Abstract
The operculum morphology of neritid snails of genus Theodoxus Montfort, 1810 yields important species-specific taxonomic characters. This study is the first attempt to describe morphological differences in snails based on operculum shapes using a geometric morphometric approach. We examined the variability of opercular shapes between sexes and among populations and species based on 91 opercula of adult specimens belonging to six populations of three species of Theodoxus from the central Balkan and the southern border of the Pannonian plain. There are no sex-related differences in operculum shape and size in the studied species. The presence of shape variations influenced by size (allometry) was confirmed for T. danubialis (C. Pfeiffer, 1828) indicating that allometry could be a component of the morphological variation of this species. At the intraspecific level, phenotypic plasticity of operculum shape was found in T. danubialis and T. fluviatilis (Linnaeus, 1758). Of particular interest is the lack of morphological variability in the rare and endangered T. transversalis (C. Pfeiffer, 1828). At the species level a clear morphological distinction of T. fluviatilis from T. danubialis and T. transversalis was detected, confirming that the operculum with a rib could be used as a species-specific morphological character. The main morphological differences between species are an outwardly-stretched opercular/apophysal rib and a shortened tip of the opercular plate in T. fluviatilis, compared to the same structures in T. danubialis and T. transversalis.
References
Adams, D.C., Rohlf, F.J. & Slice, D.E. (2004) Geometric morphometrics: ten years of progress following the ‘revolution’. Italian Journal of Zoology, 71, 5–16.
https://doi.org/10.1080/11250000409356545
Alba, D.M., Corbella, J., Guillén, G., Prats, L. & Tarruella, A. (2016) Presence of two different species of Theodoxus Montfort, 1810 (Gastropoda: Neritidae) in Catalonia. Spira, 6, 41–65.
Anistratenko, V.V., Zettler, M.L. & Anistratenko, O.Y. (2017) On the taxonomic relationship between Theodoxus pallasi and T. astrachanicus (Gastropoda: Neritidae) from the Ponto-Caspian region. Archiv für Molluskenkunde International Journal of Malacology, 146, 213–226.
https://doi.org/10.1127/arch.moll/146/213-226
Bandel, K. (2001) The history of Theodoxus and Neritina connected with description and systematic evaluation of related Neritimorpha (Gastropoda). Mitteilungen aus dem Geologisch-paläontologischen Institut der Universität Hamburg, 85, 65–164.
Bodon, M. & Giovanelli, M.M. (1995) Sulla sistematica e distribuzione di Theodoxus danubialis (Pfeiffer, 1828) in Italia. Bollettino-Museo Regionale di Scienze Naturali, 13, 493–544.
Bourdeau, P.E. (2012) Intraspecific trait cospecialization of constitutive and inducible morphological defences in a marine snail from habitats with different predation risk. Journal of Animal Ecology, 81, 849–858.
https://doi.org/10.1111/j.1365-2656.2012.01965.x
Brown, D.S. (2002) Freshwater snails of Africa and their medical importance. CRC Press, USA, 608pp.
Brown, K.M. & Lydeard, C. (2010) Mollusca: Gastropoda. In: Thorp, J. H. & Covich, A. P. (Eds.) Ecology and Classification of North American Freshwater Invertebrates, Academic Press, pp. 277–306.
https://doi.org/10.1016/B978-0-12-374855-3.00010-8
Bunje, P.M. (2005) Pan-European phylogeography of the aquatic snail Theodoxus fluviatilis (Gastropoda: Neritidae). Molecular Ecology, 14, 4323–4340.
https://doi.org/10.1111/j.1365-294X.2005.02703.x
Bunje, P.M. & Lindberg, D.R. (2007) Lineage divergence of a freshwater snail clade associated with post-Tethys marine basin development. Molecular Phylogenetics and Evolution, 42, 373–387.
https://doi.org/10.1016/j.ympev.2006.06.026
Carvajal-Rodríguez, A., Guerra-Varela, J., Fernández, B., Rolán, E. & Rolán-Álvarez, E. (2006) An example of the application of geometric morphometric tools to the morphological diagnosis of two sibling species in Nassarius (Mollusca, Prosobranchia). Iberus, 24, 81–88.
Checa, A.G. & Jimenez-Jimenez, A.P. (1998) Constructional morphology, origin, and evolution of the gastropod operculum. Paleobiology, 24, 109–132.
https://doi.org/10.1017/S0094837300020005
Chiu, Y.W., Chen, H.C., Lee, S.C. & Chen, C.A. (2002) Morphometric analysis of shell and operculum variations in the viviparid snail, Cipangopaludina chinensis (Mollusca: Gastropoda), in Taiwan. Zoological Studies, 41, 321–331.
Dagan, D. (1971) Taxonomic discrimination between certain species of the genus Theodoxus (Gastropods; Neritidae). Israel Journal of Zoology, 20, 223–229.
Dryden, I.L. & Mardia, K.V. (2016) Statistical shape analysis with applications in R. 2nd edition, Wiley, Chichester, 496 pp.
https://doi.org/10.1002/9781119072492
Elkarmi, A. & Ismail, N. (2006) Population structure and shell morphometrics of the gastropod Theodoxus macri (Neritidae: Prosobranchia) from Azraq Oasis, Jordan. Pakistan Journal of Biological Sciences, 9, 549–552.
https://doi.org/10.3923/pjbs.2006.549.552
Farman, K.S. & Almukhtar, E.A. (2015) Gastropods Morphometric Shell Landmarks variation in Diyala River Basin, Iraq. International Journal of Applied Research, 1, 660–664.
Fehér, Z., Zettler, M. & Szabo, K. (2009) An attempt to reveal the systematic relationship between Theodoxus prevostianus (C. Pfeiffer, 1828) and Theodoxus danubialis (C. Pfeiffer, 1828) (Mollusca, Gastropoda, Neritidae). Mollusca, 27, 95–107.
Feher, Z., Albrecht, C., Sereda, S. & Krizsik, V. (2012) Extremely low genetic diversity in the endangered striped nerite, Theodoxus transversalis (Mollusca, Gastropoda, Neritidae)-a result of ancestral or recent effects? North-western Journal of zoology, 8, 300–307.
Fretter V. & Graham A. (1962) British prosobranch molluscs. Their functional anatomy and ecology. Ray Society, London, 755 pp.
Glöer, P. (2002) Süsswassergastropoden Nord-und Mitteleuropas: Bestimmungsschlüssel, Lebensweise, Verbreitung, ConchBooks, Hackenheim, 327 pp.
Glöer, P. & Pešić, V. (2012) The freshwater snails (Gastropoda) of Iran, with descriptions of two new genera and eight new species. ZooKeys, 219, 11–61.
https://doi.org/10.3897/zookeys.219.3406]Glöer, P. & Pešić, V. (2015) The morphological plasticity of Theodoxus fluviatilis (Linnaeus, 1758) (Mollusca: Gastropoda: Neritidae). Ecologica Montenegrina, 2, 88–92.
Govindan, K. & Natarajan, R. (1974) Studies in Neritidae (Neritacea: Prosobranchia) from peninsular India. Proceedings of the Indian National Science Academy, B, 38, 225–239.
Heller, J. (1979) Visual versus non-visual selection of shell colour in an Israeli freshwater snail. Oecologia, 44, 98–104.
https://doi.org/10.1007/BF00346406
Ivanović, A. & Kalezić, M. (2013) Evoluciona morfologija: teorijske postavke i geometrijska morfometrija. Faculty of Biology, Belgrad, 1–223.
Jojić, V., Bugarski-Stanojević, V., Blagojević, J. & Vujošević, M. (2014) Discrimination of the sibling species Apodemus flavicollis and A. sylvaticus (Rodentia, Muridae). Zoologischer Anzeiger-A Journal of Comparative Zoology, 253, 261–269.
https://doi.org/10.1016/j.jcz.2014.02.002
Kebapçı, U. & Van Damme, D. (2012) Theodoxus fluviatilis (errata version published in 2017). The IUCN Red List of Threatened Species 2012: e.T165352A113400624. [Downloaded on 10 May 2018]
Kaliontzopoulou, A., Carretero, M.A. & Llorente, G.A. (2007) Head shape allometry and proximate causes of head sexual dimorphism in Podarcis lizards: joining linear and geometric morphometrics. Biological Journal of the Linnean Society, 93, 111–124.
https:// doi.org/10.1111/j.1095-8312.2007.00921.x
Kelly, P.M. & Cory, J.S. (1987) Operculum closing as a defence against predatory leeches in four British freshwater prosobranch snails. Hydrobiologia, 144, 121–124.
https://doi.org/10.1007/BF00014525Klingenberg, C.P. (1996) Multivariate allometry. In: Marcus L.F., Corti, M., Loy, A., Naylor, G.J.P. & Slice, D.E. (Eds.), Advances in morphometrics. Plenum Press, New York, pp. 23–49.
https://doi.org/10.1007/978-1-4757-9083-2_3
Klingenberg, C.P. (2010) Evolution and development of shape: integrating quantitative approaches. Nature Reviews Genetics, 11, 623–635.
https://doi.org/10.1038/nrg2829
Klingenberg, C.P. (2011) MorphoJ: an integrated software package for geometric morphometrics. Molecular Ecology Resources, 11, 353–357.
https://doi.org/10.1111/j.1755-0998.2010.02924.x
Klingenberg, C.P. (2013) Visualizations in geometric morphometrics: how to read and how to make graphs showing shape changes. Hystrix, 24, 15–24.
https://doi.org/10.4404/hystrix-24.1-7691
Klingenberg, C.P., Duttke, S. Whelan, S. & Kim, M. (2012) Developmental plasticity, morphological variation and evolvability: a multilevel analysis of morphometric integration in the shape of compound leaves. Journal of Evolutionary Biology, 25, 115–129.
https://doi.org/10.4404/hystrix-24.1-7691
Lawing, A.M. & Polly, P.D. (2010) Geometric morphometrics: recent applications to the study of evolution and development. Journal of Zoology, 280, 1–7.
https://doi.org/10.1111/j.1469-7998.2009.00620.x
Linnaeus, C. (1758) Systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis locis. Tomus 1. Laurentius Salvius, Holmiae, iii + 824 pp.
https://doi.org/10.5962/bhl.title.37256
Marković, V., Tomović, J., Ilić, M., Kračun-Kolarević, M., Novaković, B., Paunović, M. & Nikolić, V. (2014) Distribution of the species of Theodoxus Montfort, 1810 (Gastropoda: Neritidae) in Serbia: an Overview. Acta zoologica Bulgarica, 66, 477–484.
Merilä, J. & Hendry, A.P. (2014) Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evolutionary applications, 7, 1–14.
https://doi.org/10.1111/eva.12137
Мezhzherin, S.V., Tarasova, J.V. & Zhalay, E.I. (2011) Mollusks of the genus Theodoxus (Gastropoda, Neritidae) of Ukraine: the morphological analysis and analysis of allozsmes. Vestnik zoologii, 45, 531–540. [In Ukrainian: Моллюски рода Theodoxus (Gastropoda, Neritidae) Украины: морфологический и аллозимный анализ]
Minton, R.L., Norwood, A.P. & Hayes, D.M. (2008) Quantifying phenotypic gradients in freshwater snails: a case study in Lithasia (Gastropoda: Pleuroceridae). Hydrobiologia, 605, 173–182.
https://doi.org/10.1007/s10750-008-9332-1
Minton, R.L. & Wang, L.L. (2011) Evidence of sexual shape dimorphism in Viviparus (Gastropoda: Viviparidae). Journal of Molluscan Studies, 77, 315–317.
https://doi.org/10.1093/mollus/eyr014
Moneva, C.S.O., Demayo, C.G. & Torres, M.A.J. (2012) Applications of geometric morphometric analysis in describing sexual dimorphism in shell shapes in Vivipara angularis Muller (Family Viviparidae). Animal Biology and Animal Husbandry, 4, 14–19.
Montfort, P.D. de (1810) Conchyliologie systématique et classification méthodique de coquilles; offrant leurs figures, leur arrangement générique, leurs descriptions caractéristiques, leurs noms; ainsi que leur synonymie en plusieurs langues. Ouvrage destiné ŕ faciliter l'étude des coquilles, ainsi que leur disposition dans les cabinets d'histoire naturelle. Coquilles univalves, non cloisonnées. 2. Schoell, Paris, 676 pp.
Norton, S.F. (1988) Role of the gastropod shell and operculum in inhibiting predation by fishes. Science, 241, 92–94.
https://doi.org/10.1126/science.241.4861.92
Perrard, A., Villemant, C., Carpenter, J.M. & Baylac, M. (2012) Differences in caste dimorphism among three hornet species (Hymenoptera: Vespidae): forewing size, shape and allometry. Journal of evolutionary biology, 25, 1389–1398. https://doi.org/10.1111/j.1420-9101.2012.02527.x
Pfeiffer, C. (1828) Naturgeschichte deutscher Land-und Süsswasser-Mollusken. Dritte Abtheilung. Landes-Industrie-Comptoir, Weimar, vi+ 84 pp.
Pfleger, V. (1998) A field guide in colour to Molluscs. Blitz Editions, Leicester, United Kingdom.
Philippi, R.A. (1836) Eumeratio molluscorum Siciliae. E. Anton, Halle, Germany, 303 pp.
R Development Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from: http://www.R-project.org (accessed October 2018)
Rohlf, F.J. (2008) TpsDig, Version 2.12. Stony Brook, NY, USA: SUNY at Stony Brook. Available from: http://life.bio.sunysb.edu/morph/soft-dataacq. html (accessed October 2018)
Sheets, H.D. (2003) IMP: Integrated Morphometrics Package. Buffalo, NY, USA: Department of Physics, Canisius College. Available from: http://www3.canisius.edu/~sheets/morphsoft.html (accessed October 2018)
Schütt, H. & Şeşen, R. (1992) The genus Theodoxus in South-western Anatolia, Turkey (Gastropoda, Prosobranchia, Neritidae). Zoology In The Middle East, 6, 63–68.
https://doi.org/10.1080/09397140.1992.10637614
Shubrat, J.V. (2007) A complex analysis of the conichological features of Theodoxus species of Ukraine. Вісник Львівського університету. Серія біологічна, 45, 154–159.[In Ukrainian: Комплексний аналіз конхіологічних ознак видів роду Theodoxus України]
Singh, N., Harvati, K., Hublin, J.J. & Klingenberg, C.P. (2012) Morphological evolution through integration: a quantitative study of cranial integration in Homo, Pan, Gorilla and Pongo. Journal of Human Evolution, 62, 155–164.
https://doi.org/10.1016/j.jhevol.2011.11.006
Sólymos, P. & Feher, Z. (2011) Theodoxus transversalis. The IUCN Red List of Threatened Species 2011: e.T21726A9314252. Downloaded on 10 May 2018.
StatSoft, Inc. (2004) STATISTICA (data analysis software system), version 7. Available from: www.statsoft.com/ (accessed October 2018)
Stone, J.R. (1998) Landmark based thin plate spline relative warp analysis of gastropod shells. Systematic Biology, 47, 254–263.
https://doi.org/10.1080/106351598260905
Tarasova, J.V. (2014) The intraspecific conichological variability of Theodoxus fluviatilis (Mollusca, Gastropoda, Pectinibranchia, Neritidae) fromUkraininan reservoirs. Наукові записки Тернопільського національного педагогічного університету імені Володимира Гнатюка. Серія: Біологія, 4, 80–84. (In Ukrainian: Внутрішньовидова конхіологічна мінливість Theodoxus fluviatilis (Mollusca, Gastropoda, Pectinibranchia, Neritidae) з водойм України)
West-Eberhard, M.J. (2003) Developmental Plasticity and Evolution. Oxford University Press, Oxford, 816 pp.
Zettler, M. (2008) Two records of the regional endemic hydrobiid snail Grossuana codreanui (Grossu, 1946) in Bulgaria (Dobrudja) and some nomenclatorial notes. Mollusca, 26, 163–167.
Zettler, M.L., Frankowski, J., Bochert, R. & Rohner, M. (2004) Morphological and ecological features of Theodoxus fluviatilis (Linnaeus, 1758) from Baltic brackish water and German freshwater populations. Journal of Conchology, 38, 305–316.
Zorić, K., Marković, V., Tomović, J., Atanacković, A., Vasiljević, B., Čanak Atlagić, J., Andjus, S., Kračun-Kolarević, M., Marinković, N., Popović, N., Raković, M., Djuknić, J., Djikanović, V., Tubić, B., Ilić, M., Paunović, M., Nikolić, V. & Stamenković, G. (2016) Towards assessing genetic diversity of Theоdоxus danubialis (C. Pfeiffer, 1828) (Gastropoda; Neritidae) from Central Balkan. In: Pantovic, R.V. & Markovic, Z.S. (Eds.), Proceedings of the XXIV international conference Ecological truth, EcoIst ’16“, University of Belgrade - Technical Faculty in Bor, Serbia, pp. 61–65.