Intrapopulation variation in shell morphological traits and banding polymorphism of the land snail Cepaea vindobonensis (Gastropoda; Pulmonata; Helicidae)

Abstract

A.S. Kramarenko, Zh.V. Ignatenko, O.I. Yulevich, Y.V. Barkar, A.V. Markowska, O.O. Salamatina, V.M. Stamat, S.S. Kramarenko

The main goal of this paper was to analyze intrapopulation variation of both morphological traits and shell banding polymorphism using the example of a continuous population (a metapopulation) of the land snail Cepaea vindobonensis (Férussac, 1821). A total of 14 samples of the land snail C.  vindobonensis from a population located in the “Dubki” Park (Ukraine, Mykolayiv) were collected in May-July 2007. The land snail collection sites are divided into three areas by buildings and asphalt roads, indicated by the Latin letters A, B and C. The major diameter of shell (MJD), the minor diameter of shell (MID) and the shell height (SH) were measured with a digital calliper to the nearest 0.05 mm. Two shell shape indices (SF1 and SF2) were also computed.

A high level of the intrapopulation variation of the land snail C. vindobonensis was found in our study. Significant differences between sample means were found for all shell traits and indices used (except for SF1), however, maximum difference was noted for SH and SF2 (in both cases: P < 0.001).  About 80% of the total variation of the variance-covariance matrix was explained by the 1st and 2nd Principal Components (PC1 and PC2). The PC1 was characterized by high positive factor loadings of MJD, MID and SH and thus can be interpreted as “shell size dimension” and the PC2 had a high correlation with SF2 and thus it can be interpreted as “shell globularity”. The PC1 and PC2 determined a high level of spatial differentiation of intrapopulation morphological variation of the land snail C. vindobonensis. Samples with small (area A) and large (areas B and C) shells were separated from each other according to the PC1.  Areas B and C were characterized by individuals with flatness and globularity shells, respectively.

The areas A, B and C differed significantly in the total number of morphs, average number of morphs and frequency of rare morphs (Kruskal-Wallis H-test; in all cases P < 0.010). At the same time, the highest value of phenetic diversity was noted for samples collected within A and C areas. In general all phenetic diversity estimators showed a positive correlation with sample size (Spearman's correlation coefficient; in all cases P < 0.05). It was found that the type of biotope did not likely affect the frequency of individual morphs with respect to the shell banding polymorphism pattern. With regard to the most common morphs two patterns of the spatial arrangement of the intrapopulation variation were found – clinal pattern was for the frequency of pallescens morph and chaotic pattern was for frequency of “12345” morph.

Keywords: Intrapopulation variantion; Shell morphological traits; Shell Banding polymorphism; Land snail; Cepaea vindobonensis
 

References

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.  

Armbruster, G. (1995). Univariate and multivariate analyses of shell variables within the genus Cochlicopa (Gastropoda: Pulmonata: Cochlicopidae). Journal of Molluscan Studies, 61(2), 225-235.  

Aubry, S., Labaune, C., Magnin, F., Roche, P., & Kiss, L. (2006). Active and passive dispersal of an invading land snail in Mediterranean France. The Journal of Animal Ecology, 75(3), 802-813.

Avaca, M. S., Narvarte, M., Martín, P., & Van Der Molen, S. (2013). Shell shape variation in the Nassariid Buccinanops globulosus in northern Patagonia. Helgoland Marine Research, 67(3), 567-577.  

Balbi, M., Ernoult, A., Poli, P., Madec, L., et al. (2018). Functional connectivity in replicated urban landscapes in the land snail (Cornu aspersum). Molecular ecology, 27(6), 1357-1370.  

Baur, B. (1988). Microgeographical variation in shell size of the land snail Chondrina clienta. Biological Journal of the Linnean Society, 35(3), 247-259.  

Baur, A., & Baur, B. (1990). Are roads barriers to dispersal in the land snail Arianta arbustorum? Canadian Journal of Zoology, 68(3), 613-617  

Bengtson, S. A., Nilsson, A., Nordström, S., & Rundgren, S. (1979). Selection for adult shell size in natural populations of the landsnail Cepaea hortensis (Müll.). Annales Zoologici Fennici, 16(3), 187-194.  

Cain, A. J., & Currey, J. D. (1963). Area effects in Cepaea on the Larkhill Artillery ranges, Salisbury plain. Journal of the Linnean Society of London. Zoology, 45(303), 1-15.  

Cain, A. J., & Sheppard, P. M. (1950). Selection in the polymorphic land snail Cepaea nemoralis. Heredity, 4(3), 275-294.  

Chiba, S. (1998). Synchronized evolution in lineages of land snails in oceanic islands. Paleobiology, 24(1), 99-108.  

Clarke, B. C., Arthur, W., Horsley, D. T., & Parkin, D. T. (1978). Genetic variation and natural selection in pulmonate snails. The Pulmonates. 2A. Systematics, evolution and ecology (ed. V. Fretter & J. Peake). New York: Academic Press, 1978. P. 220-270.

Dan, N. A., & Bailey, S. E. R. (1982). Growth, mortality, and feeding rates of the snail Helix aspersa at different population densities in the laboratory, and the depression of activity of helicid snails by other individuals, or their mucus. Journal of Molluscan Studies, 48(3), 257-265.  

De Wolf, H., Backeljau, T., Medeiros, R., & Verhagen, R. (1997). Microgeographical shell variation in Littorina striata, a planktonic developing periwinkle. Marine Biology, 129(2), 331-342.  

Endler, J. A. (1977). Geographic variation, speciation, and clines. Princeton, N.J.: Princeton University Press, USA.

Funk, A., & Reckendorfer, W. (2008). Environmental heterogeneity and morphological variability in Pisidium subtruncatum (Sphaeriidae, Bivalvia). International Review of Hydrobiology, 93(2), 188-199.  

Giokas, S. (2000). Congruence and conflict in Albinaria (Gastropoda, Clausiliidae). A review of morphological and molecular phylogenetic approaches. Belgian Journal of Zoology, 130 (Suppl. 1), 93-100.

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

Gould, S., & Woodruff, D. (1985). Evolution and systematics of Cerion (Mollusca: Pulmonata) on new providence Island: a radical revision. Bulletin of the American Museum of Natural History, 182(4). 389-490.

Harvey, M., & Vincent, B. (1991). Spatial variability of length-specific production in shell, somatic tissue and sexual products of Macoma balthica in the Lower St. Lawrence Estuary. I. Small- and meso-scale variability. Marine ecology progress series. Oldendorf, 75(1), 55-66.  

Hershler, R., & Minckley, W. L. (1986). Microgeographic variation in the banded spring snail (Hydrobiidae: Mexipyrgus) from the Cuatro Ciénegas basin, Coahuila, Mexico. Malacologia, 27, 357-374.

Hummer, O., Harper, D. A. T., & Ryan, P. D. (2001). PAST: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica, 4(1), 1-9.  

Jordaens, K., Van Riel, P., Frias Martins, A. M., & Backeljau, T. (2009). Speciation on the Azores islands: congruent patterns in shell morphology, genital anatomy, and molecular markers in endemic land snails (Gastropoda, Leptaxinae). Biological Journal of the Linnean Society, 97(1), 166-176.  

Kramarenko, S. S. (2014). Active and passive dispersal of terrestrial mollusks: a review. Ruthenica, Russian Malacological Journal, 24(1), 1-14. (In Russian)

Kramarenko, S. S. (2016). Patterns of spatio-temporal variation in land snails: a multi-scale approach. Folia Malacologica, 24(3), 111-177.  

Kramarenko, S. S., & Dovgal, I. V. (2014). Spatial variation of the land snail Brephulopsis cylindrica (Gastropoda, Pulmonata, Enidae): A fractal approach. Vestnik zoologii, 48(5), 433-440.  

Moran, P. A. (1950). Notes on continuous stochastic phenomena. Biometrika, 37(1/2), 17-23.  

Ochman, H., Jones, J. S., & Selander, R. K. (1983). Molecular area effects in Cepaea. Proceedings of the National Academy of Sciences, 80(13), 4189-4193.  

Perry, R., & Arthur, W. (1991). Shell size and population density in large helicid land snails. The Journal of Animal Ecology, 60(2), 409-421  

Rangel, T. F., Diniz-Filho, J. A. F., & Bini, L. M. (2010). SAM: a comprehensive application for spatial analysis in macroecology. Ecography, 33(1), 46-50.  

Slatkin, M. (1987). Gene flow and the geographic structure of natural populations. Science, 236(4803), 787-792.  

Sokal, R. R., & Oden, N. L. (1978). Spatial autocorrelation in biology: 1. Methodology. Biological journal of the Linnean Society, 10(2), 199-228.  

Sverlova, N. V., Khlus, L. N., Kramarenko, S. S., Son, M. O., et al. (2006). Fauna, ekologiya i vnutrividovaya izmenchivost'nazemnykh mollyuskov v urbanizirovannoy srede [Fauna, ecology and intraspecific variability of the terrestrial molluscs in an urban environment]. Lviv: National Museum of Natural History at the NAS of Ukraine (in Russian).

Stankowski, S. (2011). Extreme, continuous variation in an island snail: local diversification and association of shell form with the current environment. Biological Journal of the Linnean Society, 104(4), 756-769.  

Trombulak, S. C., & Frissell, C. A. (2000). Review of ecological effects of roads on terrestrial and aquatic communities. Conservation biology, 14(1), 18-30.  

Underhill, J. E., & Angold, P. G. (1999). Effects of roads on wildlife in an intensively modified landscape. Environmental Reviews, 8(1), 21-39.  

Van Marion, P. (1981). Intra-population variation of the shell of Littorina rudis (Maton) (Mollusca: Prosobranchia). Journal of Molluscan Studies, 47(1), 99-107.  

Vong, A., Ansart, A., & Dahirel, M. (2019). Dispersers are more likely to follow mucus trails in the land snail Cornu aspersum. The Science of Nature, 106(7-8), 43.  

Woodruff, D. S., & Gould, S. J. (1980). Geographic differentiation and speciation in Cerion – a preliminary discussion of patterns and processes. Biological journal of the Linnean Society, 14(3-4), 389-416.  

Underhill, J. E., & Angold, P. G. (1999). Effects of roads on wildlife in an intensively modified landscape. Environmental Reviews, 8(1), 21-39.  

Yusseppone, M. S., Márquez, F., Luquet, C. M., Brey, T., Ríos de Molina, M. C., & Rocchetta, I. (2018). Does shell shape variation play a role in conservation of the long-lived freshwater bivalve Diplodon chilensis (Bivalvia, Hyriidae)? Ecohydrology, 11(2), e1931.  

Zhivotovsky, L.A. (1991). Population Biometrics. Moscow: Nauka Publishing.

Zhukov, O. V., Kovalenko, D. V., Kramarenko, S. S., & Kramarenko, A. S. (2019). Analysis of the spatial distribution of the ecological niche of the land snail Brephulopsis cylindrica (Stylommatophora, Enidae) in technosols. Biosystems Diversity, 27(1), 62-68.  

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