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HARVARD UNIVERSITY

Ernst Mayr Library

of the Museum of

Comparative Zoology

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ADDITIONAL FINDINGS ON THE MORPHOLOGY

OF THE PROXIMAL PART OF THE REPRODUCTIVE SYSTEM

OF THE STYLOMMATOPHORA (GASTROPODA, PULMONATA)

by

L. V. Schileyko and A. A. Schileyko

in

Scientific Reports of the Higher Educational School
of Biological Sciences
1975, No. 1, pp. 7-13, Figs. 1-3

[K morfologii proksimal 'nogo otdela
polovogo apparata Stylommatophora (Gastropoda, Pulmonata)
Nauchnye Doklady Vysshei Shkoly Biologicheskie Nauki
1975, No. 1, pp. 7-13, Figs. 1-3]

Translated by Marian Taube

and

Edited with nomenclatural changes by Kenneth C. Emberton

Department of Malacology

Academy of Natural Sciences

1900 Benjamin Franklin Parkway

Philadelphia, PA 19103-1195

Special Occasional Publication

No. 9

published by the

Department of Mollusks

Museum of Comparative Zoology

Harvard University

Cambridge, Massachusetts 02138

1992

ADDITIONAL FINDINGS ON THE MORPHOLOGY

OF THE PROXIMAL PART OF THE REPRODUCTIVE SYSTEM

OF THE STYLOMMATOPHORA (GASTROPODA, PULMONATA)

by

L. V. Schileyko and A. A. Schileyko

ABSTRACT
The external, internal, and histological structure of the
fertilization-pouch-seminal-receptacle complex (FPSC) was
studied. Great structural variation was found in the FPSC, both
in the form and size of the chambers, and in the presence of
spermathecal pouches and the fertilization chamber. It is very
probable that, upon studying a greater number of specimens, it
will be possible to use the characters of the FPSC for systematic
purposes. It was shown that oogenesis usually occurs in the time
period from April to July; beginning in August, spermatogenesis
prevails.

INTRODUCTION
The details of the structure of the reproductive system of
many representatives of pulmonate land mollusks (Stylommatophora)
are more or less completely described in the works of many
authors. Special attention has been paid to the distally placed
organs and appendages, as they hold an important meaning for
classification. The structure of the proximal parts of the

reproductive system — the region lying between the spermoviduct
and the gonads, especially the fertilization-pouch-seminal-
receptacle complex (the FPSC) — have been poorly studied.

Besides the gonad with the hermaphroditic duct, the proximal
section of the reproductive system contains two more structures:
the albumen gland and a complicated system that will be called
the FPSC (Fig. 1) . In the naming of organs there is no
uniformity, and this is why in the beginning it is necessary to
clarify the terms of separate elements in relation to their
functions.

Typically, the FPSC chamber appears to be a specialized part
of the distal region of the hermaphroditic duct (where the duct
joins with the canal of the albumen gland) . This specialized
unit is located on a more or less sharp bend of the
hermaphroditic duct, submerged to varying degrees within the
tissue of the albumen glands and usually differentiated into two
chambers, the form and sizes of which are extraordinarily
variable. One of these chambers is the actual fertilization
pouch (Befruchtungstasche, fecundation pouche) , the second serves
for storage of the sperm of the partner (allosperm) , that have
entered from the spermatheca (bursa copulatrix, receptaculum
seminis, gametolytic gland) . Thus inside the body of the mollusk
there exist two places for allosperm: the distal, where the speirm
end up directly after copulation, and the proximal, which
receives a portion of the allosperm after a certain period of
time following copulation. Traditionally, we call the distal

storage area the spermatheca, and the proximal chamber the
seminal receptacle, even though both terms carry the same
meaning. The seminal receptacle contains the sperm that is
physiologically ready for the fertilization of the egg.
Fertilization occurs in the adjacent fertilization pouch.

The confluence of the ducts that descend from the
spermatheca and the albumen gland is commonly called the
carrefour (Bayne 1973), which literally means crossroads, or
intersection. The complex as a whole (the distal part of the
hermaphroditic duct, or the ascending duct + fertilization pouch
+ seminal receptacle + descending duct) , in foreign literature,
goes under the uncertain term of "talon." The meaning of the
term FPSC should be expanded; by this term we signify the whole
complex that has a morphological and functional unity. The term
"fertilization pouch" is the accepted one in Soviet scientific
literature, which we will use only to describe just one part of
the complex (FPSC) . The fertilization pouch is joined with the
seminal receptacle through an opening, which we suggest calling
the "fecundatory pore" (fecundus = fertilizing) .

Initially, the internal structure of the FPSC of a
representative of the higher order of the Stylommatophora — Helix
pomatia — was described in the works of Meisenheimer (1907, 1912)
and later, this description was included by Kilias (1960) in a
popular treatment of the common vineyard snail. Recently, Lind
(1973) corrected and verified the data of Meisenheimer. In
essence, the findings of these authors exhaust our knowledge of

the morphology of the FPSC of the higher Stylommatophora. Flasar
(1967) devoted special work to the study of the FPSC of Oxychilus
draparnaudi (Zonitidae) . He emphasized the great variation in
this structure among the studied species and the common vineyard
snail. However, these differences mainly involve the shape of
both chambers, and are of little value to systematics. Van Mol
(1971) analyzed FPSC morphology in detail for some Bulimulidae,
and showed that the FPSC in representatives of this family is
long, and that the fertilization pouch is small, but that there
is a gigantic seminal receptacle, that consists of a number of
tubular pouches. In mollusks of the family Succineidae, both
compartments of the FPSC are small, compact, and easily seen
during external examination (Bayne 197 3) . Without going into
great detail, investigators have noted differences in the
external appearance of the FPSC among many groups of mollusks:
for example Steenburg (1925) and Wiegmann (1901) in the lower
stylommatophoran order Orthurethra (Pupillidae, Enidae) , and
Pilsbry (1939-1946) in representatives of the more numerous
families that inhabit North America.

We studied the external view and the internal structure of
63 species from different families of the Stylommatophora and the
histological structure of the FPSC of 17 species of the
Helicoidea to find characters that might be useful for
systematics.

METHODS
The mollusks were dissected, the FPSCs were extracted and
cleansed of tissue of the albumen gland and were then clarified
in glycerine. To arrive at a general understanding of the
internal structure of the FPSC, several cross-sections were made
at different levels using ophthalmic scissors. For histological
investigation the FPSC was sectioned together with the adjacent
parts of the spermoviduct, albumen gland, and hermaphroditic
duct. Samples were fixed in 70% ethyl alcohol; prior to fixation
the animals were drowned in water for a period of 18-24 hours.
Before immersion in paraffin, butanol was used. The series of
cross-sections, each with a thickness of seven microns, was
stained with hematoxylin and with eosin or orange G.

RESULTS
Morphology of the FPSC

Primitively the FPSC, as mentioned above, is a slightly
differentiated part of the hermaphroditic duct. In some
Orthurethra (for example Partula otaheitana and some Enidae) we
were unable to find two chambers in the corresponding part of the
hermaphroditic duct. The development and partitioning of the
FPSC can already be observed in some Orthurethra; in many Enidae
and Pupillidae the FPSC is externally manifested very clearly;
often, even during external examination, the two chambers can be
seen. Representatives of the family Tornatellinidae deserve
particular mention, especially the genus Fernandez ia, in which

the length of the FPSC exceeds half the length of the uterus;
moreover the FPSC is rather superficially connected with the
albumen gland. The internal structure of the FPSC of these
mollusks, unfortunately, has not been studied. In the majority
of the Orthurethra, the upper part of the hermaphroditic duct
within the limit of the albumen gland contains a transverse fold;
apparently this fold is the precursor of the FPSC. All the other
investigated Stylommatophora have an FPSC consisting of two
chambers, an ascending duct, and a descending duct, but the
structure of these chambers in mollusks of different groups is
significantly complicated by the presence of various appendages,
or pockets. More often than not, the pockets are formed in the
seminal receptacle, less often in the fertilization pouch. The
most developed pockets of the seminal receptacle occur in some
species in the families Bulimulidae and Oreohelicidae. In these
taxa, the seminal receptacle achieves a great length and is
hardly imbedded in the tissue of the albumen gland at all;
moreover, in the Oreohelicidae, the seminal receptacle is
considerably pigmented (intensely black) and tightly wound in a
spiral.

External and internal variation of the FPSC in the
Helicoidea is substantial (Fig. 2) . In some cases the FPSC seems
diagnostic of most members of a particular genus, family, or
subfamily. However, the extent of studied material is inadequate
to determine the systematic significance of the morphology of
these organs. A characteristic structure of the FPSC has been

6

noted in the Polygyridae. In this family, the expanded pockets
of the fertilization pouch are adjacent to most of the short,
spherical pockets of the seminal receptacles, giving the apical
end of the FPSC a nodular appearance. Some similarity to this
appearance is observed in the Helicodontidae; however, in species
of this family the fertilization pouch is only weakly developed.
The Bradybaenidae are characterized on the whole by relatively
long ascending and descending ducts along with quite short and
closely appressed fertilization pouch and seminal receptacle. In
the majority of the Hygromiidae, the FPSC on the whole is short
and wide, with one to three pockets extending from the
fertilization pouch, which is quite often positioned across from
the seminal receptacle.

By studying 17 species in great detail, we can formally
combine them into four groups according to the structure of their
FPSC: 1) fertilization pouch and seminal receptacle both simple
and without pockets f Xerosecta crenimargo. Bradybaena
stoliczliana. Bradybaena fruticum) ; 2) fertilization pouch with
pockets but seminal receptacle simple (Hesseolo solidior , Trichia
hispida, Archaica heptapotamica . Archaica sp. , Leucozonella sp. ) ;
3) fertilization pouch simple but seminal receptacle with pockets
(Oreohelix strigosa. Lindholmiola corcyrensis. Perforatella
bidens. Pleurodonte Isabella) ; 4) fertilization pouch and seminal
receptacle both with pockets (Caucasigena abchasica, Ammonitella
yatesi . Leucozonella ruf ispira . Webbhelix multilineata . Xeropicta
candaharica) .

The purpose of these artificial groupings is to present our
meager findings in an organized way. It should be noted that the
species included in any of these groups are significantly
different. For example, in the third group, which includes four
species belonging to four families (Oreohel icidae ,
Helicodontidae, Hygromiidae, and Camaenidae) we can observe four
distinct morphologies of the FPSC connected only by a superficial
similarity in the presence of pockets in the seminal receptacle.
In Oreohel ix striqosa. the seminal receptacle consists of two
multipocketed clusters joining into two ducts. The seminal
receptacle of Lindholmiola corcyrensis, on the contrary, is
nodular, almost spheroidal, with several very short pockets in
the form of indentations. In Perforatella bidens the seminal
receptacle has three pockets ending on different levels.
Finally, in Pleurodonte Isabella the whole length of the seminal
receptacle is separated by one barrier into two narrow pockets of
different length.

The diversity in structure of the FPSC enables us to hope
that it can be used for systematics. Exactly which characters
can be used and on what level can be determined only after the
investigation of the majority of species in each family.

Histological Structure of the FPSC

The hermaphroditic duct in the region of its ascending duct
is distinct from its gonadal section, where there are seminal
vesicles in different developmental stages. The wall of the

8

ascending duct externally consists of ringlike muscle fibers
alternating with elastic fibers; and in some cases the latter
prevail. The internal surface of the canal is pleated and lined
with a ciliated columnar epithelium. The cytoplasm of the
epithelial cells is viscous and the apical part is filled with
granules.

The combination of cilia and muscles suggests that this
section actively transports spermatids and eggs to the FPSC. The
pleated structure of the walls leads us to think that spermatids
arrive in groups and upon arrival of each group, the duct expands
in diameter by unfolding the longitudinal pleats. Most likely,
upon the arrival of a group of spermatids the ring-like muscle
mass is first to act, creating peristalsis. The cilia provide
mostly for the transport of the female gametes. In several
species the hermaphroditic duct, directly upon joining the
fertilization pouch, forms one to three pockets. In Xeropicta
candaharica fixed during the winter under laboratory conditions
these pockets as well as the fertilization pouch were filled with
spermatozoids .

The walls of the descending duct and the fertilization pouch
also consist of ringlike muscular and elastic fibers. In several
species (Oreohelix striqosa. Xeropicta candaharica, Xerosecta
crenimarqo) these contain pigment cells, which stain, sometimes
very intensely, all of the FPSC and especially the fertilization
pouch. The internal surface of the walls is pleated and lined
with ciliated columnar epithelium. In the areas of the pleats a

false impression of a multi-layered epithelium can be formed due
to the overlapping of cells. In several species (e.g.
Ammonitella yatesi) sperm were discovered in the lumen of the
descending duct. In histological structure, the walls of the
seminal receptacle and the descending duct differ from those of
the fertilization pouch if the seminal receptacle is long and
partitioned into many parts, e.g. consisting of many pockets. In
this case, the ciliated epitheliiim of the apical part of the
seminal receptacle consists of cubic cells which gradually
transform into columnar. The external layer of the wall of the
seminal receptacle also loses many of its elements (except for
the pigment cells) as a result of its branching and the
decreasing diameter of its pockets.

Judging from this, we hypothesize that the seminal
receptacle functions as more than just a container for allosperm.
Spermatids spend a period of physiological maturation inside the
seminal receptacle in close contact with separated epithelial
cells which, under these circumstances, lose cilia (Van Mol
1971) .

Seasonal Changes in the Gonad and the FPSC of Trichia hispida

Collections of this species were made near Moscow in April,
May, June, July, August, and November. Depending on the season,
we noted drastic changes in the volumes of the hermaphroditic
duct and the albumen gland. A more dramatic difference was
observed among individuals collected in July and August (Fig. 3) .

10

similar differences were observed in all species for which we
were able to collect seasonal data (Schileyko, 1971) . Obviously,
there is a close relationship between certain seasonality and the
prevalence of spermatogenesis or oogenesis.

Histological analysis confirmed this hypothesis. From April
until July, oogenesis could clearly be observed in the gonad.
The tissue structure of the walls of the ascending duct and FPSC
become more dense, and the epithelial cells which line the
internal surface are extended inward toward the lumen; the lumen
of the duct decreases but the lumen of the secretory canal of the
albumen gland, like the gland itself, is dramatically enlarged.
In an individual collected in May, an egg was found in the
fertilization pouch. From the end of July until August the
morphology changes quickly: spermatogenesis dramatically takes
over, the walls of the gonad get thin, and the lumen of the gonad
enlarges. A snail fixed in November, in a state of winter
hibernation, bears a large resemblance to the one found in April;
but eggs were found in its gonads.

ACKNOWLEDGMENTS
In conclusion, we would like to thank our foreign colleagues
Dr. J. Burch, Dr. C. M. Patterson (Michigan) and Dr. A. Smith
(California) for graciously providing material.

11

LITERATURE CITED

Bayne, C. J. 1973. Physiology of the pulmonate reproductive
tract: location of spermatozoa in isolated, self-fertilizing
succineid snails (with a discussion of pulmonate tract
terminology). Veliger, 16: 169-175.

Flasar, I. 1967. Der innere Bau der Befruchtungstasche bei
Oxychilus draparnaudi (Beck) und die Geschichte ihre
Entdeckung und Erforschung bei andere Pulmonaten. Acta
Societatis Zoologicae Bohemoslovenicae, 31: 150-158.

Kilias, R. 1960. Weinbergschnecken. Berlin.

Lind, H. 1973. The functional significance of the spermatophore
and the fate of spermatozoa in the genital tract of Helix
pomatia (Gastropoda: Stylommatophora) . Journal of Zoology.
Proceedings of the Zoological Society of London, 169: 39-64.

Meisenheimer, J. 1907. Biologie, Morphologie und Physiologie
des Begattungsvorganges und der Eiablage von Helix pomatia.
Zoologische Jahrbiicher. (Abteilung fiir Systematik) , 25: 461-
502.

Meisenheimer, J. 1912. Die Weinbergschnecken Helix pomatia L.
Monographien einheimischer Tiere, 4: 1-140.

Pilsbry, H. A. 1939-1946. Land Mollusca of North America (north
of Mexico), vols. 1 and 2. Monographs of the Academy of
Natural Sciences. Philadelphia, 3: 1-994 (parts 1 and 2),
1-520 (part 1) .

12

Schileyko, A. A. 1971. "Malacology: Deceiving similarities and
the nature of differences" (in Russian) . "Priroda"
(Nature) , 7.

Steenberg, C.-M. 1925. Etudes sur I'anatomie et la systematique
des maillots (fam. Pupillidae s. lat.). Videnskabelige
Meddelelser fra Dansk Naturhistorisk. Forening, 80: 1-215.

Van Mol, J. J. 1971. Notes anatomiques sur les Bulimulidae
(Mollusques, Gasteropodes, Pulmones) . Annales de la Societe
Royale Zoologique de Belgique, 101: 183-226.

Wiegman, F. 1901. Binnen-Mollusken aus Westchina und
Centralasien. Zootomische Untersuchungen. II. Die
Buliminiden. Annaire du Musee Zoologique de I'Academie
Imperiale des Sciences. St. Petersbourg, 6: 220-298, pis.
10-11.

13

Fig. 1. External view (A) and internal structure (B)
of the FPSC of Fruticocampylaea narzanensis.

a = ascending duct (distal hermaphroditic duct) ; ap =
pocket of ascending duct (= pocket of fertilization
pouch); d = descending duct; f = fertilization pouch;
p = fertilization pore; s = seminal receptacle

Fig. 2. External view and the internal structure of the FPSC
of various representatives of the Helicoidea. A. Lindholmiola
B.

corcyrens i s ;

Bradybaena f rut icum; C . Xerosecta crenimargo;
D. Oreohelix strigosa; E. Pleurodonte Isabella; F. LeucozoneT la

ruf i sp i ra ; G. Archaica heptapotamica ; H. Perforatel la bidens;
I. Xeropicta candaharica; J. Hesseola sol id ior ; K. Karabagh ia
b i tuberosa ; L . Tr iodops i s mu 1 1 i 1 i nea ta ■

a = ascending duct (distal hermaphroditic duct); ap = pocket
of ascending duct (= pocket of fertilization pouch); f = fertill
zation pouch; s = seminal receptacle; sp = pockets of seminal
receptac le

Fig. 3. External view of tine albumen gland and the
hermaphroditic duct of Trichia hispida in different
seasons. Roman numerals indicate months. The arrow
indicates the position of the FPSC.

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