ISSN 10623590, Biology Bulletin, 2012, Vol. 39, No. 6, pp. 542–546. © Pleiades Publishing, Inc., 2012. Original Russian Text © G.V. Berezkina, A.A. Zotin, 2012, published in Izvestiya Akademii Nauk, Seriya Biologicheskaya, 2012, No. 6, pp. 630–634.
ZOOLOGY
Ontogenetic Dynamics of the Shell Convolution Diameter of the River Snail Viviparus viviparus (Gastropoda, Pectinibranchia, Viviparidae) G. V. Berezkinaa and A. A. Zotinb a
bKol’tsov
Smolensk State University, ul. Przheval’skogo 4, Smolensk, 214000 Russia Institute of Developmental Biology, Russian Academy of Sciences, ul. Vavilova 26, Moscow, 119334 Russia email:
[email protected] Received December 15, 2011
Abstract—The dynamics of the shell convolution diameter with regard to the mollusk age was studied for the river snail Viviparus viviparus. It was found that the diameter of the first (juvenile) convolution remained con stant during the ontogenetic development. A weak, but significant increase in the diameter of the second and the third shell convolutions (also juvenile) was observed during the first year of postembryonic development. The forth and the fifth shell convolutions were formed during the first year of mollusk life after hatching; their diameters increased gradually during the second year, and remained constant for the remainder of the life span. DOI: 10.1134/S1062359012060039
INTRODUCTION It is known that the gastropod shell is a cone that is convolved into a 3D spiral or flat spiral. The shell begins forming during embryonic development, when the embryos are in the egg capsules. The maximal number of embryonic shell convolutions, their mor phology, and orientation are relatively stable (Berez kina, 2006a, 2011). The common rules of the gastro pod shell growth during postembryonic development are well studied for a number of groups of mollusks (Alimov, 1981; Zotin, 2009a, b; Berezkina, Arakelova, 2010; etc.). As the soft body tissues grow and the man tle margin shifts, shell growth is observed at the shell aperture. This process leads to permanent elongation of the last convolution and, therefore, to changes in the shell morphology. The shell growth rate depends on the mollusk age, the physiological state of the ani mal, and on the effect of various external factors. The final number of shell convolutions is a speciesspecific feature. The orientation of the convolutions depends on the environmental effects and may vary signifi cantly within the same species or even within the same population, i.e., for different generations born in dif ferent years (Berezkina, 2006b; Andreeva et al., 2010). Alongside with that, data on the stability level of the shell parameters are absent for the shell parts that were formed earlier during ontogenesis. This problem requires a special approach. It is known that the mollusk shell is a solid structure built mostly by СаСО3. Despite this, the shell is one of the components that is actively involved in the calcium ion exchange process in the mollusk organism; i.e., the
Cacarrying compounds are stored in the shell by the mantle gland cells or may be extracted from here for metabolism (Klein, Trant, 1961; Greenaway, 1971a, b; Young, 1975a, b). Са++ ions are among the dominat ing cations in the mollusk hemolymph (Nemcsok, Szasz, 1975; de With, 1977). The pathways of Са++ exchange between the external environment and mol lusk organism are quite complicated, when the exter nal epithelium, hemolymph, soft tissues, and shell participate in the metabolic processes (Greenaway, 1971b). Alongside with that, there is no evidence whether or not the ongoing chemical renewal of the shell compounds is accompanied by changes in its morphology. It is quite hard to find the ontogenetic changes in the shell convolutions that are already formed during embryonic development. We assume that obtaining reliable data is possible when a list of restrictions is applicable for the study object: (1) the mollusk life span must last not less than 3–4 years; (2) the mollusk shell must be large enough to fix the changes of the shell convolution parameters if they occur; and (3) all the shell convolutions must be easily identified even in the large specimens (i.e., the shells have to not be affected by active corrosion), which is possible if the animals inhabit relatively clean, oligotrophic or mesotrophic, waters of temperate warming. Among the freshwater gastropods, the mollusks of Viviparidae family, particularly river snails of genus Viviparus Monfort, 1810, refer the best to this list of restrictions.
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543 (b)
Shell height
(а)
D1 D2 D3 D4 5 mm D5 Scheme of the shell measurements. (a) General view of the shell of V. viviparus; (b) scheme of shell convolution measurements (plan view); D1–D5, diameters of the shell convolutions (respectively).
This study aims to assess the dynamics of the shell convolution diameter during the ontogenesis of Vivi parus viviparus. MATERIALS AND METHOD The mollusks Viviparus viviparus (Linnaeus, 1758) (Gastropoda, Pectinibranchia, Viviparidae) were sampled in the Dnepr River (in the vicinity of Smo lensk; 54°47′N, 31°55′E) and in the Shokhonka River (in the vicinity of Ples, Ivanovskaya oblast; 57°27′N, 41°30′E) on slightly silted and rocky bottom, sheltered areas with weak flow, at depths of 70 cm and less. In the Shokhonka River, the animals were sampled May 7, 2000; they were adult specimens, 3 to 4 years old, and embryos (with three shell convolutions) taken from the females. In the Dnepr River, the animals were sampled May 15, 2004 (adult specimens, 2 to 4 years old) and August 22, 2005; the last were adult specimens (1 to 4 years old) and embryos with three shell convolu tions, also taken from the females. The mollusks were preserved in 70% ethanol (water solution). The species were defined under shell morphology using the comparative approach suggested by Staro bogatov (Izzatulaev, Starobogatov, 1984; Kruglov, Starobogatov, 1985; Starobogatov, Tolstikova, 1986) according to the systematics of Viviparidae species inhabiting Russia (Chernogorenko, 1988). In addi tion, the species definition was checked using the most recent taxonomic keys (Starobogatov et al., 2004). The mollusk sex was defined; the animals were taken BIOLOGY BULLETIN
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out of the shells and examined for a penis (males). The females were examined for the egg capsules in venter; the state of embryos was checked. The embryos with three shell convolutions were sampled and preserved separately. The age of river snails was defined according to the winter growth tags, which were deep and prominent lines on the shell surface. The method was justified several times (Alimov, 1981; Berezkina, Arakelova, 2010). The shell convolution diameter and shell height were measured with 0.1mm accuracy (adults; 1× magnification) and 0.05mm accuracy (embryos; 2× magnification) under an MBS9 stereomicroscope (Russia). The scheme of measurements is presented in the figure. The dependence of shell convolution diameters on its height was expressed as Di = aHk,
(1)
where Di is the iconvolution diameter, H is the shell height, and a and k are coefficients. The probability of use of equation (1) was tested by the criteria of nonlinearity. The values of coefficients of equation (1) and the significance of their dissimilar ity were tested by regression analysis (Zotin, 2000). ANOVA was used to assess the dependence of the shell convolution diameter on the mollusk age and to compare the averages (Lakin, 1973).
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Table 1. Average diameter (mm) of the first three (embryonic) shell convolutions Dnepr River
Shokhonka River
Mollusk age groups Embryos Adults (morph 1) Adults (morph 2)
n
D1
D2
D3
n
D1
D2
D3
20 34 6
0.70 ± 0.01 0.71 ± 0.01 0.90 ± 0.06
1.81 ± 0.02 1.90 ± 0.03 2.76 ± 0.09
4.45 ± 0.04 4.65 ± 0.06 6.15 ± 0.12
20 20 –
0.71 ± 0.01 0.71 ± 0.01
1.76 ± 0.03 1.91 ± 0.03
4.34 ± 0.07 4.61 ± 0.06
Note: D1–D3 are diameters of the first, second, and third shell convolutions, respectively; n is the number of studied mollusks; “–” means no measurements were performed (valid for Tables 1 and 2).
Table 2. Average diameter (mm) of the fourth (D4) and fifth (D5) shell convolutions in mollusks of various ages Dnepr River
Shokhonka River
t, year 1 2 3 4
n
D4
D5
n
20 4 12 4
9.1 ± 0.1 9.7 ± 0.6 10.3 ± 0.3 10.2 ± 0.3
14.9 ± 0.2 15.4 ± 0.6 15.6 ± 0.3 15.9 ± 0.2
– – 6 14
RESULTS AND DISCUSSION A thin shell of maximum three convolutions forms during the embryonic development of Viviparus vivi parus. After hatching, the number of convolutions increases gradually due to shell growth in the aperture area. Growth is rapid during the first two productive seasons, i.e., in the first year of life, and in the begin ning of the second one (Berezkina, Arakelova, 2010), before maturation, which usually occurs at the age of 1.5–2 years (Pavlyuchenkova, 1997, 2004; Berezkina, 2006a). At the first reproduction, the shell convolution number averages 4.75 and it rarely reaches 5. Then the shell grows slowly, and the maximal number of shell convolutions varies from 5.5 to 5.75. The results of the shell convolution diameter and shell height are pre sented in Tables 1 and 2. Two significantly distinct morphs of mollusks (p < 0.001) were found in the population inhabiting the Dnepr River. They differed by the shell convolution diameter of the first three (juvenile) convolutions (Table 1). The pop ulation that inhabited the Shokhonka River was repre sented by uniform specimens. The diameters of the first three shell convolutions in adult mollusks referred to this parameter of the specimens of morph 1 sampled in the Dnepr River. The diameters of the first three shell convolutions did not depend on the mollusk age in adult specimens. That is why we combine the data obtained for different age groups in adult specimens, separately for each population and morph (Table 1). There was no significant difference in the embry onic shell convolution diameter in all the studied pop ulations.
D4 – – 9.3 ± 0.2 9.0 ± 0.2
D5 – – 15.5 ± 0.5 16.8 ± 0.4
The comparison of the data obtained for both embryos and adults (morph 1) leads to the following conclusions: —the diameter of the first convolution remains relatively constant; —the diameters of the second and the third convolu tions increase weakly but significantly (p < 0.01) during the first year of postembryonic development (Table 1). The fourth and the fifth shell convolutions (totally or partly) form during the first year of mollusk life after hatching. During the second year, a weak and signifi cant (p < 0.01) increase in their diameters is observed. There are no differences in the diameters of these con volutions in the mollusks that are 3 and 4 years old (Table 2). The same conclusions may be proposed when ana lyzing the dependence of the convolution diameter on the shell height. The shell height in freshwater gastropods increases during the whole life span (Zotin, 2009a, b; etc.), so it may be used as an age indicator in mollusks. Usually, the allometric (power) function (equation (1) type) is used to describe the relationship between the morpho metric characteristics of the animal (Alimov, Golikov, 1974; Mina, Klevezal’, 1976). Therefore, if the formal power coefficient k of equation (1) between the convo lution diameter and shell height is positive, so the diameter increases in accordance with the shell height increase (i.e., during the mollusk age). If k is zero, then the convolution diameter does not depend on the shell height. The results of coefficient calculations for equation (1) and the coefficients of correlation between the loga rithms of the shell convolution diameter and the shell BIOLOGY BULLETIN
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Table 3. Coefficients of allometric function (1) between the shell convolution diameter and shell height Number of convolution
n
k
ln(a, mm1 – k)
r2
p
1 2 3 4 5
94 92 93 54 54
0.008 ± 0.007 0.036 ± 0.008 0.028 ± 0.007 0.261 ± 0.101 0.293 ± 0.055
–0.36 ± 0.02 0.53 ± 0.02 1.45 ± 0.02 1.46 ± 0.30 1.84 ± 0.17
0.12 ± 0.10 0.43 ± 0.10 0.38 ± 0.10 0.42 ± 0.16 0.59 ± 0.11
ns
