Anthropogenic load іs a leading factor in the morphological variability of Chondrula tridens (Gastropoda, Enidae) in the northwestern Azov Sea region

  • O. I. Koshelev Bogdan Khmelnitsky Melitopol State Pedagogical University
  • M. V. Gensytskyi Bogdan Khmelnitsky Melitopol State Pedagogical University
  • V. O. Koshelev Bogdan Khmelnitsky Melitopol State Pedagogical University
  • N. V. Yorkina Bogdan Khmelnitsky Melitopol State Pedagogical University
  • O. M. Kunakh Oles Honchar Dnipro National University
Keywords: terrestrial mollusks; variability; conchological characteristics; morphometric analysis.


Morphometric data are widely used in biology to assess intraspecific and inter-population variability and for bioindication and environmental condition assessment. The following hypotheses have been experimentally tested in the paper: 1) the vegetation type affects the change in the shell shape of Chondrula tridens martynovi Gural-Sverlova & Gural, 2010; 2) the change in the shell shape of this species is influenced by the biotope moisture regime; 3) the shell shape changes depending on the anthropogenic load level. The material in the form of empty, fully formed Ch. tridens shells was collected in 2019 in the north-western Azov region within the basin of the Molochna River. The collection points were located in settlements and outside them and differed in vegetation, moisture regime and level of anthropogenic load. The vegetation has been expertly attributed to two alternative types: herbaceous vegetation and tree plantations. By moisture level, the locations have been assessed as xerophytic and mesoxerophytic. The anthropogenic load levels have been assessed as low, medium and high. The study revealed that the morphological characteristics of Ch. tridens demonstrate a significant component of variability, which is due to the shell size. The shell size depends on the anthropogenic impact level. Under conditions of high anthropogenic impact, the shell size increases. Mollusks from locations with low and medium anthropogenic impact levels did not differ in shell size. After extraction of the size component, morphological properties develop three main trends of variability. The mouth apparatus development of mollusks does not depend on the vegetation type, but depends on the biotope moisture level and the anthropogenic transformation level. The mollusk shell elongation was observed to have the opposite dynamics of the height parameters in relation to the width and depended on the level of anthropogenic load. Rearrangement in the mouth apparatus depended on the biotope moisture level and the anthropogenic load level. There were distinguished four clusters, the quantitative morphological features of which allowed us to identify them as morphotypes. Each location was characterized by a combination of different morphotypes, according to which the sampling points may be classified. Morphotype 1 corresponds to biotopes with low level of anthropogenic load, morphotype 4 corresponded to biotopes with high anthropogenic load. Morphotypes 2 and 3 corresponded to moderate level of anthropogenic load. Vegetation type is not an important factor in determining the morphotypic diversity of populations. Under xerophytic conditions, morphotypes 2 and 3 are more common, and under mesoxerophytic conditions, morphotypes 1 and 4 are more common. The range of molluscs in different habitats needs to be expanded in the future to clarify climatic and other patterns.


Anderson, C., Epperson, B., Fortin, M., Holderegger, R., James, P., Rosenberg, M., Scribner, K., & Spear, S. (2010). Considering spatial and temporal scale in landscape-genetic studies of gene flow. Molecular Ecology, 19(17), 3565–3575.

Anderson, T. K., Weaver, K. F., & Guralnick, R. P. (2007). Variation in adult shell morphology and life-history traits in the land snail Oreohelix cooperi in relation to biotic and abiotic factors. Journal of Molluscan Studies, 73(2), 129–137.

Barker, G. M. (2005). The character of the New Zealand land snail fauna and communities: Some evolutionary and ecological perspectives. Records of the Western Australian Museum, 68(1), 53–102.

Boschi, C. (2011). Die Schneckenfauna der Schweiz: Ein umfassendes Bild- und Bestimmungsbuch. Haupt, Bern.

Brygadyrenko, V. V., & Korolev, O. V. (2015). Morphological polymorphism in an urban population of Pterostichus melanarius (Illiger, 1798) (Coleoptera, Carabidae). Graellsia, 71(1), e025.

Brygadyrenko, V., & Reshetniak, D. (2016). Morphometric variability of Clitellocephalus ophoni (Eugregarinida, Gregarinidae) in the intestines of Harpalus rufipes (Coleoptera, Carabidae). Archives of Biological Sciences, 68(3), 587–601.

Cowie, R. H. (1990). Climatic selection on body colour in the land snail Theba pisana (Pulmonata: Helicidae). Heredity, 65(1), 123–126.

Dillon, M. E., Wang, G., & Huey, R. B. (2010). Global metabolic impacts of recent climate warming. Nature, 467(7316), 704–706.

Fusco, G., & Minelli, A. (2010). Phenotypic plasticity in development and evolution: Facts and concepts. Philosophical Transactions of the Royal Society B: Biological Sciences, 365(1540), 547–556.

Giokas, S., Pall-Gergely, B., & Mettouris, O. (2014). Nonrandom variation of morphological traits across environmental gradients in a land snail. Evolutionary Ecology, 28(2), 323–340.

Goodfriend, G. A. (1986). Variation in land-snail shell form and size and its causes: A review. Systematic Biology, 35(2), 204–223.

Gural-Sverlova, N. V., & Gural, R. I. (2010). Novye taksony nazemnyh mollyuskov iz rodov Chondrula i Brephulopsis (Enidae) s territorii Ukrainy [New taxa of the land molluscs of the genera Chondrula and Brephulopsis (Enidae) from the territory of Ukraine]. Ruthenica, 20(1), 1–12 (in Russian).

Gural-Sverlova, N. V., Busel, V. A., & Gural, R. I. (2018). Vidovoj sostav nazemnyh mollyuskov Zaporozhskoj oblasti i vliyanie na nego antropohorii [Species composition of land molluscs of Zaporozhye region and anthrogenic influence on it]. Ruthenica, 28(3), 101–112 (in Russian).

Holloway, G. J. (2002). Phenotypic plasticity: Beyond nature and nurture. Heredity, 89(6), 410–410.

Horsak, M., Chytry, M., Danihelka, J., Koci, M., Kubesova, S., Lososova, Z., Otypkova, Z., & Tichy, L. (2010). Snail faunas in the Southern Ural forests and their relations to vegetation: An analogue of the Early Holocene assemblages of Central Europe? Journal of Molluscan Studies, 76(1), 1–10.

Kerney, M., Cameron, R., & Riley, G. (1996). A field guide to the land snails of Britain and North-West Europe. Collins, London.

Kerney, M. P., Cameron, R. A., & Jungbluth, J. H. (1983). Die Landschnecken Nord und Mitteleuropas. Parey, Hamburg.

Knigge, T., Di Lellis, M. A., Monsinjon, T., & Köhler, H. R. (2017). Relevance of body size and shell colouration for thermal absorption and heat loss in white garden snails, Theba pisana (Helicidae), from Northern France. Journal of Thermal Biology, 69, 54–63.

Komlyk, V., & Brygadyrenko, V. (2020). Morphological variability of Bembidion varium (Coleoptera, Carabidae) in gradient of soil salinity. Folia Oecologica, 47(1), 23–33.

Kramarenko, S. S., & Sverlova, N. V. (2003). Do vyvchennia vnutrishnovydovoi minlyvosti Chondrula tridens (Gastropoda, Pulmonata, Buliminidae) na zakhodi Ukrainy ta ziasuvannia taksonomichnoho statusu okremykh form [The study of intraspecific variation of Chondrula tridens (Gastropoda, Pulmonata, Buliminidae) in western Ukraine and determination of the taxonomic status of certain forms]. Proceedings of the State Natural History Museum, (18), 93–110 (in Ukrainian).

Kramarenko, S. S., & Sverlova, N. V. (2006). Mizhpopuliatsiina minlyvist konkholohichnykh oznak nazemnoho moliuska Chondrula tridens (Buliminidae) Pivnichno-Zakhidnoho Prychornomoria [Interpopulation variability of conchological traits of the terrestrial mollusk Chondrula tridens (Buliminidae) in the Northwestern Black Sea Region]. Proceedings of the State Natural History Museum, 22, 105–118 (in Ukrainian).

Kunakh, O. N., Kramarenko, S. S., Zhukov, A. V., Kramarenko, A. S., & Yorkina, N. V. (2018). Fitting competing models and evaluation of model parameters of the abundance distribution of the land snail Vallonia pulchella (Pulmonata, Valloniidae). Regulatory Mechanisms in Biosystems, 9(2), 198–202.

Kunakh, O. N., Kramarenko, S. S., Zhukov, A. V., Zadorozhnaya, G. A., & Kramarenko, A. S. (2018). Intra-population spatial structure of the land snail Vallonia pulchella (Müller, 1774) (Gastropoda; Pulmonata; Valloniidae). Ruthenica, 28(3), 91–99.

Kunakh, O., & Kovalenko, D. (2019). Fitting competing models of the population abundance distribution: Land snails from Nikopol Manganese Ore Basin technosols. Ekologia Bratislava, 38(4), 367–381.

Lawton, J. H. (1999). Are there general laws in ecology? Oikos, 84(2), 177–192.

Leicht, K., Seppala, K., & Seppala, O. (2017). Potential for adaptation to climate change: Family-level variation in fitness-related traits and their responses to heat waves in a snail population. BMC Evolutionary Biology, 17(1), 140.

Madec, L., Bellido, A., & Guiller, A. (2003). Shell shape of the land snail Cornu aspersum in North Africa: Unexpected evidence of a phylogeographical splitting. Heredity, 91(3), 224–231.

Madec, L., Desbuquois, C., & Coutellec-Vreto, M. (2000). Phenotypic plasticity in reproductive traits: Importance in the life history of Helix aspersa (Mollusca: Helicidae) in a recently colonized habitat. Biological Journal of the Linnean Society, 69(1), 25–39.

Mammola, S., Milano, F., Vignal, M., Andrieu, J., & Isaia, M. (2019). Associations between habitat quality, body size and reproductive fitness in the alpine endemic spider Vesubia jugorum. Global Ecology and Biogeography, 28(9), 1325–1335.

Manel, S., Joost, S., Epperson, B., Holderegger, R., Stopfer, A., Rosenberg, M., Scribner, K., Bonin, A., & Fortin, M. (2010). Perspectives on the use of landscape genetics to detect genetic adaptive variation in the field. Molecular Ecology, 19(17), 3760–3772.

Martin, K., & Sommer, M. (2004). Relationships between land snail assemblage patterns and soil properties in temperate-humid forest ecosystems. Journal of Biogeography, 31(4), 531–545.

McGill, B., Etienne, R., Gray, J., Alonso, D., Anderson, M., Benecha, H., Dornelas, M., Enquist, B., Green, J., He, F., Hurlbert, A., Magurran, A., Marquet, P., Maurer, B., Ostling, A., Soykan, C., Ugland, K., & White, E. (2007). Species abundance distributions: Moving beyond single prediction theories to integration within an ecological framework. Ecology Letters, 10(10), 995–1015.

McQuad, C. D., Branch, G. M., & Frost, P. G. (1979). Aestivation behaviour and thermal relations of the pulmonate Theba pisana in a semi-arid environment. Journal of Thermal Biology, 4(1), 47–55.

Merila, J., & Hendry, A. (2014). Climate change, adaptation, and phenotypic plasticity: The problem and the evidence. Evolutionary Applications, 7(1), 1–14.

Miller, L. P., & Denny, M. W. (2011). Importance of behavior and morphological traits for controlling body temperature in littorinid snails. The Biological Bulletin, 220(3), 209–223.

Mizrahi, T., Heller, J., Goldenberg, S., & Arad, Z. (2010). Heat shock proteins and resistance to desiccation in congeneric land snails. Cell Stress and Chaperones, 15(4), 351–363.

Munn, A., & Treloar, M. (2017). Phenotypic plasticity in the common garden snail: Big guts and heavier mucus glands compete in snails faced with the dual challenge of poor diet and coarse substrate. Journal of Comparative Physiology B, 187(4), 545–561.

Nicolai, A., & Ansart, A. (2017). Conservation at a slow pace: Terrestrial gastropods facing fast-changing climate. Conservation Physiology, 5(1), 1–17.

Nicolai, A., Filser, J., Lenz, R., Bertrand, C., & Charrier, M. (2010). Adjustment of metabolite composition in the haemolymph to seasonal variations in the land snail Helix pomatia. Journal of Comparative Physiology B, 181, 457–466.

O’Hanlon, A., Feeney, K., Dockery, P., & Gormally, M. (2017). Quantifying phenotype-environment matching in the protected Kerry spotted slug (Mollusca: Gastropoda) using digital photography: Exposure to UV radiation determines cryptic colour morphs. Frontiers in Zoology, 14(1), 35.

Pichancourt, J. B., & van Klinken, R. D. (2012). Phenotypic plasticity influences the size, shape and dynamics of the geographic distribution of an invasive plant. PLoS One, 7(2), e32323.

Preston, F. W. (1948). The commonness and rarity of species. Ecology, 29(3), 254–283.

Riedel, A. (1988). Slimaki ladowe Gastropoda terrestria. Katalog Fauny Polski. 36. PWN, Warszawa.

Rosin, Z., Lesicki, A., Kwieciński, Z., Skórka, P., & Tryjanowski, P. (2017). Land snails benefit from human alterations in rural landscapes and habitats. Ecosphere, 8(7), e01874.

Schileyko, A. A. (1984). Fauna SSSR. Mollyuski. Nazemnyye mollyuski podotryada Pupillina fauny SSSR (Gastropoda, Pulmonata, Geophila). Tom 3, vypusk 3. [Fauna of the USSR. Mollusks, vol. 3, part 3: (Terrestrial Mollusks of the Suborder Pupillina (Gastropoda, Pulmonata, Geophila) of the Fauna of the USSR)]. Nauka, Leningrad (in Russian).

Schileyko, A. A. (2016). Functional interrelations between conchological and anatomical characters in Stylommatophora (Mollusca, Gastropoda). Archives of Zoological Museum of Lomonosov Moscow State University (54), 269–297.

Schlutz, F., & Bittmann, F. (2016). Dating archaeological cultures by their moats. A case study from the early bronze age settlement fidvar near vrable, SW Slovakia. Radiocarbon, 58(2), 331–343.

Schmidt-Nielsen, K., Taylor, C., & Shkolnik, A. (1971). Desert snails: Problems of heat, water and food. The Journal of Experimental Biology, 55(2), 385–398.

Snegin, E. A. (2011a). The genetic structure of populations of model species of terrestrial mollusks under conditions of urbanized landscape: A case study of Chondrula tridens (Gastropoda, Pulmonata). Ekological Genetics, 9(2), 54–64.

Snegin, E. A. (2011b). The role of the principle of the founder in the formation of gene pools of adventitious colonies: A case study of Chondrula tridens (Gastropoda, Pulmonata). Zoologichesky Zhurnal, 90(6), 643–648.

Sokolov, S. G., & Zhukov, A. V. (2014). Variation trends in the parasite assemblages of the Chinese sleeper Perccottus glenii (Actinopterygii: Odontobutidae) in its native habitat. Biology Bulletin, 41(5), 468–477.

Sverlova, N. V. (2006). O rasprostranenii nekotoryh vidov nazemnyh mollyuskov na territorii Ukrainy [On the distribution of some species of land molluscs on the territory of Ukraine]. Ruthenica, 16, 119–139.

Sysoev, A., & Schileyko, A. (2009). Land snails and slugs of Russia and adjacent countries. Pensoft, Sofia, Moscow.

Thomassen, H., Buermann, W., Mila, B., Graham, C., Cameron, S., Schneider, C., Pollinger, J., Saatchi, S., Wayne, R., & Smith, T. (2010). Modeling environmentally associated morphological and genetic variation in a rainforest bird, and its application to conservation prioritization. Evolutionary Applications, 3(1), 1–16.

Tytar, V. (2021). Associations between habitat quality and body size in the Carpathian-Podolian land snail Vestia turgida (Gastropoda, Clausiliidae): Species distribution model selection and assessment of performance. Zoodiversity, 55(1), 25–40.

Verberk, W., Velde, G., & Esselink, H. (2010). Explaining abundance-occupancy relationships in specialists and generalists: A case study on aquatic macroinvertebrates in standing waters. Journal of Animal Ecology, 79(3), 589–601.

Wardhaugh, C. W., Edwards, W., & Stork, N. E. (2013). Body size variation among invertebrates inhabiting different canopy microhabitat: Flower visitors are smaller. Ecological Entomology, 38(1), 101–111.

Welter-Schultes, F. (2012). European non-marine molluscs. A guide for species identification. Planet Poster Editions, Gottingen.

Welter-Schultes, F. W. (2000). The pattern of geographical and altitudinal variation in the land snail Albinaria idaea from Crete (Gastropoda: Clausiliidae). Biological Journal of the Linnean Society, 71(2), 237–250.

Willis, K., Rudner, E., & Sumegi, P. (2000). The full-glacial forests of Central and Southeastern Europe. Quaternary Research, 53(2), 203–213.

Yorkina, N., Maslikova, K., Kunah, O., & Zhukov, O. (2018). Analysis of the spatial organization of Vallonia pulchella (Muller, 1774) ecological niche in technosols (Nikopol Manganese Ore Basin, Ukraine). Ecologica Montenegrina, 17, 29–45.

Yorkina, N., Zhukov, O., & Chromysheva, O. (2019). Potential possibilities of soil mesofauna usage for biodiagnostics of soil contamination by heavy metals. Ekologia Bratislava, 38(1), 1–10.

Zhukov, O., Kunah, O., Dubinina, Y., Fedushko, M., Kotsun, V., Zhukova, Y., & Potapenko, O. (2019). Tree canopy affects soil macrofauna spatial patterns on broad- and meso-scale levels in an Eastern European poplar-willow forest in the floodplain of the River Dnipro. Folia Oecologica, 46(2), 101–114.

Zhukov, O., Kunah, O., Dubinina, Y., Zhukova, Y., & Ganzha, D. (2019). The effect of soil on spatial variation of the herbaceous layer modulated by overstorey in an Eastern European poplar-willow forest. Ekologia Bratislava, 38(3), 253–272.

Zimaroeva, А. A., Zhukov, O. V., & Ponomarenko, O. L. (2016). Determining spatial parameters of the ecological niche of Parus major (Passeriformes, Paridae) on the base of remote sensing data. Vestnik Zoologii, 50(3), 251–258.

Zymaroieva, A., Zhukov, O., Fedonyuk, T., & Pinkin, A. (2019). Application of geographically weighted principal components analysis based on soybean yield spatial variation for agro-ecological zoning of the territory. Agronomy Research, 17(6), 2460–2473.


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