The influence of climate on shell variation in Trochulus striolatus (C. Pfeiffer, 1828) (Gastropoda: Hygromiidae) and its implications for subspecies taxonomy

• Autorzy: Prockow M. , Kuznik-Kowalska E. , Mackiewicz P.
• Języki publikacji: EN

Abstrakty

EN

Trochulus striolatus is a land snail showing great morphometric variation in its shell, which is the basis for recognition of its subspecies. However, this variability can result from an influence of environment. To verify the possible effect of bioclimatic and spatial variables on the shell size and shape, we studied many samples collected from four biotic zones (lowland, submontane, montane and subalpine). Many of its shell features appeared significantly negatively correlated with a precipitation parameter and altitude, whereas positively correlated with temperature parameters. The shells were smaller at higher altitudes and in colder environment with greater precipitation. The reduced growth period can be an adaptive response to the shorter growing season in mountainous regions compared to lowland areas, where the longer season permits a longer growth resulting in larger mean adult body size. This conforms to the converse Bergmann's cline. The synergetic interactions between seasonality, temperature and moisture best explain the size variation in T. striolatus resulting from the influence of local environmental and/or climate factors. Therefore, there is no sufficient justification for subspecies recognition and the subspecific epithets for T. striolatus should be discarded.

Słowa kluczowe

EN

climate; shell variation; shell morphology; Trochulus striolatus; snail; Gastropoda; Hygromiidae; taxonomy

• Wydawca: -
• Czasopismo: Annales Zoologici
• Rocznik: 2017
• Tom: 67
• Numer: 2
• Opis fizyczny: p.199-220,fig.,ref.

Twórcy

autor

Prockow M.

• Museum of Natural History, University of Wroclaw, Sienkiewicza 21, 50-335 Wroclaw, Poland

autor

Kuznik-Kowalska E.

• Department of Invertebrate Systematics and Ecology, Institute of Biology, Wroclaw University of Environmental and Life Sciences, Kozuchowska 5b, 51-631 Wroclaw, Poland

autor

Mackiewicz P.

• Department of Genomics, Faculty of Biotechnology, University of Wroclaw, Joliot-Curie 14a, 50-383 Wroclaw, Poland

Bibliografia

• Anderson, R. 2005. An annotated list of the non-marine Mollusca of Britain and Ireland. Journal of Conchology, 38: 607-637.
• Anderson, T. K., Weaver, K. F. and R. P. Guralnick. 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, 73:129-137.
• Armbruster, G. F. J. 2001. Selection and habitat-specific allozyme variation in the self-fertilizing land snail Cochlicopa lubrica (O.F. Müller). Journal of Natural History, 35: 185-199.
• Arter, H. E. 1990. Spatial relationship and gene flow paths between populations of the alpine snail Arianta arbustorum (Pulmonata: Helicidae). Evolution, 44: 966-980.
• Baur, B. 1984. Shell size and growth rate differences for alpine populations of Arianta arbustorum (L.) (Pulmonata: Helicidae). Revue Suisse de Zoologie, 91: 37-46.
• Baur, B. 1988. Microgeographical variation in shell size of the land snail Ckondrina clienta. Biological Journal of the Linnean Society, 35: 247-259.
• Baur, B. 1993. Population structure, density, dispersal, and neighbourhood size in Arianta arbustorum (Linnaeus 1758) (Pulmonata: Helicidae). Annalen des Naturhistorischen Museums in Wien, 94: 307-321.
• Baur, B. 1994. Multiple paternity and individual variation in sperm precedence in the simultaneously hermaphroditic land snail inania arbustorum. Behavioral Ecology and Sociobiology, 35: 413-421.
• Baur, B. and Ch. Raboud. 1988. Life history of the land snail Arianta arbustorum along an altitudinal gradient. Journal of Animal Ecology, 57: 72-87.
• Berry, A. J. 1963. Growth and variation of the shell in certain Malayan limestone hill snails. Proceedings of the Malacological Society of London, 35: 203-206.
• Blanckenhorn, W. U. 1997. Altitudinal life history variation in the dung flies Scathophaga stercoraria and Sepsis cynipsea. Oecologia, 109: 342-352.
• Blanckenhorn, W. U. and M. Demon. 2004. Bergmann and Conerse Bergmann Latitudinal Clines in Arthropods: Two Ends of a Continuum? Integrative and Comparative Biology, 44: 413-424.
• Botes, A., M. A. McGeoch, H. G. Robertson, A. van Niekerk, H. P. Davids and S. L. Chow. 2006. Ants, altitude and change in the northern Cape Floristic Region. Journal of Biogeography, 33: 71-90.
• Braby, M. F. Eastwoo, R. G. and N. Murray. 2012. The subspecies concept in butterflies: has its application in taxonomy and conservation biology outlived its usefulness? Biological Journal of the Linnean Society, 106: 699-716.
• Burla, H. and W. Stahel. 1983. Altitudinal variation m Arianta arbustorum (Mollusca, Pulmonata) in the Swiss Alps. Genetica, 62: 95-108.
• Burnham, K. P. and D. R. Anderson. 2002. Model selection and multimodel inference: A practical information-theoretic approach, 2nd ed. Springer-Verlag, New York.
• Cabanne, G. S. Trujillo-Arias, N., Calderon, L., d'Horta, F. M. and C. Y. Miyaki. 2014. Phenotypic evolution of an Atlantic Forest passerine (Xiphorhynchus fuscus): biogeographic and systematic implications. Biological Journal of the Linnean Society, 113: 1047-1066.
• Cardini, A., Jansson, A.-U. and S. Elton. 2007. A geometric morphometric approach to the study of ecogeographical and clinal variation in vervet monkeys. Journal of Biogeography, 34:1663-1678.
• Chiba, S. 2009. Morphological divergence as a result of common adaptation to a shared environment in land snails of the genus Hirasea. Journal of Molluscan Studies, 75: 253-259.
• Chown, S. L. and C. J. Klok. 2003. Altitudinal body size clines: Latitudinal effects associated with changing seasonality. Ecography, 26: 445-455.
• Clessin, S. 1874. Die Gruppe Fruticicola Held des Genus Helix L. Studien über Helix-Gruppe Fruticicola Held. Jahrbücher der Deutschen Malakozoologischen Gesellschaft, 1:177-194, 305-336.
• Cook, L. M. and A. J. Cain. 1980. Population dynamics, shell size and morph frequency in experimental populations of the snail Cepaea nemoralis (L.). Biological Journal of the Linnean Society, 14: 259-292.
• Cowie, R. H. 1984. Density, dispersal and neighbourhood size in the land snail Theba pisana. Heredity, 52: 391-401.
• Cucherat, X. and S. Demuynck. 2006. Catalogue annoté des Gastéropodes terrestres (Mollusca, Gastropoda) de la région Nord - Pas-de-Calais. MalaCo, 2: 40-91.
• Čejka, T. 2000. The striking record of the land snail Trichia striolata danubialis (CLESSIN, 1874) (Gastropoda, Hygromiidae) in the Žilinská kotlina basin (Slovakia). Folia faunistica Slovaca, 5: 69-72.
• Čejka, T., Horsák, M. and D. Némethova. 2008. The composition and richness of Danubian floodplain forest land snail faunas in relation to forest type and flood frequency. Journal of Molluscan Studies, 74: 37-45.
• Davison, A. and B. C. Clarke. 2000. History or current selection? A molecular analysis of area effects in Cepaea nemoralis. Proceedings of the Royal Society of London Series B-Biological Sciences, 267:1399-1405.
• Duda, M., Sattmann, H., Haring, E., Bartel, D., Winkler, H., Harl, J. and L. Kruckenhauser. 2011. Genetic differentiation and shell morphology of Trochulus oreinos (Wagner, 1915) and T. hispidus (Linnaeus, 1758) (Pulmonata: Hygromiidae) in the northeastern Alps. Journal of MoEuscan Studies, 77: 30-40.
• Duda, M., Kruckenhauser, L., Sattmann, H., Harl, J., Jaksch, K. and E. Haring. 2014. Differentiation in the Trochulus hispidus complex and related taxa (Gastropoda, Pulmonata, Hygromiidae): morphology, ecology and their context to phylogeography. Journal of Molluscan Studies, 80: 371-387.
• Ehrmann, P. 1933. Mollusken (Weichtiere), pp. 1-264. In: P. Brohmer, P. Ehrmann and G. Ulmer (eds). Die Tierwelt Mitteleuropas. Vol. 2, Quelle and Meyer, Leipzig.
• Ellis, E. A. 1969. British Snails, 2nd ed. Clarendon Press, Oxford. 298 pp.
• Engelhard, G. H. and J. W. F. Silk. 1994. On altitude dependent characters in Albinaria idaea (L. Pfeiffer, 1849), with a revision of the species (Gastropoda: Pulmonata: Clausiliidae). Zoologische Mededelingen, 68: 21-38.
• Falkner, G. 1990. Binnenmollusken, pp. 112-280. In: R. Fetcher and G. Falkner (eds). Weichtiere Europäische Meeresund Binnenmollusken, Steinbachs Naturführer. Mosaik Verlag, München.
• Falkner, G., R. A. Bank and v. T. Proschwitz. 2001. CLECOM- PROJECT: Check-list of the non-marine Molluscan species-group taxa of the states of northern, Atlantic and central Europe (CLECOM I). Heldia, 4: 1-76.
• Falkner, G., T. E. J. Ripken and M. Falkner. 2002. Mollusques continentaux de la France: Liste de Reference annotee et Bibliographie. Museum national d'Histoire naturelle, Paris. 350 pp.
• Falling Rain Genomics Inc. 1996-2010. Data accessed October 2013 from: http://www.fallingrain.com.
• Fischer, K. and K. Fiedler. 2002. Reaction norms for age and size at maturity in response to temperature: A test of the compound interest hypothesis. Evolutionary Ecology, 16: 333-349.
• Forcart, L. 1965. New researches on Trichia hispida (Linnaeus) and related forms. Proceedings of the first European Malacological Congress, 1962: 79-93.
• Germain, L. 1930. Mollusques terrestres et fluviatiles (première partie). Faune de France, 21. Paul Lechevalier, Paris, 477 pp.
• Geyer, D. 1913. Über einige Schnecken aus dem Diluvium und ihre Bedeutung für die Ermittlung des Klimas. Jahresbericht und Mitteilungen des Oberrheinischen Geologischen Vereins (N.F.), 3: 98-112.
• Greyer, D. 1914. Über die Molluskenfauna des Salzkammergutes und ihre Beziehungen zum Diluvium in Schwaben. Verhandlungen der Kaiserlich-Königlichen Zoologisch- Botanischen Gesellschaft in Wien, 64: 270-289.
• Giokas, S., Páll-Gergely, B and O. Mettouris. 2014. Nonrandom variation of morphological traits across environmental gradients in a land snail. Evolutionary Ecology, 28: 323-340.
• Gittenberger, E., W. H. Piel and D. Groenenberg. 2004. The Pleistocene glaciations and the evolutionary history of the polytypic snail species Arianta arbustorum (Gastropoda, Pulmonata, Helicidae). Molecular Phylogenetic and Evolution, 30: 64-73.
• Goodfriend, G. A. 1986. Variation in Land-snail Shell form and Size and its Causes: a Review. Systematic Biology, 35: 204-223.
• Gould, S. J. and D. S. Woodruff. 1990. History as a cause of area effects: an illustration from Cerion on Great Inagua, Bahamas. Biological Journal of the Linnean Society, 40: 67-98.
• Haase, M., Misof, B., Wirth, T., Baminger, H. and B. Baur. 2003. Mitochondrial differentiation in a polymorphic land snail: evidence for Pleistocene survival within the boundaries of permafrost. Journal of Evolutionary Biology, 16: 415-428.
• Hausdorf, B. 2003. Latitudinal and altitudinal body size variation among north-west European land snail species. Global Ecology and Biogeography, 12: 389-394.
• Hazel, W. N. and M. S. Johnson. 1990. Microhabitat choice and polymorphism in the land snail Theba pisana (Muller). Heredity, 65: 449-454.
• Heller, J. 1981. Visual versus climatic selection of shell banding in the landsnail Theba pisana in Israel. Journal of Zoology, 194: 85-101.
• Heller, J. and M. Gadot. 1987. Convergence in the shell-banding polymorphism of two sympatric landsnails. Biological Journal of the Linnean Society, 30:163-179.
• Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. and A. Jarvis. 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25: 1965-1978.
• Honěk, A. 1993. Melanism in the land snail Helicella candicans (Gastropoda, Helicidae) and its possible adaptive significance. Malacologia, 35: 79-87.
• Hudec, V. 1964. Über die Verbreitung der Schnecke Trichia striolata (C. Pfeiff.) in der Südwestslowakei. Zoologické listy, 13: 265-268.
• Kerney, M. P., Cameron, R. A. D. and J. H. Jungbluth. 1983. Die Landschnecken Nord- und Mitteleuropas. Paul Parey, Hamburg und Berlin, 384 pp.
• Klemm, W. 1974. Die Verbreitung der rezenten Land- Gehäuse- Schnecken in Österreich. Denkschriften der Österreichischen Akademie der Wissenschaften, 117: 1-503.
• Kotsakiozi, P., Rigal, F., Valakos, E. D. and A. Parmakelis. 2013. Disentangling the effects of intraspecies variability, phylogeny, space, and climate on the evolution of shell morphology in endemic Greek land snails of the genus Codringtonia. Biological Journal of the Linnean Society, 110: 796-813.
• Körner, C. 2007. The use of 'altitude' in ecological research. Trends in Ecology and Evolution, 22: 569-574.
• Kruckenhauser, L., Duda, M., Bartel, D., Sattmann, H., Harl, J., Kirchner, S. and E. Haring. 2014. Paraphyly and budding speciation in the hairy snail (Pulmonata, Hygromiidae). Zoologica Scripta, 43: 273-288.
• Lazaridou-Dimitriadou, M., Karakousis, Y. and A. Staiku. 1994. Geographical variation in shell morphology and isoenzymes of Helix aspersa Mueller, 1774 (Gastropoda, Pulmonata), the edible land snail, from Greece and Cyprus. Heredity, 72: 23-35.
• Legendre, P. and L. Legendre. 1998. Numerical ecology, 2nd ed. Amsterdam: Elsevier, 853 pp.
• Lewis, G. 1977. Polymorphism and selection in Cochlicella acuta. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences, 276: 399-451.
• Lisický, M. J. 1991. Mollusca Slovenska. VEDA vydavatel'stvo Slovenskej akadémie vied, Bratislava, 344 pp.
• Locard, A 1888. Contributions à la faune malacologique française. XII. Études critiques sur les Helix du groupe de l'Hélix rufescens Pennant (Helix striolata, H. rufescens, H. montana, H. cœlata, H. circinata, H. clandestina). Annales de la Société Linnéenne de Lyon (Nouvelle Série), 34: 309-370.
• Locard, A. 1894. Conchyliologie française. Les coquilles terrestres de France. Description des familles, genres et espèces. Avec 515 figures dessinées d'après nature et intercalées dans le texte. Baillière, Paris, 370 pp.
• Madec, L., Desbuquois, C. and M. Coutellec-Vreto. A. 2000. Phenotypic plasticity in reproductive traits: importance in the life-history of the land snail Helix aspersa in a recently colonized habitat. Biological Journal of the Linnean Society, 69: 25-39.
• Mahler, F. 1952. Trichia montana (Studer) im Lande Salzburg. Archiv für Molluskenkunde, 81: 33-38.
• Meiri, S. 2011. Bergmann's Rule - what's in a name? Global Ecology and Biogeography, 20: 203-207.
• Meteorological Office. 2013. Data accessed October 2013 from: http://www.metoffice.gov.uk/climate/uk/regionaJ/.
• Moorkens, E. and M. C. D. Speight. 2001. The CLECOM project Ust of Irish non-marine Mollusca. Bulletin of the Irish biogeographical Society, 25: 95-104.
• Mulvey, M., Newman, M. C. and A N. Beeby. 1996. Genetic and conchological comparison of snails (Helix aspersa) differing in shell deposition of lead. Journal of Molluscan Studies, 62: 213-223.
• Naggs, F. 1985. Some preliminary results of morphometric multivariate analysis of the Trichia (Pulmonata: Helicidae) species groups in Britain. Journal of Natural History, 19:1217-1230.
• Nekola, J. C., Barker, G. M., Cameron, R. A. D. and B. M. Pokryszko. 2013. Latitudinal variation of body size in land snail populations and communities, pp. 62-82. In: F. Smith and K. Lyons (eds). Animal Body Size: Linking Pattern and Process across Space, Time, and Taxonomie Group. University of Chicago Press, Chicago.
• O'Brien, S. J. and E. Mayr. 1991. Bureaucratic mischief: recognizing species and subspecies. Science, 251: 1187-1188.
• Örstan, A. 2001. A revision of Mastus carneolus (Mousson 1863) from Istanbul, Turkey. Schriften zur Malakozoologie, 17: 65-70.
• Örstan, A. 2003. Calculation of the coefficient of variation from the diameter measurements of snail shells. Triton, 8: 31-32.
• Örstan, A. and M. Z. Yildirim. 2003. Conchological and genitalie comparisons of Jaminia loewii populations in Turkey. Zoology in the Middle East, 28: 67-76.
• Perrin, N., Honsberger, P. and A. Pontet. 1984. Approche biochimique et morphologique des espèces du genre Trichia (Helicidae, Gastropoda) de Suisse occidentale. Revue Suisse de Zoologie, 91: 483-495.
• Pfeiffer, C. 1828. Naturgeschichte deutscher Land- und Süsswasser-Mollusken. Dritte Abtheilung, Weimar, 84 pp.
• Pfeiffer, K. L. 1949. Levantina spiriplana (Olivier). Archiv für Molluskenkunde, 77: 1-51.
• Pfenninger, M. and F. Magnin. 2001. Phenotypic evolution and hidden speciation in Candidula unifasciata ssp. (Heli- cellinae, Gastropoda) inferred by 16S variation and quantitative shell traits. Molecular Ecology, 10: 2541-2554.
• Pfenninger, M., Bahl, A. and B. Streit. 1996. Isolation by distance in a population of a small land snail Trochoidea geyeri: evidence from direct and indirect methods. Proceedings of the Royal Society of London Series B-Biologi- cal Sciences, 263:1211-1217.
• Proćków, M. 2009. The genus Trochulus Chemnitz, 1786 (Gastropoda: Pulmonata: Hygromiidae) - a taxonomie revision. Folia Malacologica, 7: 101-176.
• Proćków, M., Kuźnik-Kowalska, E. and M. Lewandowska. 2012. Differences in population dynamics olBradybaena fruticum (O. F. Müller, 1774) (Gastropoda: Pulmonata: Bradybaenidae) in a submontane and lowland area of Poland. Animal Biology, 62: 451-462.
• Proćków, M., Drvotová, M., Juřičková, L. and E. Kuźnik- Kowalska. 2013a. Field and laboratory studies on the lifecycle, growth and feeding preference in the hairy snail Trochulus hispidus (L., 1758) (Gastropoda: Pulmonata: Hygromiidae). Biologia, 68:131-141.
• Proćków, M., Mackiewicz, P. and J. Pieńkowska. R. 2013b. Genetic and morphological studies of species status for poorly known endemic Trochulus phorochaetius (Bourguignat, 1864) (Gastropoda: Pulmonata: Hygromiidae), and its comparison with closely related taxa. Zoological Journal of the Linnean Society, 169: 124-143.
• Proćków, M., Strzała, T., Kuźnik-Kowalska, E. and P. Mackiewicz. 2014. Morphological similarity and molecular divergence of Trochulus striolatus and T. montanus, and their relationship to sympatric congeners (Gastropoda: Pulmonata: Hygromiidae). Systematics and Biodiversity, 12: 366-384.
• Proćków, M., Kuźnik-Kowalska, E. and P. Mackiewicz. In press. Phenotypic plasticity can explain evolution of sympatric polymorphism in the hairy snail Trochulus hispidas (Linnaeus, 1758). Current Zoology, doi: 10.1093/cz/ zow082.
• Proćków, M., Strzała, T., Kuźnik-Kowalska, E., Proćków, J. and P. Mackiewicz. 2017. Ongoing Speciation and Gene Flow between Taxonomically Challenging Trochulus Species Complex (Gastropoda: Hygromiidae). PLoS ONE, 12(1): e0170460.
• Puzin, C., Leroy, B. and J. Pétillon. 2014. Intra- and inter-specific variation in size and habitus of two sibling spider species (Araneae, Lycosidae): taxonomie and biogeo- graphic insights from sampling across Europe. Biological Journal of the Linnean Society, 113: 85-96.
• Rötzer, T. and F.-M. Chmielewski. 2001. Phenological maps of Europe. Climate Research, 8: 249-257.
• Ruggiero, A. and T. Kitzberger. 2004. Environmental correlates of mammal species richness in South America: effects of spatial structure, taxonomy and geographic range. Ecography, 27: 401-416.
• Schileyko, A. A 1978. On the systematics of Trichia s. lat. Malacologia, 17:1-56.
• Shelomi, M. 2012. Where are we now? Bergmann's Rule sensu lato in insects. American Naturalist, 180: 511-519.
• Sulikowska-Drozd, A. 2001. Shell variability in Vestia turgida (Rossmässler, 1836) along an altitudinal gradient. Folia Malacologica, 9: 73-81.
• Sulikowska-Drozd, A 2011. Population dynamics of the Carpathian clausiliid Vestia gulo (E. A. Bielz 1859) (Pulmonata: Clausiliidae) under various climatic conditions. Journal of Conchology, 40: 462-470.
• Taylor, J. W. 1916. Monograph of the land and freshwater Mollusca of the British Isles, Part 22. Taylor Bros, Leeds, 160 pp.
• Umiński, T. 1975. Life cycles in some Vitrinidae (Mollusca, Gastropoda) from Poland. Annales Zoologici, 33: 17-33.
• Viazzo, P. P. 1989. Upland Communities: Environment, Population and Social Structure in the Alps since the Sixteenth Century. Cambridge University Press, Cambridge, 325 pp.
• Welter-Schultes, F. W. 2000a. Spatial analysis of shell parameters suggests low species number of Mastus (Gastropoda: Pulmonata: Enidae) in central and eastern Crete. Folia Malacologica, 8: 151-160.
• Welter-Schultes, F. W. 2000b. The pattern of geographical and altitudinal variation in the land snail Albinaria idaea from Crete (Gastropoda: Clausiliidae). Biological Journal of the Linnean Society, 71: 237-250.
• Welter-Schultes, F. W. 2012. European non-marine molluscs, a guide for species identification. Planet Poster Editions, Göttingen, 679 pp.

Identyfikatory

DOI

10.3161/00034541ANZ2017.67.2.002