinophilic
phagocytes.
As in C. meyendori, the prostate extended from the
bottom of the pallial cavity up to the anus, surpassing it
slightly. It was surrounded by a sheet of subepithelial
gland cells producing a homogeneous secretion, and
opened to the pallial cavity through a small ventral slit
placed proximally. In cross section and viewed from the
frontal side, the prostate lay lateral-ventrally to the
rectum 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. Along
the prostate a narrow medial strip of epithelium ran
dorsally, 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 surface
facing the pallial cavity, this band formed narrow ridges
(crests), which were continuous with the epithelium lining
the pallial cavity (Figure 5D).
Beyond the anus, the prostate projected into a narrow
non-glandular cephalic sperm duct, which led to the base
of the penis. Inside the penis the sperm duct continued as a
closed ciliated eccentrically placed penis duct that still
kept 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 and
5.42 mm in length (average 3.75 1.12 mm; N7) (Figure
4F). It was muscular, with the muscle bres arranged in
the same manner as in C. meyendori. It also had blood
sinuses and was coated with a ciliated epithelium bearing
glandular cells, which were absent at the distal region of
the penis.
Females measured between 25.35 and 39.00 mm in shell
length (average 31.52 4.02 mm; N22). One of them was
identied as male when collected due to its well-developed
penis.
The anatomical organization and histology of the
female reproductive system of B. cariniferus was very
similar to that of C. meyendori, thus it will be only briey
described, with special emphasis on the main dierences.
The ovary was built up by branching tubules, which
united in a single coelomic oviduct running ventrally to
the visceral mass and parallel to the columellar muscle.
The coelomic oviduct was whitish and straight throughout
most of its length, but in most females (nine out of ten
studied) it turned dark red and was more or less heavily
twisted close to the kidney resembling an atrophied
seminal vesicle (Figure 6A).
In breeding females, the ovary occupied about one-
third to half of the visceral mass, and its colour was deep
red. It could be clearly distinguished from the digestive
gland, which was orange due to the pigment of the
ingested polyps of Astroides calycularis. The connective tissue
was completely reabsorbed, and the follicles were occluded
by mature oocytes lled with large yolk granules (Figure
6B). During the postreproductive season the ovary was
dark reddish brown, the walls of the follicles were
collapsed, and eosinophilic phagocytes surrounded the
follicles and invaded their empty lumen, where remains of
degenerated yolk granules (residual bodies) from the last
spawning event were retained (Figure 6C). In prerepro-
ductive females, the connective tissue surrounding the
follicles was more developed, and the lumina of the latter
were small when compared to those of ripe follicles.
Groups of premeiotic and previtellogenic oocytes
surrounded by small nurse cells adhered to the inner wall
of the follicles (Figure 6D). In some follicles, small golden
brown granules, representing degenerating oocytes from a
previous breeding season, could also be observed.
The pallial section of B. cariniferus showed the same
basic structure as in C. meyendori. The albumen gland
was an U-shaped loop, with the convex side oriented
dorsally and with equally developed branches, and
produced a blue globular secretion. The bilaterally
symmetrical capsule gland was also divided into a
posterior lobe, a central main lobe, a reduced dorsal lobe
with a medial band of cubical epithelium (Figure 6E) and
an anterior lobe, each of them producing the same type of
secretion as C. meyendori. The anterior lobe of the capsule
gland projected also into a long non glandular vestibule,
which connected anteriorly with the bursa copulatrix at
the level of the vaginal opening (Figure 6H). The latter
lay in a relatively short furrow running parallel to the
vestibule and anked by a ciliated fold (Figure 6I). In
cross section the vestibule showed numerous longitudinal
ciliated folds (Figure 6F), which reduced in number
posteriorly until they completely disappeared. Along the
dorsal wall of the vestibule ran the ventral channel, which
was anked by a large curved dorso-median fold with
narrow ridges and a left bilobed fold (Figure 6F).
Between these two folds ran smaller ciliated crests along
the ventral channel that disappeared at the level of the
capsule gland. At this level, only a large left fold and one
or two reduced right folds anking the ventral channel
persisted (Figure 6G). The ventral channel was continuous
with the lumen of the capsule gland throughout its whole
length.
The seminal receptacle, also round and with a single
cavity lined by a smooth vacuolized columnar epithelium,
was situated between the posterior lobe of the capsule
gland and the albumen gland. It was usually brown in
colour, and lled with unoriented packed eusperm. The
duct leading from the oviduct to the seminal receptacle
was covered by a cubical ciliated epithelium from which
emanated longitudinal folds. The bursa copulatrix repre-
sented a large muscular lateral diverticulum of the pallial
oviduct, histologically and functionally similar to that of
C. meyendori, running rst dorsal to the vestibule and
then parallel and to the left of the capsule gland.
As a rule, females of B. cariniferus also presented male
secondary sexual characters. Except for two females that
lacked any male secondary sexual character, the
remaining 20 females of 22 dissected had a small penis or
showed 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 + non
muscular
closed with
line of fusion
+ + + long blind sac
of vs
one common
Coralliophila brevis ^ with pr ? non
muscular
closed + + + long blind sac
of vs
one common
Coralliophila meyendori ^ with pr + non
muscular
closed with
line of fusion
of vs
one common
Coralliophila squamosa ^ with pr + non
muscular
closed with
line of fusion
of vs
one common
Leptoconchus ^ ? ^ ? closed with
line of fusion
* * ^ small sac
separated
from pod
two independent
Ocenebrinae ^ with pr + non
muscular
closed with
line of fusion
+ + +/7 long or small
blind sac of vs
one common
Muricinae ^ non
gland-
ular
+ non
muscular
closed with
line of fusion
of vs or
continuous
with cg
one common
Rapaninae ^ with pr ^ non
muscular
closed duct
within duct
+ + +/7 continuous
with cg
one common
Trophoninae ^ with pr + muscular open/closed
without line
of fusion
+ + ^ small blind sac
of vs or
continuous
with cg
one common
alg, albumen gland; bc, bursa copulatrix; cg, capsule gland; csd, cephalic sperm duct; fgo, female genital orice; mgpd, male
gonopericardial duct; pd, penis duct; po, proximal orice of the pallial sperm duct; pod, pallial oviduct; pr, prostate gland; psd, pallial
spermduct; psp, proximal spermpouch; vs, vestibule; +, present; ^, absent; ?, state unknown; *, pallial oviduct is glandular, but whether
divided into albumen and capsule gland is uncertain. Own observations and data extracted from Fretter (1941), Gohar & Soliman (1963),
Harasewych (1984), Kool (1988, 1993 a, b), Fretter & Graham (1994), Oehlmann (1994), and Pastorino & Harasewych (2000).
The female penis was between 0.12 and 0.80 mm long
(average 0.51 0.25; N10), looking like a wart or like a
male penis.
As in the preceding species, females lacked a ventral
pedal gland.
Intermediate sexual stages
Transitional males
One individual (shell length: 27.15 mm) with a well-
developed penis was a transitional male. The pallial and
cephalic sperm ducts of this individual did not dier from
those of functional males. The gonad was in the spent
stage. The gonadic follicles showed wide empty lumina
invaded by phagocytes and small groups of undieren-
tiated gonocytes, and small groups of previtellogenic and
premeiotic oocytes appeared attached to the inner surface
of their walls. In the lumen of some follicles remains of
eusperm were observed (Figure 7A).
Transitional females
Three individuals identied as a male when collected
and kept in the laboratory for a period of between 10 and
38 months were transitional females in an advanced stage
of sex change. Each of these individuals bore a developed
penis, had an ovary with immature oocytes (Figure 7B),
an atrophied convoluted seminal vesicle, and a complete
non-glandular cephalic sperm duct.
The pallial section of the reproductive tract running
along the rectum, however, diered markedly among
them. One individual that reduced its penis in the labora-
tory and was xed the following year at the end of the
reproductive season (shell length: 30.00 mm; aperture
height: 12.20 mm) presented an albumen gland similar to
that of functional females, an incipient capsule gland and a
yellowish seminal receptacle lled with sperm and
connected 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 prostate
gland. It diered only from the latter in that its glandular
tissue was more developed than that of the prostate at the
proximal region reducing in height and thickness gradu-
ally toward the distal end. This transitional female also
had two longitudinal membranous folds running along
the ventral side of the incipient capsule gland (Figure
7C). The penis of this individual looked like a wart and
was 0.45 mm long.
The pallial reproductive tract of an individual (shell
length: 30.00; aperture length: 13.00 mm) that underwent
penis reduction close to onset of the reproductive season
and was xed as soon as penis reduction was detected,
was very similar to that of functional females. It diered
only from that of a mature female in that the duct of the
seminal receptacle was lacking, and the empty and
yellowish seminal receptacle was a sac like dorsal expan-
sion of the oviduct between the albumen and the capsule
gland (Figure 7D). The penis of this female was relatively
long measuring 2.10 mm in length.
The pallial section of the reproductive tract of an indi-
vidual that did not suer a visible penis reduction and was
xed before onset of the breeding season (shell length:
31.70 mm; aperture height: 14.20 mm) consisted of a
glandular gonoduct without an apparent external gland-
ular dierentiation extending toward the anus, similar to
the prostate gland, but with the glandular sheet gradually
thinning close to the anterior end of the duct. In the
posterior end of this pallial gonoduct, an incipient
seminal receptacle occurred as a sac like expansion,
Table 3. Distribution among Mediterranean coralliophilids of characters of the reproductive system with probably systematic value.
Babelomurex cariniferus Coralliophila brevis Coralliophila meyendori Coralliophila squamosa
p curved and gradually tapering club shaped club shaped broad base with long fl
pp ^ + + ^
alg inverted U-loop with equal
branches
inverted U-loop with
unequal branches
inverted 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 ig
d psp ciliated ? ciliated ?
vc continuous with cg ? closed o from cg
proximally
?
f of vs 42 ? 2 ?
f of vc 2; l and r ? 1; l 2; l and r
avl ^ ^ ^ +
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, ingesting
gland; 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; characters
with 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 left
of this glandular pallial gonoduct ran a long blind sac, the
posterior part of the functional bursa copulatrix, with a
longitudinally folded internal wall and lled with
eusperm. The individual also had a single fold running
parallel to the posterior part of the bursa copulatrix and
giving rise anteriorly to a small muscular pouch in front of
the orice of the glandular pallial gonoduct (Figure 7E).
DISCUSSION
Functional reproductive system
Based on characters of the reproductive system, within
Coralliophilidae two main anatomical groups might be
distinguished. These groups correspond to species
diering in ecology and biogeographical distribution; one
is represented by the ectobiotic Mediterranean species
Coralliophila meyendori, Coralliophila brevis, Coralliophila
squamosa and Babelomurex cariniferus, and the other by the
Indo-Pacic endobiotic boring species Leptoconchus
cumingii, Leptoconchus globosus (L. peronii) and Magilopsis
lamarckii, and hence by the genus Leptoconchus, since
Massin (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 systems
outlined in Ponder (1973, gures 5 & 6; 1998, gures
15.155), Fretter (1984, gure 1F&M) and deMaintenon
(1999, gures 11A&12A). In addition to this common
basic structure, the reproductive system of the
Mediterranean coralliophilids shows the following
characteristic features: (1) complete absence of the male
gonopericardial duct; (2) a prostate gland formed by a
compact sheet of subepithelial homogeneous glandular
tissue; (3) a small ventral slit at the proximal region of
the prostate; (4) a closed non muscular cephalic sperm
duct lacking glandular cells; (5) a muscular penis with
an eccentrically placed closed ciliated penis duct still
retaining the line of fusion of an initially open sperm
groove; (6) a bursa copulatrix arising as a long distal
blind sac of the vestibule; and (7) a single female
genital orice leading to the vestibule.
All of these traits occur simultaneously in Babelomurex
cariniferus, Coralliophila meyendori (present study) and in
Coralliophila squamosa (Oehlmann, 1994 as C. lamellosa)
(Table 2). In Coralliophila brevis, the ne structure of the
penial sperm duct is unknown, and the absence of the
male gonopericardial duct has still to be veried. Never-
theless, dierences with the remaining Mediterranean
species are not expected, because in Leptoconchus the histo-
logical structure of the penial duct is similar to that of the
Mediterranean species and the gonopericardial duct is
also absent (Gohar & Soliman, 1963). The proximal
orice of the prostate gland, however, has still to be
conrmed in C. brevis, since Leptoconchus lacks it (Gohar
& Soliman, 1963). Within the related Muricidae, a repro-
ductive system following the basic neogastropod design
and presenting this set of traits has been described in a
few Ocenebrinae. Other muricid subfamilies may present
some of the traits indicated, but they never present all of
them simultaneously and the basic design of their repro-
ductive system may also vary (see Table 2).
The reproductive system of the Indo-Pacic genus
Leptoconchus described by Gohar & Soliman (1963) diers
from that of the former group in a few aspects. In
Leptoconchus, the pallial section of the anterior sperm duct is
fused throughout its whole length, and a spermpouch at the
proximal region of the glandular pallial oviduct acting as a
seminal receptacle or as a sperm ingesting gland is appar-
ently lacking. The genus Leptoconchus also diers from the
Mediterranean species in the structure of the bursa copula-
trix and in the shape of the penis. In Leptoconchus, the bursa
copulatrix, referred to as sperm sac by Gohar & Soliman
(1963), consists of a small pouch dorsal and anterior to the
glandular pallial oviduct, and opens independently to the
pallial cavity close fromthe orice of the latter. In addition,
the penis is similar to that of B. cariniferus, curved, gradually
tapering toward the tip, lacking a distal papilla but propor-
tionally longer and slender than in the latter species. A
similar penis is only observed in Reliquiaecava robillardi
(Massin, 1987), also an Indo-Pacic coral-boring species. A
bursa copulatrix with an independent orice to the pallial
cavity is unknown in Muricidae, while a proximal sperm
pouch ( sperm ingesting gland) is consistently absent in
Trophoninae (Harasewych, 1984; Pastorino &Harasewych,
2000; but see Kool, 1993b), and sporadically in
Ocenebrinae and Rapaninae (Kool, 1993a). Since in this
family presence/absence of a sperm ingesting gland has
been shown to have systematic value (Harasewych, 1984),
its phylogenetic implication in Coralliophilidae should be
studied.
Despite the uniformity in the basic anatomical
organization and in the histology of certain organs, the
Mediterranean coralliophilids studied dier also in
certain 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 to
the rectum; (e) the grade of development of the female
gonopericardial duct; (f ) the grade of closure and
number of ciliated folds of the ventral channel; (g) the
number of folds of the vestibule; (h) the presence/absence
of an anteroventral lobe in the capsule gland; and (i) the
function of the posterior sperm sac placed between
the albumen and the capsule gland (Table 3).
In Muricidae, the shape of the albumen gland and penis
and the position of the prostate relative to the rectum
are phylogenetically important at subfamilial level
(Harasewych, 1984; Kool, 1993a,b). The cross section of
the prostate and the structure of the capsule gland and
ventral channel have also been considered as a good
systematic criterion in Muricidae (Wu, 1973), but this
has still to be conrmed by a phylogenetic study. In
Coralliophilidae, at least the shape of the penis, the grade
of development of the female gonopericardial duct, the
presence/absence of an anteroventral lobe in the capsule
gland, and the function of the posterior sperm sac placed
between the albumen and the capsule gland might have
systematic value and separate genera. Based on these char-
acters Mediterranean coralliophilids can be divided into
the following anatomical groups: (A) Coralliophila squamosa;
(B) C. meyendori and C. brevis; and (C) Babelomurex
cariniferus.
In Coralliophila squamosa, the penis is laterally attened,
curved backwards, divided into a broad base and a
relatively long and thin distal agellum or pseudopapilla
(Oehlmann, 1994, gure 28A), the female gonopericardial
duct is completely developed, the posterior sperm sac
functions as a sperm ingesting gland, and the capsule
gland 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 and
the posterior sperm pouch functions as a seminal recep-
tacle (present study). Groups B and C dier from each
other in the shape of the penis. In C. meyendori and
C. brevis the penis is curved, club-shaped and with a
minute ventral papilla, while in B. cariniferus the penis
lacks a papilla, is laterally attened, curved and gradually
but slightly tapering toward the tip. In Babelomurex
naskensis, 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 markedly
dierent anatomical groups, A and B, that might represent
dierent evolutionary lines is in agreement with the results
of a preliminary phylogenetic study using fragments of 12S
rDNA revealing that the genus Coralliophila is polyphyletic
(Oliverio & Mariottini, 2000, 2001a). The reproductive
system of C. squamosa resembles more closely that of
certain Ocenebrinae than that of any other Mediterranean
coralliophilid studied, since in some Ocenebrinae a female
gonopericardial duct, a long bursa copulatrix, a capsule
gland 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 a
less derived evolutionary line within Coralliophilidae that
shares plesiomorphic characters with Ocenebrinae. This is
also supported by a preliminary phylogenetic analysis that
splits C. squamosa very early from the basis of a clade
grouping coralliophilids (Richter & Luque, 2002).
There are a few traits of the female reproductive system
shared at least by two of the Mediterranean coralliophilids
studied here that deserve special attention, since these
traits are lacking in the related family Muricidae. These
traits are: (i) a reduced dorsal lobe of the capsule gland
with partial substitution by a medial band of folded
cubical epithelium; (ii) a long non-glandular tubular
vestibule occupying between one-third to half of the
pallial oviduct; (iii) the presence of cilia and longitudinal
folds 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 for
moulding egg-capsules. The distribution of these charac-
ters among the Mediterranean coralliophilids studied
here is represented inTable 3.
In Muricidae, the vestibule is either a relatively short
non-glandular muscular region of the pallial oviduct in
front of the capsule gland leading directly to the vaginal
orice (Fretter, 1941; Fretter & Graham, 1994; Oehlmann,
1994) or it does not exist, since the lumen of the bursa
copulatrix is continuous with the lumen of the capsule
gland 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 and
X. muriciformis rather represents a functionally modied
vestibule should be determined. Outside Coralliophilidae,
a long tubular vestibule has been described in Mangelia
(Turridae) (Smith, 1967), Costellariidae (Ponder, 1972 as
Vexillidae), Columbellidae (Marcus & Marcus, 1962b;
deMaintenon, 1999) and in the fasciolariid Leucozonia
nassa (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, gure
92). Outside Coralliophilidae, a reduced dorsal lobe with
a broad medial epithelial band has been reported in
Strigatella paupercula (Mitridae) (Ponder, 1972).
In the only muricids where the duct leading to the
sperm ingesting gland has been studied (Fretter, 1941;
Kool, 1988; Fretter & Graham, 1994), it is lined by a
smooth epithelium and lacks valves. Outside
Coralliophilidae, ciliated ducts leading to the seminal
receptacle or sperm ingesting glands has been described
in Costellariidae, Volutomitridae and Mitridae (Ponder,
1972), Marginellidae (Ponder, 1973), in the nassariid
Nassarius vibex (deMaintenon, 2001a), in the fasciolariid
Leucozonia nassa (Marcus & Marcus, 1962a) and in the
conid Conus mediterraneus (Martoja-Pierson, 1958). In
Costellariidae, the duct even bears longitudinal ciliated
folds (Ponder, 1972). In the Mediterranean coralliophilids,
the duct leading to the seminal receptacle seems to derive
from the ventral channel of the pallial oviduct as indicated
by longitudinal ciliated folds emanating from its internal
wall. If this is true, the lateral ducts of Nassarius vibex and
coralliophilids are not homologous. In Nassarius vibex, the
duct leading to the sperm ingesting gland arises as a
tubular outgrowth of the dorsal lumen of the glandular
pallial oviduct (deMaintenon, 2001a). Study of the onto-
geny of the lateral ducts leading to the seminal receptacles
or sperm ingesting glands in coralliophilids and other
neogastropods will reveal whether these ducts are homo-
logous or might have evolved convergently from dierent
structures.
Aventral 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 and
within Neogastropoda, the absence of a ventral pedal
moulding gland has been only reported in Costellariidae
and Volutomitridae (Ponder, 1972). Since most neogas-
tropod families have this gland, it is rather likely that
it has been lost independently in Coralliophilidae,
Costellariidae and Volutomitridae.
The occurrence of these traits in other coralliophilids
especially in Coralliophila squamosa should be determined.
In a preliminary phylogenetic analysis based on anato-
mical characters of the gross anatomy, reproductive and
alimentary system, the reproductive strategy and larval
development, the absence of the ventral pedal gland, the
reduced dorsal lobe and the long vestibule have been
revealed as potential synapomorphies of a clade grouping
Leptoconchus, Babelomurex cariniferus, Coralliophila meyendori
and Coralliophila brevis (Richter & Luque, 2002). This clade
appears within the monophyletic Coralliophilidae, which
the analysis separates from Muricidae. If the occurrence of
these traits in other coralliophilids, including C. squamosa,
is demonstrated these traits should be considered as
synapomorphies for the whole Coralliophilidae (Richter
& Luque, 2002).
Reproductive system of transitional sexual stages
The transitional sexual stages observed in C. meyendori
and B. cariniferus provide direct anatomical evidences for
the existence of protandry in these species. The pseudo-
penes observed in the functional females should therefore
be interpreted as the remains of a male penis, and not as a
consequence of imposex, a recently described and rela-
tively common phenomenon in marine neogastropods
caused by tributyltin (TBT) pollution of seawater (Gibbs
et al., 1987, 1990; Fioroni et al., 1991; Oehlmann, 1994;
Kohn et al., 1999; deMaintenon, 2001b).
Pseudopenes occur also in functional females of C. brevis
(present study), C. squamosa (Oehlmann, 1994), C. abbreviata
(Fioroni et al., 1991), C. neritoidea (Soong & Chen, 1991;
Lin & Liu, 1995; Lalli et al., 1997), C. radula and
C. costularis (Lalli et al., 1997). In C. neritoidea, protandry
was demonstrated by direct observation of penis reduction
of experimentally controlled individuals (Chen et al.,
1998). Anatomical evidences, however, were not provided.
Lalli et al. (1997), studied the gonads of C. neritoidea and
C. costularis, and did not nd evidences for sex change.
However, sample size was too small to be conclusive and
individuals were collected during the breeding season.
Anatomical study of the reproductive system of individuals
dissected during the resting period may provide evidence
for sex change in other coralliophilids.
The transitional sexual stages of C. meyendori and B.
cariniferus clarify the ontogeny of dierent accessory
organs of the female reproductive system, like the bursa
copulatrix and the vestibule. Knowledge of the ontogeny
of these organs may be useful for resolving phylogenies,
because it helps to identify their dierent anatomical
components and permits establishing homologies among
the accessory organs of dierent species.
In the Mediterranean coralliophilids, the vestibule
appears to originate during sex change from male to
female as a result of the resorption of the glandular tissue
surrounding the distal region of the pallial gonoduct. This
is supported by the fact that in earlier ontogenetic stages of
both species, in males and transitional sexual stages, the
pallial gonoduct is glandular throughout its entire length.
A dierent origin is not expected in C. brevis. In other non-
coralliophilid taxa, the vestibule may develop in a similar
manner during ontogeny through secondary loss of the
subepithelial glandular tissue of the distal pallial gonoduct
(capsule gland if the species is dioecious). Alternatively, it
might represent a distal region of the pallial gonoduct that
never develops subepithelial glandular tissue during onto-
geny thus retaining phylogenetically primitive traits.
The bursa copulatrix of Mediterranean coralliophilids
seems to originate from two dierent components. A tran-
sitional female of B. cariniferus in an advanced stage of sex
change develops a small muscular pouch placed in front of
the anterior end of the pallial gonoduct and a long blind
sac parallel to the oviduct. A transitional female in an
earlier stage of sex change lacks this muscular pouch and
the blind sac, and presents two membranous folds running
parallel to the glandular gonoduct. The two membranous
folds, presumably by fusing ventrally throughout their
length, might form the posterior part of the functional
bursa copulatrix that runs backwards along the vestibule
starting at the vaginal opening. The small muscular
pouch, presumably homologous to the anterior sperm sac
observed in mature females of Leptoconchus (Gohar &
Soliman, 1963) and the smooth walled sac next to the
vaginal opening of immature females of Nassarius vibex
(deMaintenon, 2001a), might represent an early ontoge-
netic stage of the anterior part of the functional bursa
copulatrix in front of the vaginal opening. The denitive
bursa copulatrix might develop by fusion of these two
components at the point where, in functional females, the
vestibule, ventral channel and bursa copulatrix connect.
In other neogastropods, a long bursa copulatrix arising
as a blind sac of the vestibule might develop in a similar
manner. In Leptoconchus, presumably the component
forming the posterior part of the bursa copulatrix is
lacking.
This study was supported by a research grant to the rst
author from the Direccio n General de Investigacio n Cient| ca y
Te cnica and by funds of the projects Fauna Ibe rica I-V (DGI-
CYT PB-92-0121). We are indebted to Marco Oliverio and Jose
Templado for their kindly supply of coralliophilid specimens,
and to A
ngeles Juarranz for her help in histology. We also

acknowledge Alan Kohn for his useful comments and suggestions
on the manuscript, and Agust| n Barrajo n for his help in sam-
pling.
REFERENCES
Chen, M.-H., Yang, Y.-W. & Soong, K., 1998. Preliminary obser-
vations on change of sex by the coral inhabiting snail
Coralliophila violacea (Lamarck) (Gastropoda: Corallio-
philidae). Journal of Experimental Marine Biology and Ecology, 230,
207^212.
deMaintenon, M.J., 1999. Phylogenetic analysis of the
Columbellidae (Mollusca: Neogastropoda) and the evolution
of herbivory from carnivory. Invertebrate Biology, 118, 258^288.
deMaintenon, M.J., 2001a. Analysis of reproductive system onto-
geny and homology in Nassarius vibex (Gastropoda:
Buccinidae: Nassariinae). Journal of Molluscan Studies, 67, 37^50.
deMaintenon, M.J., 2001b. Ontogeny of the pseudohermafroditic
reproductive system in Nassarius vibex (Gastropoda:
Buccinidae: Nassariinae). Journal of Molluscan Studies, 67, 51^58.
Fioroni, P., Oehlmann, J. & Stroben, E., 1991. The pseudoher-
maphroditism of prosobranchs: morphological aspects.
Zoologischer Anzeiger, 226, 1^26.
Fretter, V., 1941. The genital ducts of some British stenoglossan
prosobranchs. Journal of the Marine Biological Association of the
United Kingdom, 25, 173^211.
Fretter, V., 1984. Prosobranchs. InThe Mollusca. Vol. 7. Reproduction
(ed. A.S. Tompa et al.), pp. 1^47. London: Academic Press.
Fretter, V. & Graham, A., 1994. British prosobranch molluscs. Their
functional anatomy and ecology. London: The Ray Society.
Ghisotti, F. & Spada, G., 1970. Latiaxis (Babelomurex) babelis
(Re quien 1848). Schede Malacologiche del Mediterraneo 21Bc01,
pp. 1^6.
Gibbs, P.E., Bryan, G.W., Pascoe, P.L. & Burt, G.R., 1987. The
use of the dog-whelk, Nucella lapillus, as an indicator of tribu-
tyltin (TBT) from antifouling paints. Journal of the Marine
Biological Association of the United Kingdom, 67, 507^523.
Gibbs P.E., Bryan, G.W., Pascoe, P.L. & Burt, G.R., 1990.
Reproductive abnormalities in female Ocenebra erinacea
(Gastropoda) resulting from tributyltin-induced imposex.
Journal of the Marine Biological Association of the United Kingdom,
70, 639^656.
Gohar, H.A.F. & Soliman, G.N., 1963. On the biology of three
coralliophilids boring in living corals. Publications of the Marine
Biological Station, Al Ghardaqa, Red Sea, 12, 99^126.
Harasewych, M.G., 1984. Comparative anatomy of four primi-
tive muricacean gastropods: implications of Trophonine
phylogeny. American Malacological Bulletin, 3, 11^26.
Kantor, Y.I., 1995. On the morphology of the digestive system of
Latiaxis (Babelomurex) (Gastropoda, Coralliophilidae) with
notes on the phylogeny of the family. Ruthenica, 5, 9^15.
Kantor, Y.I., 1996. Phylogeny and relationships of
Neogastropoda. In Origin and evolutionary radiation of the
Mollusca (ed. J.D. Taylor), pp. 221^230. Oxford: Oxford
University Press.
Kohn, A., Lalli, C.M. & Wells, F.E., 1999. Imposex in Conus at
Rottnest Island, Western Australia: ve years after the rst
report. In The seagrass ora and fauna of Rottnest Island, Western
Australia (ed. D.I. Walker and F.E. Wells), pp. 199^209. Perth:
Western Australian Museum.
Kool, S.P., 1988. Aspects of the anatomy of Plicopurpura patula
(Prosobranchia: Muricoidea: Thaidinae), new combination,
with emphasis on the reproductive system. Malacologia, 29,
373^382.
Kool, S.P., 1993a. The systematic position of the genus Nucella
(Prosobranchia: Muricidae: Ocenebrinae). The Nautilus, 107,
47^57.
Kool, S.P., 1993b. Phylogenetic analysis of the Rapaninae
(Neogastropoda: Muricidae). Malacologia, 35, 155^259.
Lalli, C.M., Wells, F.E., Poolsanguan, W. & Thongkukiatkul, A.,
1997. Population structure and reproduction in three species of
Coralliophila (Mollusca: Gastropoda) from the Houtman
Abrolhos Islands, Western Australia. In The marine ora and
fauna of the Houtman Abrolhos Islands, Western Australia (ed. F.E.
Wells), pp. 141^158. Perth: Western Australian Museum.
Lin, T.Y. & Liu, P.J., 1995. Fecundity of female coral-inhabiting
snails, Coralliophila violacea (Gastropoda: Coralliophilidae). The
Veliger, 38, 319^322.
Marcus, E. & Marcus, E., 1962a. On Leucozonia nassa. Boletim
Faculdade de Filosoa, Ciencias e Letras Universidade Sao Paulo, 261,
Zoologia, 24, 11^30.
Marcus, E. & Marcus, E., 1962b. Studies on Collumbellidae.
Boletim Faculdade de Filosoa, Ciencias e Letras Universidade Sao
Paulo, 261, Zoologia, 24, 335^402.
Martoja, M. & Bouquegneu, J.M., 1988. Murex trunculus: un
nouveau cas de pseudo-hermaphroditisme chez un gastropode
prosobranche. Bulletin de la Societe Royal de Lie'ge, 57, 45^58.
Martoja-Pierson, M., 1958. Anatomie et histologie de lappareil
ge nital de Conus mediterraneus Brug. Bulletin de Biologie, 2,
183^204.
Massin, C., 1982. Contribution to the knowledge of two boring
gastropods with annotated list of the genera Magilus
Montfort, 1810 and Leptoconchus Rppell, 1835. Bulletin de
lInstitut Royal de Sciences Naturelles de Belgique, 53, 1^29.
Massin, C., 1987. Reliquiaecava, a new genus of Coralliophilidae
(Mollusca, Gastropoda). Bulletin de lInstitut Royal de Sciences
Naturells de Belgique, 57, 79^90.
Oehlmann, J., 1994. Imposex bei Muriciden (Gastropoda,
Prosobranchia), eine kotoxikologische Untersuchung zu TBT-Eekten.
Gttingen: Cuvillier-Verlag.
Oliverio, M. & Mariottini, P., 2000. Sistematica dei Muricoidi
correlativa a Coralliophila: dati moleculari nucleari e mitocon-
driali. Abstracts I Congresso Congiunto delle Societa' Malacologiche del
Mediterraneo, 12^16 Novembre 2000, Genova.
Oliverio, M. & Mariottini, P., 2001a. A molecular framework for
the phylogeny of Coralliophila and related muricoids. Journal of
Molluscan Studies, 67, 215^224.
Oliverio, M. & Mariottini, P., 2001b. Contrasting morphological
and molecular variation in Coralliophila meyendor (Muricidae,
Coralliophilinae). Journal of Molluscan Studies, 67, 243^246.
Pastorino, G. & Harasewych, M.G., 2000. A revision of the
Patagonian genus Xymenopsis Powell, 1951 (Gastropoda:
Muricidae). The Nautilus, 114, 38^58.
Ponder, W.F., 1972. The morphology of some mitriform gastro-
pods with special reference to their alimentary and
reproductive systems (Mollusca: Neogastropoda). Malacologia,
11, 295^342.
Ponder, W.F., 1973. The origin and evolution of the
Neogastropoda. Malacologia, 12, 295^338.
Ponder, W.F. & Ware n, A., 1988. Appendix. Classication of the
Caenogastropoda and Heterostrophaa list of the family-
group names and higher taxa. Malacological Review, 4,
Supplement, 288^326.
Richter, A. & Luque, A
.A., 2002. Current knowledge on

Coralliophilidae (Gastropoda) and phylogenetic implication
of anatomical and reproductive characters. Bolletino
Malacologico, 38, 5^19.
Richter, A. & Luque, A
.A., in press. Sex change in two

Mediterranean species of Coralliophilidae (Mollusca:
Gastropoda: Neogastropoda). Journal of the Marine Biological
Association of the United Kingdom.
Sabelli, G. & Spada, B., 1980. Guida illustrata allidenticazione
delle conchiglie del Mediterraneo. Fam. Coralliophilidae.
Bollettino Malacologico. Milano, 16, Supplement, 1^3.
Smith, E.H., 1967. The reproductive system of British Turridae
(Gastropoda: Toxoglossa). The Veliger, 10, 176^187.
Soong, K. & Chen, J.L., 1991. Population structure and sex-
change in the coral-inhabiting snail Coralliophila violacea at
Hsiao-Liuchiu, Taiwan. Marine Biology, 111, 81^86.
Spada, G., 1968. Osservazioni sullhabitat della Coralliophila
(Babelomurex) babelis Re quien, 1848. Conchiglie, 4, 170^176.
Ward, J., 1965. The digestive tract and its relation to feeding
habits in the stenoglossan prosobranch Coralliophila abbreviata
(Lamarck). CanadianJournal of Zoology, 43, 447^464.
Wu, S.K., 1973. Comparative studies on the digestive and repro-
ductive systems of some muricid gastropods. Bulletin of the
American Malacological Union, 18.
Submitted 26 January 2003. Accepted 1 August 2003.
Reproducedwith permission of thecopyright owner. Further reproductionprohibited without permission.

Sistem Reproduksi Gastropoda Pesisir

Enviado por

Dados do documento

Título original

Direitos autorais

Formatos disponíveis

Compartilhar este documento

Compartilhar ou incorporar documento

Opções de compartilhamento

Você considera este documento útil?

Este conteúdo é inapropriado?

Direitos autorais:

Formatos disponíveis

Sistem Reproduksi Gastropoda Pesisir

Enviado por

Direitos autorais:

Formatos disponíveis

Reproductive anatomy of three Mediterranean species of

Coralliophilidae (Mollusca: Gastropoda: Neogastropoda)

ngeles Juarranz for her help in histology. We also

.A., 2002. Current knowledge on

.A., in press. Sex change in two

Você também pode gostar