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Acta Zoologica Lituanica
ISSN: 1392-1657 (Print) 1648-6919 (Online) Journal homepage: http://www.tandfonline.com/loi/tzec19
MORPHOLOGICAL AND ANATOMICAL
CHARACTERISTICS OF OXYLOMA SARSI (ESMARK,
1886) (GASTROPODA: STYLOMMATOPHORA:
SUCCINEIDAE)
Ingrida Šatkauskienė
To cite this article: Ingrida Šatkauskienė (2007) MORPHOLOGICAL AND ANATOMICAL
CHARACTERISTICS OF OXYLOMA SARSI (ESMARK, 1886) (GASTROPODA: STYLOMMATOPHORA:
SUCCINEIDAE), Acta Zoologica Lituanica, 17:4, 333-340, DOI: 10.1080/13921657.2007.10512851
To link to this article: http://dx.doi.org/10.1080/13921657.2007.10512851
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Acta Zoologica Lituanica, 2007, Volumen 17, Numerus 4
ISSN 1392-1657
333
MORPHOLOGICAL AND ANATOMICAL CHARACTERISTICS OF
OXYLOMA SARSI (ESMARK, 1886) (GASTROPODA:
STYLOMMATOPHORA: SUCCINEIDAE)
Ingrida ÐATKAUSKIENË
Department of Biology, Vytautas Magnus University, Vileikos 8, LT-44404 Kaunas, Lithuania. E-mail: i.satkauskiene@gmf.vdu.lt
Abstract. Identification of Oxyloma sarsi is confused by the similarity of its shell to those of other
succineid species. In this paper, morphological criteria (shape, colour and size of the shells (measure-
ments), the reproduction system and the structure of the radula) for identification of O. sarsi are
reconsidered. New data dealing with morphological identification of O. sarsi are presented: body pig-
mentation, the shape and size of the jaw, and the parameters of the reproductive system (length of the
vagina and oviductus).
Key words: Succineidae, Oxyloma, reproduction system, identification
INTRODUCTION
The distribution of molluscs of the family Succineidae
is worldwide (Kerney & Cameron1979; Pfleger 1999).
Four species of the family Succineidae are found in
Europe and Lithuania: Succinea putris (Linnaeus, 1758),
Succinella oblonga (Draparnaud, 1801), Oxyloma sarsi
(Esmark, 1886) and Oxyloma elegans (Risso,1826)
(Gurskas 1997; Kerney 1999; Pfleger 1999; Ðivic-
kis 1960). There are only few groups in the world-
wide terrestrial malacofauna that have so pronounced
outward appearance as the representatives of the fam-
ily Succineidae. Because of the specific appearance of
the shell, Succineidae are easily distinguishable from
other families. However, within the family, different
Succineidae species usually cannot be distinguished by
conchological characters and therefore can be identi-
fied only by their anatomy, which includes not only
anatomical analysis of the genital structure, but also
the arrangement and proportion of the organs (Gusa-
rov 1999; Kerney1999; Patterson1971; Rigby 1965).
In addition, more precise identification requires analy-
sis of an animals pigmentation, colour and shape of
the shell, degree of shell calcification, size and habits
of an individual (Hoagland & Davis 1987; Patter-
son1971; Spamer & Bogan 1998). There are many
publications that analysed Succineidae in North Ame-
rica (Hoagland & Davis 1987; Patterson 1971; Spamer &
Bogan 1998; Stevens et al. 1998). However, biology
and systematics of the genera Oxyloma (Wester-
lund, 1885) and Succinea (Draparnaud, 1801) are not
extensively investigated in Europe, including Lithuania.
In the guide to Lithuanian molluscs, Ðivickis (1960)
described various Succineidae species basically ac-
cording to their conchological characteristics and there-
fore according to this guide precise identification of
the species is impossible. In another guide Gurskas
(1997) presented morphological characteristics of the
species Succineidae and the schemes of the reproduc-
tion system of three Succineidae species: S. putris,
O. elegans and O. sarsi according to Kerney et al.
(1983), Shileiko and Likharev (1986) and Grossu
(1988). However, some schemes are ambiguous, which
again in some cases does not allow precise identifica-
tion of the species.
The entire genus Oxyloma requires extensive review and
illustration. The species O.sarsi is treated as endangered
by Kerney (1999). Kerney (1999) mentioned that
O.sarsi now is found only in a few places in the Lea
valley in Herts and Essex, the lower Waveney valley and
in the East Anglian Broadland. Surviving populations are
at constant risk that originates from pollution. Vulner-
able. N.European: known from the scattered areas be-
tween the Alps and northern Scandinavia. Meanwhile,
the distribution and situation of this species in Lithuania
are unknown due to its difficult identification and
misidentification with the other species of Succineidae.
The aim of this paper is to present morphological-ana-
tomical characteristics of one species of the genus
Oxyloma (family Succineidae), Oxyloma sarsi.
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334
Ðatkauskienë I.
MATERIAL AND METHODS
Adult individuals (N = 118) of Oxyloma sarsi (Esmark, 1886)
were collected in MayJuly 2005 from two popula-
tions in the Kaunas district: Domeikava (populationI)
and Vaiðvydava (population II) villages. Specimens from
population I were taken from the coast of the Neris
River at the very proximity of water having a sandy
substrate. Composition of vegetation in the biotope was:
Polygonatum sp. Artemisia spp. Equisetum spp.
Poa spp. Salex spp. Population II was collected in a
wet grassland, near a mixed deciduous forest. Compo-
sition of the biotope was: Carex spp. Polygonatum spp.
Taraxacum officinale L. Poa spp.
Collected molluscs were frozen at -20°C. In these con-
ditions, molluscs may be kept for long periods and
used when needed for anatomical or DNA analysis.
The main part of the collected individuals (N = 118)
was used for morphological-anatomical analysis. An-
other part (N = 18) was used for culture in the labora-
tory, where the ecology and biology (reproduction,
development, life time) of the specimens were ob-
served. The sample of the foot of some individuals
(N = 10) was removed and preserved in 70% ethanol
for DNA analysis.
Before anatomical analysis, the shells of the molluscs
were removed, cleaned and kept in dry vials. The genital
systems, jaws, radula and the fragments of the mantle
were prepared from the molluscs and stored in 70%
ethanol. In order to analyse the penial appendix and
epiphallus, the penial sheath was opened and pinned
up to reveal the details of their structure. Photographs
of the shells, molluscs and reproduction systems were
taken by using a digital camera Nikon Cool Pix 5200.
Parts of the genital systems and jaws were measured
and photographed through a stereoscopic microscope
MOTIC BA4000 with a digital camera Canon D350.
The software used was MOTIC IMAGES Plus 2.0.
The radula and the fragments of the mantle were pho-
tographed by using a microscope PZO (Poland) at
magnification 140× and 280×.
Shell length and width, and aperture length and width
were measured. Data were represented as a mean ± stan-
dard deviation (sample size, minimum and maximum
values). The correlation coefficient between shell para-
meters (shell length and width, and aperture length and
width) were calculated with Analysis ToolPak (MS Excel).
Preliminary identification of species was performed by
using the guides to molluscs by Pfleger (1999), and
Kerney and Cameron (1979).
RESULTS
Morphological characteristics
The shell of alive O. sarsi mollusc is dark or black
(Fig. 1). According to Ðivickis (1960), some varia-
tions in colour and form of this species can be ob-
served. During this study, however, none of these varia-
tions did occur. The empty shell of O.sarsi is thin,
amber-coloured (there is a little variation in colouring),
translucent and consists of 3 whorls (Fig. 2).
The first whorl is large and clearly separated from the
remaining whorls. The sutures of the whorls are clear
and profound. The surface of the shell is glossy, trans-
versely striped. The edge of the shell aperture is thin,
with slight incurvature and lips.
The average height and width of the shells of the speci-
mens from the two populations were 9.03 ± 1.48 (N =
118; Min 7; Max 14) and 4.25 ± 0.57 mm (N =
118; Min 3; Max 6), respectively. Height and width
of the aperture of the shells were 6.28 ± 0.94 (N = 61;
Min 4.5; Max 8.9) and 3.71 ± 0.72 mm (N= 61;
Min 2.9; Max 5.9), respectively.
In order to verify whether there is correlation between
size parameters of the shell, the correlation coefficient
was calculated between shell length and width, and
aperture height and width. The correlation coefficient,
which varied between 0.85 and 0.92, indicated strong
correlation between these parameters (Table 1).
The sole of O. sarsi is pale, almost transparent. Sides
of the body are slightly pigmented, whereas the top of
the head is usually darkly pigmented (Fig. 1). The ob-
served pigmentation of the mantle through the micro-
scope showed that the pigmented cells are stellular,
separate and have no clear interdependence (Fig. 3).
Figure 1. Alive O. sarsi (Esmark, 1886) molluscs at copu-
lation.
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335
Morphological and anatomical characteristics of Oxyloma sarsi (Esmark, 1886)
Pigmentation of all the investigated individuals of
O. sarsi was similar and quite consistent.
Characteristics of the radula and jaw
The radula of O. sarsi is of an extended rhombus shape.
Each tooth of the radula consists of a basal plate, lying
on the basal lamina, and of a cutting plate, directed
backwards, used for food scraping (Jackiewicz 1998).
The radular teeth are arranged in parallel longitudinal
rows and distinguished by a different structure in the
middle and in the lateral sides of the radula. Teeth in
the radula are aligned in parallel rows and are distin-
Figure 2. The shell of S. putris (Linnaeus, 1758) (A and B)
and O. sarsi (Esmark,1886) (C and D).
Table 1. The correlation coefficient between shell parameters of Oxyloma sarsi.
Shell length Shell width Aperture height Aperture width
Shell length 1
Shell width 0.870945 1
Aperture height 0.881997 0.884864 1
Aperture width 0.864413 0.855932 0.914969 1
Figure 3. Pigmentation of the pallium of O. sarsi (×140).
guished by a different structure in the middle and at
the edges of the radula. The teeth in the middle of the
radula are large, with a splay cusp of the cutting plate
(Fig. 4A). The basal plate consists of a large rounded
cusp located in the centre and of smaller irregular cusps
lying laterally to the central cusp. The lateral teeth are
with a rectangular cutting plate (Fig. 4B). The neighbou-
ring small teeth have sharp cusps and cover the basal
plate. The number of these teeth can vary from 2 to 5,
but the usual number is 5.
The jaw of molluscs is built of conchiolin, produced
by the epithelial cells of the oral cavity. The jaw is used
first and foremost for cutting off larger fragments of
food (Jackiewicz1998). The basal plate of the jaw of
O. sarsi is quadrate, thin, light yellow in colour
(Fig. 9B). The cutting plate of the jaw is thick, dark
brownish, with rounded broad tips. The width of the
cutting plate between the tips was: 0.98 ± 0.095 mm
(N = 14; Min 0.85; Max 1.05). The height of the
jaw from the basal to the cutting plate was 0.99 ±
0.065 mm (N = 14; Min 0.97; Max 1.05).
Characteristics of the reproduction system
The uterus (uterus) of O. sarsi is large, having a dis-
tinct shape. A thin albumin gland (glandula albuminalis)
is separated from the uterus. The vagina (vagina) is
thick, long and forms a bend. The oviduct (oviductus)
is short, rapidly descending to the uterus. The average
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336
Ðatkauskienë I.
Figure 5. The interior structure of the penis of O. sarsi.
Figure 6. The reproduction system of O. sarsi (A), scheme
of the reproduction system (B) and the prepared penial
appendix (C): PP penis; PM penial sheath; M vagina;
S vas deferens; SP spermatheca; SPs stalk of
spermatheca; K oviductus; P prostata; G uterus; A
penial appendix.
Figure 4. The radula of O. sarsi (K cutting plate of teeth;
Bz basal plate of teeth): A medial teeth (×280); B
lateral teeth (×140).
length of the vagina is 4.04 mm ± 1.02 (N = 19; Min
2.63 mm; Max 5.86 mm). The average length of the
oviduct is 2.21 mm ± 0.63 (N = 19; Min 1.1; Max
4 mm). The prostate (prostata) is large and elongated.
The penis (penis) is mace-shaped, covered by a weakly
pigmented penial sheath (Fig. 6A, B). A distinct penial
B
A A
B
C
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337
Morphological and anatomical characteristics of Oxyloma sarsi (Esmark, 1886)
misidentification and confusion of O. sarsi with
S. putris.
As seen from Table 2, many authors (Gurskas 1997;
Gusarov 1999; Kerney 1999) indicate only the height
and width of the shells, however for precise identifi-
cation of species the parameters of the aperture are
also required. The proportion of the parameters of the
shell and aperture reflects a real form of O. sarsi.
Table 2 shows that shell parameters of O. sarsi obtai-
ned in this study are lower in comparison to those of
other authors. This discrepancy is not clear and re-
mains to be explained.
Pigmentation of Oxyloma by some features (shape of
the pigmented cells and type of connections) (Fig. 3)
differed from that of the similar species S. putris, of
which the pigmented cells are stellular, distributed ir-
regularly and are interconnected by thin, pigmented
strips (Fig. 7).
Nevertheless, the pigmentation of the mantle should
not be used as a single criterion for species identifica-
tion. Jackiewicz (1993) reported that colour patterns
on the mantle show great diversity, being similar in
some species only. Forsyth (2005) mentioned that
Succinea strigata could be distinguished from the other
species of the family by its shell, jaw and external pig-
mentation.
Table 2. Comparison of size parameters (in mm) of O. sarsi indicated by various authors.
Average shell Ðivickis Gurskas Gusarov Kerney Present study
parameters (1960) (1997) (1999) (1999) (2007)
Shell height 10.6 20.0 10.211.5 1215 9.03 ± 1.48
Shell width 05.3 05.5 4.86.5 * 4.25 ± 0.57
Aperture
height 08.1 * * * 6.28 ± 0.94
Aperture width 04.1 * * * 3.71 ± 0.72
* not indicated
Figure 7. Pigmentation of the pallium of S. putris (×280).
appendix is observed after the removal of the penial
sheath (Fig. 6C). The spermatheca is frequently large
and spherical in shape. The stalk of the spermatheca is
short (Fig. 6A, B). The interior structure of the penis
consists of the disorderly, reticulate spread of mem-
brane strands (Fig. 5).
DISCUSSION
Size, shape and colour of the shell of molluscs, includ-
ing those involved in this study, can be used as simple
and reliable indicators for preliminary identification the
genus Oxyloma in field conditions. The molluscs of
Oxyloma are small, dark, with an elongated shell and
differ considerably from S. putris specimens, which
are longer and wider. The average length and width of
the shells of O. sarsi and S. putris collected from vari-
ous populations were 9.03 ± 1.48 (N = 118; Min 7;
Max 14) and 4.25 ± 0.57 mm (N = 118; Min 3;
Max 6), and 17.47 mm ± 0.23 mm (N = 74; Min
12 mm; Max 22.9mm) and 8.23 mm ± 0.13 mm
(N= 74; Min 5.5 mm; Max 10.9 mm), respec-
tively. Statistical analysis showed that these parameters
were significantly different between these species (p <
0.0001). The same p value was obtained when com-
paring height and width of the aperture in both spe-
cies.
Certainly, size indicators cannot be applied to distin-
guish between juveniles of Oxyloma and S. putris, es-
pecially in mixed populations.
The size of the collected individuals of O. sarsi are in a
relatively good agreement with the measurements of
O. sarsi presented by Gusarov (1999), where the av-
erage height and width of the shells were 10.211.5
and 4.86.5 mm, respectively (Table 2). The same
agreement is observed when comparing the measure-
ments presented by Ðivickis (1960) (Table 2). Mean-
while, the height of the shell of O. sarsi indicated by
Gurskas (1997) is considerably larger than in this study
and that reported by other authors (Table2). One of
the reasons for such discrepancy could originate from
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338
Ðatkauskienë I.
Preliminary analysis of the radula structure led us to
propose that the radula can be used as a suitable crite-
rion for identification of the genus Oxyloma and its
separation from the species S. putris (Fig. 8). Never-
theless, the differences of the radula structure in
O.sarsi and O. elegans are not considerable, which
shows that it should not be used as a sole criterion for
separation of these two species (unpublished data).
The jaw of O. sarsi (Fig. 9B) could be used as one of
the criterion to identify this species, because a single
rounded and weakly pronounced tooth in the middle
of the cutting plate is a specific feature of O. sarsi.
The width and height of the jaw of O. sarsi are signifi-
cantly different (p < 0.0001) from jaw parameters in
S. putris (width of the cutting plate between the tips
was: 1.5mm ± 0.2 mm (N = 14; Max 2.1 mm; Min
1.2 mm); height of the jaw from the basal to the cut-
ting plate was: 1.2 mm ± 0.1 mm (N = 14; Max
1.6 mm; Min 0.9mm) (Fig. 9).
The reproduction system of the investigated specimens
of O. sarsi (Fig. 6) showed small variability. Some
variations were observed in the shape of the appendix
and the length of the stalk of the spermatheca. Despite
these small variations, the reproduction system still can
Figure 8. The radula (lateral teeth) of S. putris (×140) (A)
and the radula (lateral teeth) of O.sarsi (×140) (B).
Figure 9. The jaw of S. putris (×32) (A) and the jaw of
O. sarsi (×32) (B): K cutting plate; Bz basal plate.
A
A
B
B
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339
Morphological and anatomical characteristics of Oxyloma sarsi (Esmark, 1886)
be used as a quite reliable criterion for identification of
this species. The salient feature of the reproduction
system is the difference between the length of the va-
gina and oviductus. The average length of the vagina
is 4.04 mm ± 1.02 (N = 19; Min 2.63 mm; Max
5.86 mm) and that of the oviductus is 2.21 mm ± 0.63
(N= 19; Min 1.1; Max 4 mm). Meanwhile, the
proportion of the vagina and oviductus of S. putris is
converse (Fig. 10). The vagina is shorter: 3.37 mm ±
0.93mm (N = 23; Max 4.77 mm; Min 1.27 mm)
and the oviductus is longer: 6.97mm ± 1.51 mm (N=
23; Max 9.46 mm; Min 4.03 mm). Statistical analy-
sis showed that the length of the vagina and oviduct in
O. sarsi and S. putris was significantly different (p <
0.0001). Another important feature of the reproduc-
tion system of O. sarsi is a distinct penial appendix
that is observed after the removal of the penial sheath
(Fig. 6C). The penis of O.sarsi is mace-shaped, cov-
ered by a weakly pigmented penial sheath, whereas
that of S. putris is oblong and waisted (Figs6, 10).
In conclusion, the study shows that the first and pre-
liminary criterion for identification of Oxyloma sarsi
(Esmark, 1886) in field conditions could be the pa-
rameters of the shell (9.03 × 4.25 mm) and aperture
(6.28 × 3.71 mm), the elongated shape of the shell
(determined by the proportions of the shell and aper-
tures) and a dark, almost black colour of alive mol-
luscs. The jaw with a single weakly developed tooth in
the middle of the cutting plate could be used as the
second criterion. For more accurate identification, both
criteria must be complemented by extensive analysis
of the reproductive system. The distinct features of
Figure 10. The reproduction system of S. putris (modi-
fied after Kerney & Cameron1979): PP penis; M va-
gina; S vas deferens; SP spermatheca; SPs stalk of
spermatheca; K oviductus.
the reproductive system of O. sarsi are the appendix
of the penis (feature of the genus) and the dispropor-
tion between the length of the vagina and oviductus
(feature of the species).
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MORFOLOGINË-ANATOMINË OXYLOMA SARSI
(ESMARK, 1886) (GASTROPODA: STYLOMMATOPHORA:
S
UCCINEIDAE) CHARAKTERISTIKA
I. Ðatkauskienë
SANTRAUKA
Succineidae ðeimos rûðies Oxyloma sarsi identifikacija
yra sudëtinga dël jos panaðumo su kitomis ðios ðeimos
rûðimis. Dël ðios prieþasties O. sarsi paplitimo ir gau-
sumo Lietuvoje duomenys gali bûti netikslûs, todël yra
bûtina iðryðkinti morfologinius-anatominius kriterijus,
kuriais remiantis bûtø galima nustatyti ðià rûðá. Straips-
nyje pateikiami O. sarsi kriaukliø matavimo parametrai,
radulës ir lytinës sistemos charakteristika. Pirmà kartà
pateikiami lytinës sistemos (kiauðintakio, makðties)
struktûrø matavimai, þandikauliø ir kûno pigmenta-
cijos charakteristika.
Received: 14 November 2006
Accepted: 6 November 2007
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