Bull
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Abdurasulova and Pazilov
Bull. Iraq nat. Hist. Mus.
(2021) 16 (4): 547-555. https://doi.org/10.26842/binhm.7.2021.16.4.0547
NATURE OF VARIABILITY OF
CANDAHARIA LEVANDERI (SIMROTH, 1902) IN THE FERGHANA
AND SURKHAN - SHERABAD VALLEYS, UZBEKISTAN
Surayyo Sh. Abdurasulova * and Аbduvaeit P. Pazilov **
*Doctoral student, Gulistan State University, Gulistan, Uzbekistan.
**Professor, Gulistan State University, Gulistan, Uzbekistan.
*Corresponding author e-mail: i.kamronbek2013@mail.ru
Received Date: 28 August 2021, Accepted Date: 09 November 2021, Published Date: 20 December2021
This work is licensed under a Creative Commons Attribution 4.0 International License
ABSTRACT
The variability of Candaharia levanderi (Simroth, 1902)(Gastropoda, Stylommatophora,
Parmacellidae) in two biotopes (southern and northern slopes, the Kampirtepa gorges, the
Kugitang Tau ridge) has been investigated using polymerase chain reaction (PCR) with the
implementation of primers, the 18S DNA of the region is amplified, the variability (sharply
differing in color) of two populations of C. levanderi is studied .
The first population is in the suburbs of Namangan, (Namangan Region); the second
population is in Kampirtepa gorges, Kugitang Tau ridge (Surkhandarya Region). It is
established that, most often, the variability of morphological signs is observed on the
coloration of mollusks. The development of body coloration is an adaptive feature that
reflects the adaptability to certain biotopes on the one hand, and landscape and climatic
conditions on the other .
Keywords: Biotope, Candaharia levanderi, Ferghana valley, Morphological feature, Surkhan-
Sherabad valley.
INTRODUCTION
Like other terrestrial mollusks, slugs are characterized by a high level of intra-and inter-
population variability. The nature and intensity of the color of slugs are often adaptive,
reflecting their adaptability to certain biotopes on the one hand, and landscape and climatic
conditions on the other (Likharev and Viktor, 1980).
It should be noted that the nature of the variability of shell-bearing mollusks living in
Central Asia is discussed in a number of works (Schileyko, 1971; Uvalieva, 1990; Pazilov,
1991; Pazilov and Daminova, 2001; Pazilov and Gaibnazarova, 2012; Pazilov and Umarov,
2021). Similar studies were conducted in the far (Cain, 1977; Goodfriend, 1986; Pettitt, 1977;
https://doi.org/10.26842/binhm.7.2021.16.4.0535
https://creativecommons.org/licenses/by/4.0/
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Nature of variability of Candaharia levanderi
Tissot, 1988a, 1988b, 1988c) and near abroad (Kramarenko, 1993; Kramarenko and Popov,
1994; Khokhutkin, 1997).
However, there is no data on the variability of slugs, including Candaharia levanderi
(Simroth, 1902), until today. Therefore, the main goal of this work was the investigation of
the inter-population variability of morphological features of C. levanderi, spread in various
landscape and climatic conditions of the Ferghana and Surkhan-Sherabad valleys.
MATERIALS AND METHODS
Material for the study has been collected during two years (2019-2020) from spatially
separated populations of C. levanderi inhabiting different habitat and climate and
geographical conditions: Fergana valley (suburbs of Namangan, near Gavasay village,
Gavasay gorges); the Northern slopes of Zarafshan range, Urgutsay; Surkhan-Sherabad valley
(Kugitang Tau, Babatag, Baysun Tau ranges (Map 1).
Collected from different habitats, the habitats of the species are radically different from
each other; in Surkhan–Sherabad district, winter is short and cold, summer is long and hot.
Hot days in Surkhan-Sherabad valley come early and last for a long time. The average
temperature of July in the flat part is 28-32 °C. The average temperature in January is +3 °C.
Precipitation on the plains ranges from 130 mm to 360 mm per year, in the foothill areas from
440 mm to 620 mm. In Namangan region, the climate is sharply continental. The average
temperature in January is +4 °C, in July +35 °C. Precipitation on the plains ranges from 135
mm to 370 mm per year, in the foothills - from 460 mm to 640 mm.
Collection of material was carried out in the plains in March and April and in the mountain
in May and June. This is due to the fact that slugs are active during these months. The optimal
temperature for succulents is 18-22 °С, and humidity is up to 20-30%. In lowland areas, the
air temperature warms up earlier, and in mountainous areas-later (Likharev and Viktor, 1980).
During the collection process, all living mollusks were seized within 5 pilot sites (size is 1 sq.
meter).
During the analysis of morphological features, 30 sexually mature species were randomly
selected from each sample and quantitative and qualitative variability were studied with the
help of the MBS-9 binocular microscope. In the study, the DNA genome was taken from the
heel part of the species C. levanderi. We use “DNeasy Blood & Tissue Kits” for DNA
sequencing in genomic DNA sequencing (QIAGEN GmbH, Germany). The PZR is made
with an automatic programmable amplifier (Touchgene Gradient, UK). During DNA
sequencing ABI PRISM ® Bigdye ™ Terminator v. 3.1, performed using a set of reagents,
special reaction parameters were recorded in the automatic sequencer ABI PRISM 3100-
AVANT. The sequencing data were taken in the "ab1" format and analyzed using the
Chromas version 1.45 program (McCartney, 1996 - 1998). Moreover, highly discriminating
individuals by morphological characteristics have been studied in the nucleotide sequence
using molecular genetic methods.
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Map (1): Map of proliferation of C. levanderi in the studied territories (Pazilov and
Azimov, 2003). ( - collection points of terrestrial mollusks).
RESULTS AND DISCUSSION
C. levanderi is considered as a Central Asian endemic species and it is found in almost all
high-altitude zones: in the desert zone-among cultivated plants, in Adyr zone-among semi-
shrubs, in mountainous zones under shrubs and among large rocks. In Uzbekistan, it is spread
in the Ferghana and Surkhan-Sherabad valleys, as well as in the ridges, such as Zarafshan,
Turkestan, Babatag, Baysun Tau and Kugitang tau.
Usually the coloration gray or grayish-yellow; mantle darker than the rest of body.
Sometimes there are populations with a dark pattern on the upper side of the body of spots
and stripes. When shortening, a clear but rounded corner appears on the posterior edge of the
mantle. The sole is always lighter than the upper side of the body it is monochrome.
After studying all the available material, it can be noted that the limits of variability of
morphological features of C. levanderi were much wider than those given in the monographs
of Likharev and Viktor (1980), Schileyko and Rymzhanov (2013) when describing the
species.
Most often, the variability of morphological features is observed in the coloration of
mollusks, and such variability is clearly observed even in biotopes located not far from each
other. For example, in mollusks living among the bushes of the Kampirtepa gorges (Kugitang
tau ridge), on the northern slopes of the hills (Pl. 1A), the body color of the mollusks is
yellowish, covered with elongated dark spots, and on the sides of the mollusk these spots
combined with yellow formed a dark yellow color. The length of the body when moving is
80-90 mm, with a reduction of 55-60 mm.
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Nature of variability of Candaharia levanderi
Plate (1): C. levanderi; (А) Living on the northern slopes of hills, (B) In southern slopes,
Kampirtepa gorges, Kugitang tau ridge (Surkhandarya region).
The color of mollusks living on the southern slopes of hills (Pl. 1B), among herbaceous
plants in an open space, is most often yellow, or part of the neck is earthy (gray), the rest is
yellow, when moving it is shiny yellow, on the sides of the legs are light gray. The length of
the body when moving is 75-85 mm and when reducing is 50-55 mm.
The mollusks living in the suburbs of Namangan (Pl. 2) have the following variability: the
body size is much larger than that of other populations, the body base is yellow, however, the
black spots on it are well developed and merge, as a result of which the body color of the
mollusks is dark yellow. On the neck there are two yellow stripes running from the mantle to
the tentacles, the separator of the tail part of the body is also yellow. On the underside of the
body there are dark spots located in a line. The length of the body when moving is 105-120
mm. when reduced; it is 70-75 mm.
Plate (2): C. levanderi living among thickets of grasses, in the suburbs of Namangan
(Namangan Region).
Thus, the results of the study show that the variability of C. levanderi is mainly observed
on the coloration of mollusks. For example, the body color (coloration) of mollusks living
among shrubs is yellowish, covered with elongated dark spots (Pl. 1A), the color of the
species of those living among herbaceous plants in an open space, is most often yellow (Pl.
1B), whereas mollusks living among thickets of grasses, have black spots on the body and
they are well developed and merge, as a result of which the color of the body of mollusks
becomes dark yellow (Pl. 2).
А B
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Abdurasulova and Pazilov
Apparently, the development of body coloration is an adaptive feature, reflecting, on the
one hand, adaptability to certain biotopes on the other hand, and landscape and climatic
conditions.
Using a polymerase chain reaction (Kuznetsov, 2002), with the use of primers, the 18S
DNA of the region was amplified, the variability (sharply differing in color) of two
populations of C. levanderi was studied. The first population is in the suburbs of Namangan,
(Namangan Region); the second population is Kampirtepa gorges, Kugitang Tau ridge
(Surkhandarya Region). The obtained data were compared with the international database
(Genbank), and the following results were obtained (Diag. 1).
Diagram (1): Comparison of the nucleotide sequences of C. levanderi of two populations
(direction from 5’ to 3’ – end, the dot indicates the nucleotide bases).
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Nature of variability of Candaharia levanderi
When comparing the nucleotide sequences of these sites (18S DNA of the region) between
the population: the suburbs of Namangan and the Kampirtepa gorges (Kugitang tau), 2
nucleotide positions are noted, which are represented by the transition between pyrimidines
(thymine instead of adenine on 205 nucleotides, thymine instead of cytosine on 206
nucleotides). The obtained results show that the nucleotide sequences of partial sections of
18S rDNA in two populations differ in morphological character (color), there were no
significant differences between their nucleotides and these individuals were one species of C.
levanderi living in different landscape and climatic conditions.
We can conclude, the snails change their color depending on the conditions of the habitat,
the composition of nutrition and the pigment contained in the mantle. Also, we have not
studied environmental factors, light intensity, pH, salinity of the studied species. Thus, having
studied the variability of C. levanderi in two populations, it was found that this species differs
in an extremely wide range of variability both biotopically and geographically
(populationally), which, living in two biotopes not far from each other, differ extremely
sharply in color and body structure.
The study of the variability of morphological features of C. levanderi revealed a certain
pattern in shape and color. For example, light brown or yellow color is characteristic of
mollusks living on the southern slopes in more open areas, while reddish-brown or dark
brown color is characteristic of biotopes with mesophytic and moisture-loving plant
associations.
CONFLICT OF INTEREST
We declare that there is no conflict of interest between the authors. We confirm that all the
pictures in the manuscript belong to us. We note in this study that there is no conflict of
interest regarding the use of the Gulistan State University laboratory.
LITERATURE CITED
Cain, A. J. 1977. Variation in the spire index of some coiled gastropod shells, and its
evolutionary significance. Philosophical Transactions of the Royal Society of London,
277: 377-428.
Goodfriend, G. A. 1986. Variation in land-snail form and size and its causes: a review.
Systematic Zoology, 35 (2): 204-223.
Khokhutkin, I. M. 1997. Structure of species variability on the example of terrestrial molluscs.
UrO RaN, Ekaterinburg, 175 pp. (In Russian).
Kramarenko, S. S. 1993. Seasonal variability of the size-age structure of the Brephulopsis
bidens population from the vicinity of the city of Simferopol. In: Topical issues of
ecology of the Azov-Black Sea region and the Mediterranean. SSU, Simferopol, p.
195-199. (In Russian).
553
Abdurasulova and Pazilov
Kramarenko, S. S. and Popov, V. N. 1994. Variation of morphological traits in land snails,
Brephulopsis Lindholm, 1925 (Gastropoda: Pulmonata: Buliminidae) in the
introgressive hybridization zone. Zhurnal obshchey biologii, 54 (6): 682-690. [In
Russian].
Kuznetsov, E. A. 2002. Polymerase chain reaction as one of the methods of genetic diagnosis.
Trudy Vserossiyskogo Instituta Gel'mintologii, 38: 163-183. (in Russian).
Likharev, I. M. and Viktor, A. J. 1980. The fauna of slugs of the USSR and adjacent countries
(Gastropoda Terrestria Nuda). Nauka, Leningrad, 437 pp. [in Russian].
Pazilov, A. 1991. Variation patterns of Chondrulopsina fedtschenkoi (Mollusca, Pulmonata)
from the Fergana and Alai ridges. Zoological Journal, 70 (10): 130-134. (In Russian).
Pazilov, A. and Azimov, D. A. 2003. Land Mollusca (Gastropoda, Pulmonata) of Uzbekistan
and Contiguous territories. Fan publishing, Tashkent, 316 pp. (In Russian).
Pazilov, A. and Daminova, D. R. 2001. The nature of variability of Chondrulopsina
intumescens of the Turkestan and Babatag ridges. Ruthenica, 9 (2): 183-186. (In
Russian).
Pazilov, A. and Gaibnazarova, F. 2012. Conchological variability of the terrestrial mollusk
Gibbulinopsis signata from the Baysuntau, Kugitangtau and Babatag ridges / Ukraine.
Ternopil National Pedagogical University named after Gnatko. Molluscs: Results,
Challenges and Achievements, Special issue: 54-56. (In Russian).
Pazilov, A. P. and Umarov, F. U. 2021. On the ecology and species diversity of the freshwater
gastropods of springs in Andijan region, Uzbekistan. Bulletin of the Iraq Natural
History Museum, 16 (3):325-340.
Pettitt, C. 1977. An investigation of variation in shell form in Discula (Hystricella) turricula
(Love, 1831) (Pulmonata; Helicacea). Journal of Conchology, 29: 147-150.
Schileyko, A. A. 1971. Malacology: deceitfulness, similarity and the nature of differences.
Priroda, 7: 75-80. (In Russian).
Schileyko, A. A. and Rymzhanov, T. S. 2013. Terrestrial molluscs of Kazakhstan and
adjacent territories. KMK Scientific Publishing Association, Moscow, Alma-Ata, 389
pp. (In Russian).
Tissot, B. N. 1988a. Geographic variation and heterochrony in two species of cowries (genus
Cyprea). Evolution, 42: 103-117.
Tissot, B. N. 1988b. Morphological variation along gradients in a population of black abalone
554
Nature of variability of Candaharia levanderi
Haliotis cracherodii Leach, 1814. Journal of Experimental Marine Biology and
Ecology, 117 (1): 71-90.
Tissot, B. N. 1988c. Multivariate analysis. In: McKinney, M. L. (ed.). Heterochrony in
evolution: a multi-disciplinary approach. Plenum Press, New York, p. 35-51.
Uvalieva, K. K. 1990. Terrestrial mollusks of Kazakhstan and adjacent territories. Science
KazSSR, Alma-Ata, 224 pp. (In Russian).
555
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Bull. Iraq nat. Hist. Mus.
(2021) 16 (4): 547-555.
Candaharia levanderi (Simroth, 1902) التباينطبيعة
أوزبكستان ،وديان شراباد -في فرغانا وسورخان
عبدوفايت ب. بازيلوف ** سولوفا * واسورايو ش. عبد الر
دكتوراه، جامعة والية كلستان، جولستان، أوزبكستان. * طالب
ن.** أستاذ بجامعة والية جولستان، جولستان، أوزبكستا
2021/ 12/ 20، تاريخ النشر: 2021/ 11/ 09، تاريخ القبول: 2021/ 08/ 28تاريخ االستالم:
الخالصة
Candaharia levanderi (Simroth, 1902)النوع تباينتم التحقيق في
(Gastropoda, Stylommatophora, Parmacellidae) ة في اثنين من البيئات الحيوي
( Kugitang Tau ridge، و Kampirtepa، وديان بية والشمالية)املنحدرات الجنو
تضخيم مع بتطبيق البادئات املناسبة( PCRتفاعل البوليميراز املتسلسل )باستخدام
التباين )االختالف الحاد في اللون( درس حمض النووي ، و لل 18S DNA املنطقة
. من النوع اعالهسكانيتين ملجموعتين
؛ املجموعة ضواحي نامانجان )منطقة نامانجان( من ية االولىاملجموعة السكان
. Kampirtepa gorges, Kugitang Tau ridge (Surkhandarya Region) منالثانية
هذا النوع من تلوين ل املظهريةالعالمات تغايرا في، لوحظ ثبت أنه ، في أغلب األحيان
كيف مع بيئات لقدرة على التالرخويات. يعد تطور لون الجسم ميزة تكيفية تعكس ا
، واملناظر الطبيعية والظروف املناخية من جهة أخرى.حيوية معينة من جهة