First records of the terrestrial slug Arion ater s. l. (Linnaeus, 1758) (Pulmonata: Arionidae) from Turkey

Heike Reise, e-mail: Heike.Reise@senckenberg.de

Senckenberg Museum of Natural History Görlitz, Am Museum 1, 02826 Görlitz, Germany

Zeynel Arslangündoğdu, e-mail: zeynel@istanbul.edu.tr

Istanbul University Cerrahpasa, Forestry Faculty, Department of Forest Entomology and Protection, Bahçeköy, 34473 Istanbul, Turkey

Bettina Schlitt, e-mail: Bettina.Schlitt@senckenberg.de

Senckenberg Museum of Natural History Görlitz, Am Museum 1, 02826 Görlitz, Germany

John M. C. Hutchinson, e-mail: majmch@googlemail.com; John.Hutchinson@senckenberg.de

Senckenberg Museum of Natural History Görlitz, Am Museum 1, 02826 Görlitz, Germany

Erdem Hızal, e-mail: hizal@istanbul.edu.tr

Istanbul University Cerrahpasa, Forestry Faculty, Department of Forest Entomology and Protection, Bahçeköy, 34473 Istanbul, Turkey

Ergün Bacak, e-mail: ergun.bacak@istanbul.edu.tr

Istanbul University Cerrahpasa, Vocational High School of Forestry, Forestry Department, Bahçeköy, 34473 Istanbul, Turkey
Abstract

A strong population of the terrestrial slug Arion ater s. l. is reported from the European and Asian parts of Istanbul, Turkey. This is the first confirmed report of this large, conspicuous taxon from Turkey and from Asia. Our samples from five synanthropic sites indicate that it is already well established. Partial sequences of the mitochondrial COI gene (cytochrome c oxidase subunit I) place the Turkish slugs in a small clade shared with a few specimens from western France, perhaps indicating the origin of the Istanbul population. The next closest haplotypes (9% difference) fall within the clade identified as Arion ater s. s. This fits with the genital morphology of the Turkish slugs, which is most similar to the ater-form of A. ater s. l. Our discovery also puts a new light on the recent report of the highly invasive pest slug Arion lusitanicus auct. non Mabille, 1868 (often called Arion vulgaris Moquin-Tandon, 1855) in Isparta, which was identified only on the basis of external morphology. As reliable morphological distinction of these two species requires examination of the genital anatomy, the specimen from Isparta should be reinvestigated.

Key words
invasive species; Arion lusitanicus; Arion vulgaris; Arion rufus; Istanbul
References

Balashov I. 2018. Case 3685 – Arion vulgaris Moquin-Tandon, 1855 (Gastropoda, Stylommatophora, Arion­idae): proposed validation of the specific name as available. Bulletin of Zoological Nomenclature 75: 12–15. https://doi.org/10.21805/bzn.v75.a006
Carlisle T. R. 2015. Chocolate Arion (Arion rufus). Avail­able online at https://www.inaturalist.org/­observations/2342095 (accessed 12 November 2018).
Chevallier H. 1972. Arionidae (Mollusca, Pulmonata) des Alpes et du Jura français. Haliotis 2: 7–23.
Chevallier H. 1974. Les grands Arion de France (Mollusca, Pulmonata). Taxonomie, biogeographie, écologie, polymorphisme, croissance et cycle biologique. Doctoral thesis, Université de Paris.
Damjanov S. G., Likharev I. M. 1975. Fauna na B’lgarija. 4. Gastropoda terrestria. Bulgarian Academy of Scien­ces, Sofia.
Dreijers E., Reise H., Hutchinson J. M. C. 2013. Mating of the slugs Arion lusitanicus auct. non Mabille and A. rufus (L.): different genitalia and mating behaviours are incomplete barriers to interspecific sperm exchange. Journal of Molluscan Studies 79: 51–63. https://doi.org/10.1093/mollus/eys033
Fehér Z., Eröss Z. P. 2009. Checklist of the Albanian mollusc fauna. Schriften zur Malakozoologie 25: 22–38.
Folmer O., Black M., Hoeh W., Lutz R., Vrijenhoek R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.
Forsyth R. G. 2004. Royal BC Museum handbook: land snails of British Columbia. Royal BC Museum, Victoria, Canada.
Godan D. 1979. Schadschnecken und ihre Bekämpfung. Ulmer, Stuttgart.
Hatteland B. A., Roth S., Andersen A., Kaasa K., Støa B., Solhøy T. 2013. Distribution and spread of the invasive slug Arion vulgaris Moquin-Tandon in Norway. Fauna norvegica 32: 13–26.
Hatteland B. A., Solhøy T., Schander C., Skage M., von Proschwitz T., Noble L. R. 2015. Introgression and differentiation of the invasive slug Arion vulgaris from native A. ater. Malacologia 58: 303–321. https://doi.org/10.4002/040.058.0210
Irikov A., Eröss Z. 2008. An updated and annotated checklist of Bulgarian terrestrial gastropods (Mollusca: Gastropoda). Folia Malacologica 16: 197–205. https://doi.org/10.12657/folmal.016.015
Likharev I. M., Wiktor A. J. 1980. Slizni fauny SSSR i sopredelnykh stran (Gastropoda terrestria nuda). Fauna SSSR (Novaja serija 122) 3 (5): 1–437. Academy of Sciences, Zoological Institute, Leningrad.
Oshanova N. 1968. Zur Verbreitung der Arionidae in Bulgarien (Gastropoda). Malakologische Abhandlungen Staatliches Museum für Tierkunde Dresden 2: 235–241.
Păpureanu A.-M., Reise H., Varga A. 2014. First records of the invasive slug Arion lusitanicus auct. non Mabille (Gastropoda: Pulmonata: Arionidae) in Romania. Malacologica Bohemoslovaca 13: 6–11. http://mollusca.sav.sk/pdf/13/13.Papureanu.pdf
Peláez M. L., Valdecasas A. G., Martinez D., Horreo J. L. 2018. Towards the unravelling of the slug A. ­ater–A. rufus complex (Gastropoda Arionidae): new genetic approaches. Web Ecology 18: 115–119. https://doi.org/10.5194/we-18-115-2018
Pfenninger M., Weigand A., Bálint M., Klussmann-Kolb A. 2014. Misperceived invasion: the Lusitanian slug (Arion lusitanicus auct. non-Mabille or Arion vulga­ris Moquin-Tandon 1855) is native to Central Europe. Evolutionary Applications 7: 702–713. https://doi.org/10.1111/eva.12177
Pilsbry H. A. 1948. Land Mollusca of North America (north of Mexico). Vol. II, Part 2. Academy of Natural Sciences of Philadelphia, Philadelphia, i–xlvii, 521–1113.
Pintér L., Suara R. 2004. A magyarországi puhatestűek elterjedése II. Hungarian Museum of Natural History, Budapest.
QGIS Development Team 2017. QGIS Geographic Information System. Open Source Geospatial Foun­dation Project. Available online at https://www.osgeo.org/projects/qgis/ (accessed 2017).
Rabitsch W. 2006. DAISIE Arion vulgaris (Moquin-Tandon, 1855) Fact Sheet. Online Database of Delivering Alien Invasive Species Inventories for Europe. Available online at http://www.europe-aliens.org/­speciesTheWorst.do (accessed 05 November 2018).
Reischütz A., Reischütz P. L. 2007. Rote Liste der Weichtiere (Mollusca) Österreichs. In: Zulka K. P. (ed.). Rote Listen gefährdeter Tiere Österreichs. Teil 2: Kriechtiere, Lurche, Fische, Nachtfalter, Weichtiere. Grüne Reihe des Lebensministeriums 14/2: 363–433.
Reise H., Schwarzer A.-K., Hutchinson J. M. C., Schlitt B. 2017. Co-occurrence and hybridisation of three morphotypes of Arion rufus and A. ater in Eastern Saxony, Germany. In: Ćmiel A. M., Lipińska A., Zając K., Zając T., Cameron R. A. D. (eds): EUROMAL, 8th European Congress of Malacological Societies, 10–14 September 2017, Kraków, Poland, Book of Abstracts, Bogucki Wydawnictwo Naukowe: 82.
Rowson B. 2017. Arion rufus. The IUCN Red List of Threatened Species 2017: e.T171016A1320066.
Rowson B., Anderson R., Turner J. A., Symondson W. O. C. 2014a. The slugs of Britain and Ireland: undetected and undescribed species increase a well-studied, economically important fauna by more than 20%. PLoS ONE. 9: e91907. https://doi.org/10.1371/journal.pone.0091907
Rowson B., Turner J., Anderson R., Symondson B. 2014b. Slugs of Britain and Ireland. Identification, understanding and control. Field Studies Council, Telford /National Museum of Wales, Cardiff.
Rudzīte M., Dreijers E., Ozolina-Moll L., Parele E., Pilāte D., Rudzītis M., Stalažs A. 2010. Latvijas gliemji: sugu noteicējs. A guide to the molluscs of Latvia. LU Akadēmiskais apgāds, Rīga.
Rüetschi J., Stucki P., Müller P., Vicentini H., Claude F. 2012. Rote Liste Weichtiere (Schnecken und Muscheln). Gefährdete Arten der Schweiz, Stand 2010. Bundesamt für Umwelt, Bern und Schweizer Zentrum für die Kartographie der Fauna, Neuenburg. Umwelt-Vollzug Nr. 1216. https://www.bafu.admin.ch/bafu/de/home/themen/biodiversitaet/publikationen-studien/publikationen/rote-liste-weichtiere.html
von Proschwitz T. 1997. Arion lusitanicus Mabille and A. rufus (L.) in Sweden: a comparison of occurrence, spread and naturalization of two alien slug species. Heldia 4: 137–138.
Welter-Schultes F. W. 2012. European non-marine molluscs, a guide for species identification. Planet Poster Editions, Göttingen.
Wiese V. 2014. Die Landschnecken Deutschlands. Quelle & Meyer, Wiebelsheim.
Wiktor A. 1973. Die Nacktschnecken Polens. Arionidae, Milacidae, Limacidae (Gastropoda, Stylommatophora). Monografie Fauny Polski 1. Polish Academy of Sciences, Warsaw, Krakow.
Wiktor A. 1996. The slugs of the former Yugoslavia (Gastropoda terrestia nuda – Arionidae, Milacidae, Li­macidae, Agriolimacidae). Annales Zoologici 46: 1–110. http://rcin.org.pl/dlibra/docmetadata?id=57707
Winnepenninckx B., Backeljau T., De Wachter R. 1993. Extraction of high molecular weight DNA from molluscs. Trends in Genetics 9: 407. https://doi.org/10.1016/0168-9525(93)90102-N
Yıldırım M. Z., Gürlek M. E. 2017. Türkiye Karasal Gastropod Faunası için Yeni Kayıt: Arion vulgaris Moquin-Tandon 1855 (Gastropoda: Pulmonata: Arionidae). Mehmet Akif Ersoy Üniversitesi Fen Bilimleri Enstitüsü Dergisi 8 (Ek Sayı 1): 228–230.
Yıldırım M. Z., Kebapçı Ü. 2004. Arion (Mesarion) subfuscus (Draparnaud, 1805) a new record of the malacofauna of Turkey. Israel Journal of Zoology 49: 318–319.
Zemanova M. A., Knop E., Heckel G. 2016. Phylogeographic past and invasive presence of Arion pest slugs in Europe. Molecular Ecology 25: 5747–5764. https://doi.org/10.1111/mec.13860
Zemanova M. A., Knop E., Heckel G. 2017. Introgressive replacement of natives by invading Arion pest slugs. Scientific Reports 7: 14908. https://doi.org/10.1038/s41598-017-14619-y
Zemanova M. A., Broennimann O., Guisan A., Knop E., Heckel G. 2018. Slimy invasion: climate niche and current and future biogeography of Arion slug invaders. Diversity and Distributions 24: 1627–1640. https://doi.org/10.1111/ddi.12789

Folia Malacologica (2018) 26: 213-220
First published on-line: 2018-12-11 00:00:00
https://doi.org/10.12657/folmal.026.024
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