Arion rufus var. vulgaris Moquin-Tandon, 1855 Arion lusitanicus auct. non Mabille
The Spanish slug (Arion vulgaris, but formerly widely referred to as Arion lusitanicus owing to a misidentification) is an air-breathing land slug, a terrestrialpulmonategastropodmollusk in the family Arionidae, the roundback slugs. Other vernacular names are Lusitanian slug, Iberian slug, and killer slug.
It is a large, conspicuous slug, which has spread across much of Europe since the 1950s and now reached North America. It may attain high densities and be a serious horticultural and agricultural pest, and is considered an invasive species. The life cycle is annual, with adults appearing in summer and dying off before winter.
Confusion over nomenclature
The Spanish slug was identified as Arion lusitanicus when it was first reported as an invading species in France in 1956,[3] and hence it is sometimes called the Lusitanian slug (e.g.[4]). This was a case of misidentification. In slugs, it is often impossible to find external characters that distinguish closely related species using external features, as colouration can be quite variable, and the rather plastic anatomy makes diagnostic anatomical features difficult to establish. The current consensus is that the true Arion lusitanicus is a species of the western part of the Iberian Peninsula.[5][6] Examination of slugs from the Serra da Arrábida mountains in Portugal from where it was originally described by Jules François Mabille in 1868 showed that the true A. lusitanicus differed from the invader in its internal anatomy, the shape of the spermatophore and the number of chromosomes.[7][8]
The misidentification was first recognised in 1997,[5] and more widely publicised in an atlas of British molluscs.[9]Arion vulgaris was proposed as a substitute name[10] based on a drawing of the genitalia in an 1855 work by Alfred Moquin-Tandon.[2] However, it is debatable whether the name applies to this drawing, so one temporary solution was to use the name Arion lusitanicus auct. non Mabille (i.e. "as used by authors other than Mabille").[11] Nevertheless, A. vulgaris has increasingly been used since, and this is the proposal that has been formally submitted to the International Commission on Zoological Nomenclature.[12][13]
It has been erroneously reported that the slug was originally introduced via vegetables from Spain. These reports are usually based on outdated information published in pre-1999 literature. The common name "Spanish slug" was further based on the unsubstantiated assumption that the species would not only live in Portugal, but also in Spain. Arion vulgaris seems to be rare in Spain.[14] Another name sometimes applied is the "Iberian slug".
Distribution
The native distribution of Arion vulgaris is not exactly known. Genetic evidence (the higher incidence of rare alleles) suggests an origin in France or Spain,[14] contrary to earlier genetic analyses that did not adequately sample these regions.[4] In Britain the slug was first recorded in 1954,[9] which is not an indication of it being native there. It is presumed that the specimen illustrated in Moquin-Tandon's original 1855 description[2] was from France.
Non-indigenous distribution
The non-indigenous distribution of Arion vulgaris includes almost the whole of Western and Central Europe and extends to various parts of Southern, Northern and Eastern Europe.[15] The first confirmed Asian record was in 2022 from Armenia.[16] A 2017 report from the Asian part of Turkey was not based on dissection and is liable to be A. ater s.l.[17]Arion vulgaris is now also recorded from Canada (2009)[18][19] and Mexico.[20] Reports of "A. lusitanicus" from Madeira may be copied from an 1895 report,[21] in which case they need confirmation; similarly, a 1975 report from the Azores[22] could be of the true A. lusitanicus.[6] Claims of its presence in Algeria also appear unsupported.[23]
Chronological overview of expansion of Arion vulgaris in Europe:
Belarus – since 2020[52] (2018 record not confirmed anatomically)[47]
This species has not yet become established in the USA, but it is considered to represent a potentially serious threat as a pest, an invasive species which could negatively affect agriculture, natural ecosystems, human health or commerce. Therefore, it has been suggested that this species be given top national quarantine significance in the USA.[53]
British authorities were also concerned as of 2014 that it may become a major pest.[24][25]
Description
The size of the adult slug is 60–140 mm. The colour ranges from yellow to black, but is most commonly brick-red, dirty orange, or brown. The tentacles are darker. Adult A. vulgaris may not differ in external appearance from Arion rufus, and so reliable identification requires dissection to examine the genitalia. In contrast, the juveniles of these species can be distinguished because only A. vulgaris has longitudinal bands.[54] However, juveniles of other large Arion species such as Arion flagellus also have longitudinal bands.[55]
Reproductive system: The atrium is small. The adjacent part of the oviduct is dilated and muscular, with the same diameter as the atrium and containing a longitudinal ligula. This distinguishes A. vulgaris from Arion ater s.l., in which the oviduct is thinner and the atrium is larger and contains the ligula. Arion flagellus also has a ligula in the dilated part of the oviduct, but the ligula does not reach as far towards the atrium as in A. vulgaris. The spermatheca is spherical, its diameter twice that of the oviduct.[55][56]
Ecology
The habitat of Arion vulgaris includes all agricultural ecosystems, as well as natural environments such as river and lake margins, forest edges, forests in valleys or meadows. In Switzerland it has been found up to 1700 m altitude.[54]
It is a serious agricultural and horticultural pest in large parts of Europe, eating a cosmopolitan range of growing plant parts as well as decaying vegetation. Opportunistically it eats carrion, including squashed conspecifics. It is active mostly during the night and in wet weather during the day. Densities can reach 50 individuals per m2 or locally even higher.[57][58]
Whilst a slug can crawl several metres within a night,[58] long-distance dispersal is believed to be on vegetables, on horticultural seedlings, and on plant debris disposed of as waste.[57]
The species has an annual life cycle with mating starting in July and eggs first laid some weeks later in late summer. Clutches are laid on the soil surface or in crevices up to 10 cm underground, with an average clutch size of about 70 eggs; an adult slug typically lays about 400 eggs in its lifetime. The eggs hatch from autumn to spring. Neither eggs nor slugs can survive temperatures below ―3 °C, so overwinter survival depends on hiding under shelters.[59] Adults normally die off in autumn before winter frosts.[57]
As an invasive species
Arion vulgaris is considered among the 100 worst alien species in Europe in DAISIE European Invasive Alien Species Gateway,[15] and this is the only land gastropod among them.[15]Arion vulgaris is the worst slug pest in Europe[15] and it has an important economic, ecological, and social impact.[15]
The local name of the slug in the regions it has invaded is typically a translation of "Spanish slug". In recent years, as its dominance has increased, it has been nicknamed "killer slug",[60] perhaps due to its tendency to eat dead or weaker individuals of the species, although its destructive impact on gardens may seem just as appropriate a reason for the name.
Like other pulmonate snails and slugs, it is a hermaphrodite and this species has the capacity to self-fertilize,[61] so that one single slug can start an infestation. Long-distance transport of produce and garden plants has been assumed to be a common means of its rapid dispersal.
Besides causing economic damage, the arrival of A. vulgaris has often been associated with the disappearance within a few years of the similarly sized congener Arion ater s.l., at least in synanthropic habitats.[56] While the two species coexist they may mate with each other[62] and produce fertile offspring.[63] Hybrids are often identifiable by their intermediate genital anatomy.[56][64] It has been proposed that in Scandinavia crossing of A. vulgaris and the indigenous A. ater ater might have produced a more frost-resistant variety.[65] However, genetic investigations have not shown that introgression of A. ater genes into A. vulgaris persist for long once the native species has disappeared.[64] In the Swiss Alps, Arion ater rufus persists only at high elevations, and hybrids with A. vulgaris occur in a contact zone along the altitudinal gradient.[63]
Given the densities that A. vulgaris can attain, other ecological effects of its invasion on the native flora and fauna are to be expected. For instance, the seeds that it consumes are less likely to survive to germinate than with other gastropods with which it was compared.[66] In Sweden complete defoliation of native shrubs in natural woodland has been reported.[67]
^ abcMoquin-Tandon A. (1855). Histoire naturelle des mollusques terrestres et fluviatiles de la France contenant des études générales sur leur anatomie et leur physiologie et la description particulière des genres, des espèces et des variétés. Tome second. pp. 1-646, atlas 1-92, Pl. I-LIV [= 1-54]. Paris. (Baillière).
^ abvan Regteren Altena, C.O. (1956). "Notes sur les limaces, 3. Sur la présence en France d'Arion lusitanicus Mabille". Journal de Conchyliologie. 95: 89–99.
^ abCastillejo, J. (1997). "Las babosas de la familia Arionidae Gray, 1840 en la Península Ibérica e Islas Baleares. Morfología y distribución. (Gastropoda, Pulmonata, terrestria nuda)". Revista, Real Academia Galega de Ciencias. 16: 51–118.
^ abHolyoak, D.T.; Holyoak, G.A.; Mendes, R.M. da Costa (2019). "A revised check-list of the land and freshwater Mollusca (Gastropoda and Bivalvia) of mainland Portugal". Iberus. 37: 113–168.
^(in Spanish) Castillejo J. (1997). Babosas del Noroeste Ibérico. Universidade de Santiago de Compostela, Spain, 192 pp.
^Columba, M.; Backeljau, T.; Gregorini, A.; Jordaens, K. (2007). "Chromosome numbers and chromosomal evolution in the land snail genus Arion (Gastropoda, Pulmonata)". In Jordaens, K.; Van Houtte, N.; Van Goethem, J.; Backeljau, T. (eds.). World Congress of 390 Malacology, Antwerp, Belgium, 15–20 July 2007. Abstracts. Antwerp: Unitas Malacologica. p. 40.
^ abcKerney M. (1999). Atlas of the land and freshwater molluscs of Britain and Ireland. pp. 1-264. Colchester. (Harley).
^Falkner, G.; Ripken, T.E.J.; Falkner, M. (2002). Mollusques continentaux de France. Liste de référence annotée et bibliographie. Paris: Muséum national d’Histoire naturelle.
^Bank, R.A.; Falkner, G.; von Proschwitz, T. (2007). "CLECOM-Project: a revised checklist of the non-marine Mollusca of Britain and Ireland". Heldia. 5: 41–72.
^Balashov, Igor (May 2018). "Case 3685 — Arion vulgaris Moquin-Tandon, 1855 (Gastropoda, Stylommatophora, Arionidae): proposed validation of the specific name as available". The Bulletin of Zoological Nomenclature. 75: 12–15. doi:10.21805/bzn.v75.a006. ISSN0007-5167. S2CID90067777.
^Kadolsky, D.; Welter-Schultes, F.; Bank, R.A. (31 December 2018). "Comment (Case 3685) – Arion vulgaris Moquin-Tandon, 1855 (Gastropoda, Stylommatophora, Arionidae): modified proposal to preserve the specific name in its accustomed sense". The Bulletin of Zoological Nomenclature. 75 (1): 251. doi:10.21805/bzn.v75.a051. S2CID92607223.
^ abcZemanova, Miriam A.; Knop, Eva; Heckel, Gerald (November 2016). "Phylogeographic past and invasive presence of Arion pest slugs in Europe". Molecular Ecology. 25 (22): 5747–5764. doi:10.1111/mec.13860. PMID27664400. S2CID22971610.
^ abcdeDAISIE European Invasive Alien Species Gateway. Arion vulgaris. Last updated 30 October 2006, accessed 27 September 2009.
^Kraepelin, K. (1895). "Zoologische Ergebnisse einer Frühjahrs - Exkursion nach Madeira und den Canarischen Inseln". Verhandlungen des Naturwissenschaftlichen Vereins in Hamburg. 2: 6–17.
^Backhuys, W. (1975). Zoogeography and taxonomy of the land and freshwater molluscs of the Azores. Amsterdam: Backhuys and Meesters. ISBN9789004064478.
^Borredá, V.; Martínez-Ortí, A. (2017). "Contribution to the knowledge of the terrestrial slugs (Gastropoda, Pulmonata) of the Maghreb". Iberus. 35 (1): 1–10.
^Turner H., Kuiper J. G. J., Thew N., Bernasconi R., Rüetschi J., Wüthrich M. & Gosteli M. (1998). Fauna Helvetica 2. Atlas der Mollusken der Schweiz und Liechtensteins. pp. 1-527. Neuchâtel.
^Cesari, P. (1978). "Nota preliminare sulla diffusione in Italia e l'esplosione demografica nel Veneto di Arion lusitanicus Mabille". Lavori, Società veneziana di Scienze naturali. 3: 3–7.
^ abcdefghPăpureanu A.-M., Reise H. & Varga A. (2014). "First records of the invasive slug Arion lusitanicus auct. non Mabille (Gastropoda: Pulmonata: Arionidae) in Romania". Malacologica Bohemoslovaca13: 6-11. PDF
^Schmid, G. (1970). "Arion lusitanicus in Deutschland". Archiv für Molluskenkunde. 100: 95–102.
^(in German) Reischütz P. L. & Stojaspal F.J. (1971). "Bemerkenswerte Mollusken aus Ostösterreich" [Remarkable Mollusks from East Austria].Mitteilungen der zoologischen Gesellschaft Braunau 1/13: 339-344
^Risch, P.; Backeljau, T. (1989). "On the occurrence of Arion lusitanicus Mabille, 1868 in Belgium (Mollusca: Pulmonata)". Annalen van de Koninklijke Belgische Vereniging voor Dierkunde. 119 (1): 25–38.
^ abvon Proschwitz, T. (1992). "Spanska skogsnigeln - Arion lusitanicus Mabille - en art i snabb spridning med människan i Sverige". Göteborgs Naturhistoriska Museum, Årstryk. 1992: 35–42.
^Hatteland, B.A.; Roth, S.; Andersen, A.; Kaasa, K.; Støa, B.; Solhøy, T. (13 February 2013). "Distribution and spread of the invasive slug Arion vulgaris Moquin-Tandon in Norway". Fauna Norvegica. 32: 13–26. doi:10.5324/fn.v32i0.1473. hdl:1956/12402.
^de Winter, A.J. (1989). "Arion lusitanicus Mabille in Nederland (Gastropoda, Pulmonata, Arionidae)". Basteria. 53: 49–51.
^Quinteiro, J.; Rodriguez-Castro, J.; Castillejo, J.; Iglesias-Pineiro, J.; Rey-Mendez, M. (May 2005). "Phylogeny of slug species of the genus Arion: evidence of monophyly of Iberian endemics and of the existence of relict species in Pyrenean refuges". Journal of Zoological Systematics and Evolutionary Research. 43 (2): 139–148. doi:10.1111/j.1439-0469.2005.00307.x.
^Dvořák, L.; Horsák, M. (2003). "Současné poznatky o plzáku Arion lusitanicus (Mollusca: Pulmonata) v České republice". Časopis Slezského Muzea Opava (A). 52: 67–71.
^Bloch, Dorete (2003). "Morsnigilin ella hin spanski snigilin". Frøði. 1: 16–18.
^Vuksa, M.; Djedovic, S.; Stojnic, B. (2003). "IPM approach to control of the slug Arion lusitanicus Mabille – a new pest species in Serbia and Montenegro". In Dussart, GBJ (ed.). Slugs & snails: agricultural, veterinary & environmental perspectives. BCPC Symposium Proceedings No. 80. Alton, UK: British Crop Protection Council. pp. 147–152. ISBN1901396800.
^Stankovic, S.V.; Stojkoska, E.; Norris, A. (2006). "Annotated checklist of the terrestrial gastropods (Gastropoda) of the Republic of Macedonia". In Petkovski, S. (ed.). Anniversary Proceedings (1926–2006). Eighty years of achievement by the Macedonian Museum of Natural History. Skopje: Macedonian Museum of Natural History. pp. 43–55.
^Adomaitis, M.; Skujienė, G. (2016). "Invazinė šliužų rūšies Arion lusitanicus (Mabille, 1868) (Mollusca, Pulmonata, Arionidae) plitimo Lietuvoje perspektyvos". Lietuvos Biologinė: Būklė, Struktūra, and Apsauga. 4: 41–49.
^Cowie, R.H.; Dillon, R.T.; Robinson, D.G.; Smith, J.W. (July 2009). "Alien non-marine snails and slugs of priority quarantine importance in the United States: a preliminary risk assessment". American Malacological Bulletin. 27 (1–2): 113–132. doi:10.4003/006.027.0210. S2CID54919881.
^ abGrimm, B.; Schaumberger, K. (August 2002). "Daily activity of the pest slug Arion lusitanicus under laboratory conditions". Annals of Applied Biology. 141 (1): 35–44. doi:10.1111/j.1744-7348.2002.tb00193.x.
^Slotsbo, S.; Hansen, L.; Holmstrup, M. (February 2011). "Low temperature survival in different life stages of the Iberian slug, Arion lusitanicus". Cryobiology. 62 (1): 68–73. doi:10.1016/j.cryobiol.2010.12.005. PMID21168402.
^Hagnell, J.; von Proschwitz, T.; Schander, C. (2006). "Self-fertilising observed in the invasive Iberian slug Arion lusitanicus, Mabille 1868". Journal of Conchology. 39: 107.
^ abHutchinson, J.M.C.; Schlitt, B.; Reise, H. (6 September 2021). "One town's invasion by the pest slug Arion vulgaris (Gastropoda: Arionidae): microsatellites reveal little introgression from Arion ater and limited gene flow between infraspecific races in both species". Biological Journal of the Linnean Society. 134 (4): 835–850. doi:10.1093/biolinnean/blab082.
^Hagnell, J.; Schander, C; von Proschwitz, T. (2003). "Hybridisation of arionids: the rise of a super slug?". In Dussart, GBJ (ed.). Slugs & snails: agricultural, veterinary and environmental perspectives. Symposium Proceedings No. 80. Alton, UK: British Crop Protection Council. pp. 221–226.
^von Proschwitz, T. (1997). "Utbredning och spridning av spansk skogssnigel [Arion lusitanicus Mabille] och röd skogssnigel [Arion rufus (L.)] – en översikt av utvecklingen i Sverigerige. Göteborgs Naturhistoriska Museum, Årstryck". Göteborgs Naturhistoriska Museum, Årstryck. 1996: 27–45.
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