The find of six species new to Belgium highlights the role of the stone trade as a pathway for non-native land snails (Gastropoda: Stylommatophora)

Authors

  • Louis Bronne Natagora (NPO), Traverse des Muses 1, 5000 Namur, Belgium
  • Johann Delcourt University of Liège, Department of Biology, Ecology and Evolution, Service of Behavioural Biology, Institut de Zoologie (I1), Quai Van Beneden 22, B-4020 Liège, Belgium

DOI:

https://doi.org/10.26496/bjz.2024.116

Keywords:

non-native species, first record, stone yard, invasive species

Abstract

Surveys in stone yards in Wallonia (southern Belgium) led to the find of six taxa of land snails being new to Belgium and one being new to Wallonia. The new taxa can be divided into two groups: living animals of the European species Charpentieria itala, Laciniaria plicata, Chilostoma cingulatum, and Theba pisana, and shells with remains of the dead animals in the case of the Asian taxa Cathaica fasciola, Acusta sp., and Bradybaena jourdyi. The latter are widespread in their respective Asian native range while Acusta sp. and B. jourdyi had never been reported from Europe. We discuss the role of stone yards as hubs for the dispersion of land snails. The individuals of the newly observed taxa may have arrived in several waves (with successive arrivals of stones) and may not reproduce in the stone yard. We explore the risks of settling. In this study, we provide evidence that the doorsnails C. itala and L. plicata have already settled elsewhere in Wallonia. Theba pisana, C. fasciola and Acusta sp. have the potential to behave as invasive

References

ADAM W. (1947). Révision des mollusques de la Belgique I. Mollusques terrestres et dulcicoles. Musée royal d’histoire naturelle de Belgique, Bruxelles.

ALMEIDA M.N. & BESSA E.C. DE A. (2001). Estudo do crescimento e da reprodução de Bradybaena similaris (Férussac) (Mollusca, Xanthonychidae) em laboratório. Revista brasileira de zoologia 18: 1115–1122.

BAKER G.H. (2002). Helicidae and Hygromiidae as pests in cereal crops and pastures in South Australia. In: BARKER G.M. (ed.) Molluscs as Crop Pests: 193–215. CAB International, Wallingford. https://doi.org/10.1079/9780851993201.0193

BARTLOW A. & AGOSTA S. (2021). Phoresy in animals: review and synthesis of a common but understudied mode of dispersal. Biological Reviews 96: 223–246. https://doi.org/10.1111/brv.12654

BAUFELD P., SCHRADER G. & STEINMÖLLER S. (2018). Express-Risikoanalyse zu Cathaica fasciola. Journal für Kulturpflanzen 70: 163–165.

BAUR B. & BAUR A. (2017). Reproductive strategies in stylommatophoran gastropods. In: SALEUDDIN S. & MUKAI S. (eds) Physiology of Molluscs: a Collection of Selected Reviews, Volume 2: 311–377. Apple Academic Press, Waretown, New Jersey.

BECK H., ZIMMERMANN N., MCVICAR T., VERGOPOLAN N., BERG A. & WOOD E. (2018). Present and future Köppen-Geiger climate classification maps at 1-km resolution. Scientific Data 5: 180214. https://doi.org/10.1038/sdata.2018.214

BICHAIN J.-M., HOMMAY G. & LAMAND F. (2023). Liste de référence annotée et actualisée des mollusques continentaux du Grand Est (France). Bulletin de la Société d’Histoire naturelle et d’Ethnographie de Colmar 79: 13–41.

BOURGUIGNAT J.R. (1877). Histoire des Clausilies de France, vivantes et fossiles. Annales des Sciences Naturelles (Zoologie) 5: 1–50.

BRONNE L. & DELCOURT J. (2022). The snail Morlina glabra (Gastropoda: Oxychilidae), although previously unreported, is widespread throughout Belgium and at least present in the Netherlands and Luxembourg. Journal of Conchology 44: 267–275.

CAPINHA C., ESSL F., SEEBENS H., MOSER D., & PEREIRA H.M. (2015). The dispersal of alien species redefines biogeography in the Anthropocene. Science 348: 1248–1251. https://doi.org/10.1126/science.aaa8913

CHEN X. (2009). Self-fertilization and cross-fertilization in the land snail Arianta arbustorum (Mollusca, Pulmonata: Helicidae). Journal of Zoology 232: 465–471. https://doi.org/10.1111/j.1469-7998.1994.tb01587.x

COWIE R. (2022). Theba pisana (White Garden Snail). CABI Compendium. CABI International. https://doi.org/10.1079/cabicompendium.62094

COWIE R. & ROBINSON D.G. (2003). Pathways of introduction of nonindigenous land and freshwater snails and slugs. In: CARLTON J. (ed.) Invasive Species: Vectors and Management Strategies: 93–122. Island Press, Washington DC, USA.

COWIE R., DILLON R.T., ROBINSON D.G. & SMITH J.W. (2009). Alien non-marine snails and slugs of priority quarantine importance in the United States: A preliminary risk assessment. American Malacological Bulletin 27: 113–122. https://doi.org/10.4003/006.027.0210

DAFF (2022). National Hitchhiker (Contaminating) Plant Pest Action Plan 2022–2032. Department of Agriculture, Fisheries and Forestry, Canberra. Available from https://www.agriculture.gov.au/biosecurity-trade/pests-diseases-weeds/plant/national-action-plans [accessed 15 September 2022].

DÄUMER C., GREVE C., HUTTERER R., MISOF B. & HAASE M. (2012). Phylogeography of an invasive land snail: natural range expansion versus anthropogenic dispersal in Theba pisana pisana. Biological Invasions 14: 1665–1682. https://doi.org/10.1007/s10530-012-0179-z

DELCOURT J. (2022). L’ornithochorie des mollusques ou la dispersion des limaces et escargots par les oiseaux. Aves 59: 51–69.

DE-NIU C., GUO-QING Z., WENXIAN X., MAN-SHENG W., YANHONG L., XINGMIN C. & JIQING W. (2002). Bradybaena ravida (Benson) in cereal-cotton rotations of Jingyang County, Shaanxi Province, China. In: BARKER G.M. (ed.) Molluscs as Crop Pests: 315–324. CAB International, Wallingford. https://doi.org/10.1079/9780851993201.0315

DEVRIESE R., WARMOES T. & VERCOUTERE B. (1997). Land- en zoetwatermollusken van de Benelux. Uitgave van de Jeugdbond voor Natuurstudie en Milieubescherming, Gent. (3e druk), 192 p.

DE WILDE J., MARQUET R. & VAN GOETHEM, J. (1986). Voorlopige atlas van de landslakken van België /Atlas provisoire des gastéropodes terrestres de la Belgique. Koninklijk Belgisch Instituut voor Natuurwetenschappen / Institut royal des Sciences naturelles de Belgique, Brussels.

DÖRGE N., WALTHER C., BEINLICH B. & PLACHTER H. (1999). The significance of passive transport for dispersal in terrestrial snails (Gastropoda, Pulmonata). Zeitschrift für Ökologie und Naturschutz 8: 1–10.

DVOŘÁK L. (2016). Two new records of Laciniaria plicata (Draparnaud, 1801) from western Bohemia (Gastropoda: Clausiliidae). Malacologica Bohemoslovaca 15: 1–2. https://doi.org/10.5817/MaB2016-15-1

DVOŘÁK L.D. & KUPKA J. (2007). The first outdoor find of an American snail Zonitoides arboreus (Say, 1816) from the Czech Republic. Malacologica Bohemoslovaca 6: 1–2.

EPPO (2023). Theba pisana. https://gd.eppo.int/taxon/THEBPI/distribution [accessed on 19 October 2023].

ETA K. & HAUSDORF B. (2019). Chilostoma cingulatum (Studer, 1820) und Cornu aspersum (O.F. Müller, 1774) in Hamburg (Gastropoda: Helicidae). Mitteilungen der Deutschen Malakozoologischen Gesellschaft 100: 13–16.

FALIŃSKI J. (1972). Anthropochory in xerothermic grasslands in the light of experimental data. Acta Societatis Botanicorum Poloniae 3: 357–368. https://doi.org/10.5586/asbp.1972.028

FISCHER S., POSCHLOD P. & BEINLICH B. (1996). Experimental studies on the dispersal of plants and animals on sheep in calcareous grasslands. Journal of Applied Ecology 63: 1206–1221. https://doi.org/10.2307/2404699

FISCHER W. (2020). Beiträge zur Kenntnis der österreichischen Molluskenfauna. LXX. Bemerkungen zu Neufunden von eingeschleppten Schnecken im Norden Wiens und dem südlichen Marchfeld. Nachrichtenblatt der Ersten Vorarlberger Malakologischen Gesellschaft 27: 29–32.

FISCHER W. & REISCHÜTZ P. (2010). Beiträge zur Kenntnis der österreichischen Molluskenfauna XIX. Es kam nicht nur der Marmor nach Wien – Biodiversität auf dem Gelände eines ehemaligen Steinmetzbetriebes. Nachrichtenblatt der Ersten Vorarlberger Malakologischen Gesellschaft 17: 9–12.

GARGOMINY O. (2022). TAXREF. Version 4.9. UMS PatriNat (OFB-CNRS-MNHN), Paris. Checklist dataset. https://doi.org/10.15468/vqueam

GBIF (2023a). GBIF Laciniaria plicata Available from https://doi.org/10.15468/dl.2qm4nd [accessed on 25 February 2023].

GBIF (2023b). GBIF Bradybaena jourdyi Available from https://doi.org/10.15468/dl.v85ad2 [accessed on 25 February 2023].

GHEOCA V., BENEDEK A.M. & SCHNEIDER E. (2023). Taxonomic and functional diversity of land snails reflects habitat complexity in riparian forests. Scientific Reports 13: 9808. https://doi.org/10.1038/s41598-023-36896-6

GROENENBERG D.S.J., SUBAI P. & GITTENBERGER E. (2016). Systematics of Ariantinae (Gastropoda, Pulmonata, Helicidae), a new approach to an old problem. Contributions to Zoology 85: 37–65. https:/doi.org/10.1163/18759866-08501003

HAUSDORF B. (2023). Distribution pattern of established alien land snail species in the Western Palaearctic Region. NeoBiota 81: 1–32. https://doi.org/10.3897/neobiota.81.96360

HEY P., UMBRECHT K. & BICHAIN J.-M. (2017). Présence de la Clausilie septentrionale Alinda biplicata biplicata (Montagu, 1803) (Mollusca: Gastropoda, Clausiliidae) en milieu urbain (Strasbourg, Bas-Rhin). Bulletin de la Société d’Histoire naturelle et d’Ethnographie de Colmar 74: 35–39.

HOÀNG NGỌC K., TRẦN T. & NGUYỄN THANH B. (2021). Species composition of land snails in ban thi and Xuan Lac commune belong to Nam Xuan Lac species and landscape conservation area, Cho Don district, Bac Kan province. Scientific Journal of Tan Trao University 6: 111–118. https://doi.org/10.51453/2354-1431/2020/390

HORSÁK M., ŠTEFFEK J., ČEJKA T., LOŽEK V. & JUŘIČKOVÁ L. (2009). Occurrence of Lucilla scintilla (R.T. Lowe, 1852) and Lucilla singleyana (Pilsbry, 1890) in the Czech and Slovak Republics – with remarks how to distinguish these two non-native minute snails. Malacologica Bohemoslovaca 8: 24–27.

HOSTIE E. (1935). Helix pisana, Müll. en Belgique. Les Naturalistes belges 16: 24.

HULME P.E., BACHER S., KENIS M., KLOTZ S., KÜHN I., MINCHIN D., NENTWIG W., OLENIN S., PANOV V., PERGL J., PYŠEK P., ROQUES A., SOL D., SOLARZ W. & VILÀ M. (2008). Grasping at the routes of biological invasions: a frame-work for integrating pathways into policy. Journal of Applied Ecology 45: 403–414. https://doi.org/10.1111/j.1365-2664.2007.01442.x

HWANG C.C., ZHOU W.-C., GER M.-J., GUO Y., QIAN Z.-X., WANG Y.-C., TSAI C.-L. & WU S.-P., (2021). Biogeography of land snail genus Acusta (Gastropoda: Camaenidae): Diversification on East Asian islands. Molecular Phylogenetics and Evolution 155: e106999. https://doi.org/10.1016/j.ympev.2020.106999

INKHAVILAY K., SUTCHARIT C., BANTAOWONG U., CHANABUN R., SIRIWUT W., SRISONCHAI R., PHOLYOTHA A., JIRAPATRASILP P. & PANHA S. (2019). Annotated checklist of the terrestrial molluscs from Laos (Mollusca, Gastropoda). ZooKeys 834: 1–166. https://doi.org/10.3897/zookeys.834.28800

JANSEN B. (2015). Veldgids Slakken en Mossels. KNNV Uitgeverij, Zeist.

JONES K.H. & PRESTON H.B. (1910). Notes on some species of Mollusca collected in China from 1904 to 1907, with descriptions of new species. Journal of Molluscan Studies 9: 9–12. https://doi.org/10.1093/oxfordjournals.mollus.a066312

KAYEYE J., KABALE B., CISHIBANJI P., MASHIMANGO J. & BAJOPE J. (2014). A preliminary survey and distribution of land snails of Katana region, southern Kivu, Democratic Republic of Congo. International Journal of Innovation and Scientific Research 9: 212-224.

KHẮC H.N., NHƯỢNG Đ.V., CẬY N.T. & NHẤT T.T. (2012). Landsnails (Gastropoda) in Tam Dao national park, Vinh Phuc province, Vietnam. Vietnam Journal of Biology 34: 317–322. https://doi.org/10.15625/0866-7160/v34n3.2462

KOBIALKA H., SCHWER H. & KAPPES H. (2009). Rote Liste der gefährdeten Schnecken und Muscheln (Mollusca: Gastropoda et Bivalvia) in Nordrhein-Westfalen. 3. Fassung 2009. Mitteilungen der Deutschen Malakozoologischen Gesellschaft 82: 3–30.

KOLENDA K., NAJBAR A., KUŚMIEREK N. & MALTZ T. (2017). A possible phoretic relationship between snails and amphibians. Folia Malacologica 25: 281-285. https://doi.org/10.12657/folmal.025.019

KWITT S. & PATZNER R. (2019). Nachweise von Charpentieria itala (Martens, 1824) in Salzburg (Gastropoda, Clausiliidae). Linzer biologische Beiträge 51: 1115–1118.

LANGERAERT W. (2021). An exploratory study on the patterns of mtDNA and phenotypic variation in the introduced land snail Theba pisana (O.F. Müller, 1774) in Belgium (Gastropoda: Eupulmonata: Helicidae). MSc Thesis, UGhent. Available from https://lib.ugent.be/catalog/rug01:003014802 [accessed on 10 January 2023].

MALTZ L. & SULIKOWSKA-DROZD A. (2014). Selfing and brooding in Alinda biplicata (Gastropoda: Pulmonata: Clausiliidae) – life history traits of a good coloniser. Animal Biology 64: 97–113. https://doi.org/10.1163/15707563-00002434

MEISSNER H., LEMAY A., BERTONE C., SCHWARTZBURG K., FERGUSON L. & NEWTON L. (2009). Evaluation of Pathways for Exotic Plant Pest Movement into and within the Greater Caribbean Region. Caribbean Invasive Species Working Group (CISWG) and United States Department of Agriculture (USDA), Center for Plant Health Science and Technology (CPHST), Plant Epidemiology and Risk Analysis Laboratory (PERAL).

MICHALAK P.S. & PRICE T. (2010). New Pest Response Guidelines. Temperate Terrestrial Gastropods. U.S. Department of Agriculture.

MNHN (2022). Collections of the Musée National d’Histoire Naturelle, online galery. Available from https://science.mnhn.fr/institution/mnhn/collection/im/item/search [accessed 19 October 2022].

MOLLUSCABASE (eds) (2022). MolluscaBase. Chilostoma cingulatum (S. Studer, 1820). Available from http://www.molluscabase.org/aphia.php?p=taxdetails&id=871135 [accessed 18 May 2022].

MORLET L. (1886). Diagnoses Molluscorum novorum Tonkini. Journal de Conchyliologie. 34: 75–78. Available from https://www.biodiversitylibrary.org/page/16070966 [accessed 19 October 2022].

NAIQIN W., FENGJIANG L. & ROUSSEAU D.-D. (2018). Terrestrial mollusk records from Chinese loess sequences and changes in the East Asian monsoonal environment. Journal of Asian Earth Sciences 155: 35–48.

NMR (2022). Collections of the Natural History Museum Rotterdam, online gallery. Available from https://nmr-pics.nl [accessed 19 October 2022].

PÁLL-GERGELY B., SÁRVÁRI F., TŐKÉSI N. & FEHÉR Z. (2020). Chilostoma (Cingulifera) cingulatum (S. Studer, 1820) (Gastropoda: Pulmonata: Helicidae) new to the fauna of Hungary. Soosiana 34: 12–17. https://doi.org/10.5281/zenodo.3701569

PELTANOVÁ A., PETRUSEK A., KMENT P. & JUŘIČKOVÁ L. (2012). A fast snail’s pace: colonization of Central Europe by Mediterranean gastropods. Biological Invasions 14: 759–764. https://doi.org/10.1007/s10530-011-0121-9

PHILIPPI R.A. (1847). Abbildungen und Beschreibungen neuer oder wenig gekannter Conchylien. Zweiter Band. Fischer, Cassel.

POPPE G. & POPPE P. (2022). Conchology.be. Available from https://conchology.be [accessed 5 May 2022].

PROĆKÓW M., KONOWALIK K. & PROĆKÓW J. (2019). Contrasting effects of climate change on the European and global potential distributions of two Mediterranean helicoid terrestrial gastropods. Regional Environmental Change 19: 2637–2650. https://doi.org/10.1007/s10113-019-01573-w

RÉGNIER C., ACHAZ G., LAMBERT A., COWIE R.H., BOUCHET P. & FONTAINE B. (2015). Mass extinction in poorly known taxa. Proceedings of the National Academy of Sciences 112:7761-6. https://doi.org/10.1073/pnas.1502350112

RICHLING I. & VON PROSCHWITZ T. (2021). Identification problems of travelling snail species — new exotic introductions to tropical greenhouses in Gothenburg, Sweden (Gastropoda: Achatinellidae, Strobilopsidae, Helicarionidae). PeerJ 9: e11185. https://doi.org/10.7717/peerj.11185

ROSENBAUER A. (2011). Vorkommen südeuropäischer Schneckenarten in Steinmetzbetrieben. Mitteilungen der Deutschen Malakozoologischen Gesellschaft 85: 27–34.

ROWSON B., TURNER J., ANDERSON R. & SYMONDSON B. (2014). Slugs of Britain and Ireland. FSC, Telford.

SCHILEYKO A. (2011). Check-list of land pulmonate molluscs of Vietnam (Gastropoda: Stylommatophora). Ruthenica 21: 1–68.

SCHMID G. (2000). Die Große Felsenschnecke Chilostoma cingulatum (Studer) an Buntsandsteinmauern in Nordschwarzwald. Carolinea 58: 149–154.

SCHMID G. (2002). In Baden-Württemberg eingeschleppte oder ausgesetzte Mollusken. Jahreshefte der Gesellschaft für Naturkunde in Württemberg 158: 253–302. https://doi/org/10.26251/jhgfn.158.2002.253-302

SEEBENS H., BLACKBURN T.M., DYER E.E., GENOVESI P., HULME P.E. et al. (2017). No saturation in the accumulation of alien species worldwide. Nature Communications 8: 14435. https://doi.org/10.1038/ncomms14435

SULIKOWSKA-DROZD A. (2005). Distribution and habitat preferences of clausiliids (Gastropoda: Pulmonata: Clausiliidae) in the eastern part of the Polish Carpathians. Folia Malacologica 13: 49–94. https://doi.org/10.12657/folmal.013.007

SULIKOWSKA-DROZD A., HIRANO T., WU S.-P. & PÁLL-GERGELY B. (2018). High fecundity, rapid development and selfing ability in three species of viviparous land snails Phaedusinae (Gastropoda: Stylommatophora: Clausiliidae) from East Asia. Zoological Studies 57: 38. https://doi.org/10.6620/ZS.2018.57-38

VAN DEN NEUCKER T. & RONSMANS J. (2015). The globally invasive Paralaoma servilis (Gastropoda: Punctidae) reported for the first time in Belgium. Journal of Conchology 421: 95-96.

VAN GOETHEM J. (1988). Nouvelle liste commentée des Mollusques récents non marins de Belgique. Document de travail de l’Institut royal des Sciences naturelles de Belgique 53: 1–69.

VENDETTI J., SANDIG K., SAHAKYAN A. & GRANADOS A. (2021). Multiple introductions of the pestiferous land snail Theba pisana (Müller, 1774) (Gastropoda: Helicidae) in Southern California. Insects 12: 662. https://doi.org/10.3390/insects12080662

VILVENS C., MARÉE B., MEULEMANS E., ALEXANDRE M., WAIENGNIER E. & VALTAT S. (2008). Mollusques terrestres et dulcicoles de Belgique. Tome I : Gastéropodes terrestres à coquille (1ère partie). Société belge de Malacologie, Jodoigne.

WELTER-SCHULTES F. W. (2012). European Non-Marine Molluscs, a Guide for Species Identification. Planet Poster Editions, Göttingen.

WIESE V. (2014). Die Landschnecken Deutschlands: Finden – Erkennen – Bestimmen. Quelle & Meyer, Leipzig.

ZHANG M.-Z., DU Y.-L., QIN X.-C., ZHAO Y.-J., WANG J.-Z. & ZHANG Z.-Y. (2015). Study on the behaviour of dormancy breaking in Cathaica fasciola (Draparnaud 1801) (Gastropoda: Stylommatophora). Molluscan Research 35: 213–217. https://doi.org/10.1080/13235818.2015.1044886

Downloads

Published

2024-01-24

How to Cite

Bronne, L., & Delcourt, J. (2024). The find of six species new to Belgium highlights the role of the stone trade as a pathway for non-native land snails (Gastropoda: Stylommatophora). Belgian Journal of Zoology, 154, 11–30. https://doi.org/10.26496/bjz.2024.116

Issue

Section

Articles