Paropeas achatinaceum (Pfeiffer, 1846) and Other Alien Subulinine and Opeatine Land Snails in European Greenhouses (, )

Authors: Horsák, Michal, Naggs, Fred, and Backeljau, Thierry Source: Malacologia, 63(1) : 123-130 Published By: Institute of Malacology URL: https://doi.org/10.4002/040.063.0112

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PAROPEAS ACHATINACEUM (PFEIFFER, 1846) AND OTHER ALIEN SUBULININE AND OPEATINE LAND SNAILS IN EUROPEAN GREENHOUSES (GASTROPODA, ACHATINIDAE)

Michal Horsák1*, Fred Naggs2 & Thierry Backeljau3,4

ABSTRACT

Land snails of the family Achatinidae, subfamilies Subulininae and Opeatinae, are commonly reported as alien species in European greenhouses, where they often reach high densities. These introduced species usually have tropical cosmopolitan distributions. Four of them (Opeas hannense, Allopeas clavulinum, Subulina octona, and S. striatella) are commonly reported and illustrated from greenhouses across Europe. A fifth species, Allopeas gracile, has also been reported from Europe, though from a few records only. In this paper, we report on a European colony of a sixth species, Paropeas achatinaceum, that was discovered in Austria in 2016. We provide photographic documentation for these six species with critical characters to distinguish them. In the past, at least five other alien nominal subulinine spe- cies have been reported from greenhouses in Europe. These are briefly discussed along with nomenclatural notes.

Introduction families Subulininae and Opeatinae (previously included in the Subulinidae), are commonly Biological invasions are one of the greatest reported from European greenhouses where environmental and economic threats, often re- they often reach high densities. The groups sponsible for biodiversity loss and local extinc- have a primarily tropical cosmopolitan distribu- tions (Canning-Clode, 2015). There are many tion with over 1,300 described species (Naggs, pathways for alien species introductions, and 1994). Four of these species are commonly re- these differ among taxonomic groups. Land ported and illustrated from greenhouses across snails are often introduced unintentionally, for Europe (e.g., Kerney et al., 1983; Anderson, instance in soil, with plant material, attached 2005; von Proschwitz, 2005; Kobialka et al., to vehicles, and shipped in containers. Due to 2006; Olenin & Didziulis, 2009; Horsák et al., the enormous diversity of land snails (> 35,000 2013; Naggs et al., 2015; Horsák et al., 2019). species worldwide; Barker, 2001), local biolo- These are: (i) Opeas hannense (Rang, 1831) [= gists cannot be expected to be familiar with Opeas goodallii (Miller, 1822) = Opeas pumilum species from other parts of the world, (Pfeiffer, 1840)], (ii) Allopeas clavulinum (Potiez and there is often limited information on the & Michaud, 1838) [see Kadolsky (2012) for the indigenous local snail fauna. Thus, many alien explanation for keeping 1838, instead of 1835, species may remain undetected and/or errone- as the publication year], (iii) Subulina octona ously identified for a long time (e.g., Naggs, (Bruguière, 1789), and (iv) Subulina striatella 2004; Naggs & Raheem, 2005), even though (Rang, 1831) [= Striosubulina striatella (Rang, they may pose severe economic and environ- 1831), as suggested by MolluscaBase, al- mental threats (Pimentel et al., 2000). Many though Raheem et al. (2014: 117) point out that alien land snail species have been reported the reproductive anatomy of S. octona closely from greenhouses (e.g., Flasar & Kroupová, resembles that of S. striatella, thus implicitly 1976; Leiss & Reischütz, 1996; Albrecht & questioning the genus level distinction between Meng, 1997; Horsák et al., 2004; Cameron, these two species]. A fifth species, Allopeas 2016). Species of the family Achatinidae, sub- gracile (Hutton, 1834), has been reported from

1Department of Botany and Zoology, Masaryk University, Kotlářská 2, CZ-611 37 Brno, Czech Republic. 2Mollusca Group, Invertebrates Division, Department of Life Sciences, The Natural History Museum, London SW7 5BD, U.K. 3Royal Belgian Institute of Natural Sciences, OD Taxonomy and Phylogeny, Vautierstraat 29, 1000 Brussels, Belgium. 4University of Antwerp, Evolutionary Ecology Group, Universiteitsplein 1, 2610 Antwerp, Belgium. *Corresponding author: [email protected] 123

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Europe, too, although only rarely and without shells. We also review published records of all any photographic documentation (but see other alien Subulininae hitherto reported from Naggs et al., 2015). Europe. Because the taxonomy and nomen- We here report on a viable colony of an- clature of the Subulininae remain a source of other subulinine species, non-native in Europe, considerable confusion and disagreement, Paropeas achatinaceum (Pfeiffer, 1846) [=Al - we provide nomenclatural comments when lopeas javanicum (Reeve, 1849), also placed appropriate. in Prosopeas or Lamellaxis], that has been discovered in Austria. Because several spe- cies of Subulininae and Opeatinae have been RESULTS AND DISCUSSION recognized as successful invaders in many parts of the world (Pilsbry, 1946; Cowie, 1997; Paropeas achatinaceum was recorded in Vi- Robinson & Slapcinsky, 2005), it is important to enna Zoo (Tiergarten Schönbrunn) on 27 Feb- report any introductions into a new continent, ruary 2016 (M. Horsák leg.), 11 live specimens as recorded here. This information is also es- were collected from a large population in the sential for updating and revising the “EASIN rainforest pavilion (48°10’52.5”N, 16°18’21.7”E) – European Alien Species Information Net- along with Subulina octona. Paropeas achatina- work” database (https://easin.jrc.ec.europa.eu/ ceum has a high-turreted, yellowish to brownish easin) (Katsanevakis et al., 2012) and its older shell (Fig. 1a, b), in general reaching up to 15 relatives, “NOBANIS – North European and mm in height and 5 mm in width (Cowie et al., Baltic Network for Invasive species” (https:// 2017). Adult shells have a soft silky or waxen www.nobanis.org/) and “DAISIE – Delivering lustre, hardly or not transparent, with a distinct Alien Invasive Species Inventories for Europe” vertical striation, which in fresh specimens ap- (Olenin & Didziulis, 2009). We provide notes pear as thread-like ribs. Full-grown shells have on how to distinguish the above-mentioned up to 8–9 whorls, the last whorl occupying about 1 six species that have been recorded recently /3 of the shell length. While the native area of from Europe, along with photographs of their this species is unclear (even if its type locality

FIG. 1. Subulinine and opeatine species (Achatinidae: Subulininae, Opeatinae) repeatedly recorded in European greenhouses along with Paropeas achatinaceum recorded for the first time. a, b:P. acha- tinaceum (Vienna, Austria); a = 11.5 mm x 3.5 mm, b = 8.9 x 3.2; c: Allopeas gracile (London, United Kindom; copyright NHMUK, used with permission), 10.2 x 3.3; d: Allopeas clavulinum (Brno, Czech Republic), 6.9 x 2.4; e: Opeas hannense (Olomouc, Czech Republic), 5.1 x 1.9; f: Subulina octona (Prague, Czech Republic), 13.1 x 3.6; g: Subulina striatella (Prague, Czech Republic), 12.5 x 4.1. The shells of Subulina octona and S. striatella are immature to illustrate the size and shape differences better as adult shells reach heights of 18–25 mm.

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is in Java), it is widely distributed and common and more bulbous than in the other species in disturbed habitats around the Indo-Pacific (Fig. 1f, g). However, this size difference can region (Fig. 2; Naggs, 1994). It was established be deceiving as both reach sexual maturity and in the Hawaiian Islands prior to 1904 (Cowie, start reproducing before reaching two thirds 1997); additional early Pacific records were or less of their full shell length (Pilsbry, 1946; provided by Brook (2010). It was first detected D’ávila et al., 2018). in Florida in 2001, where it probably arrived on Given the great species diversity of the Subu- plant material imported from tropical regions. lininae and the ease by which many of these Subsequently, in 2002–2003, several well-es- species are transported via commerce, more tablished populations were discovered, mostly species may be expected to reach Europe. associated with horticultural plants (Robinson In fact, at least five other nominal species, & Slapcinsky, 2005), representing the first additional to the six mentioned above, have penetration inland on any major landmass. The been reported from greenhouses in Europe. species reproductive anatomy was described These are briefly discussed below. We also in detail by Naggs (1994). summarize all European records of A. gracile Paropeas achatinaceum has been confused because in Europe this species is known from with A. clavulinum, but the shell of the latter only a few records. This is in contrast to the is far more glossy and, when fresh, far more remaining five subulinines and opeatines that transparent (Fig. 1b, d; see also Naggs, 1994). are well established and common in European Moreover, A. clavulinum has almost no shell greenhouses. sculpture, whereas P. achatinaceum shows Allopeas gracile (Hutton, 1834) was de- distinct vertical striations. Paropeas achati- scribed from India, but Neck (1976) and naceum can also be confused with A. gracile Auffenberg & Stange (1988) suggested that but differs in having a less lanceolate, that its origin was in South America. However, later is, more turreted, shell shape with a notably archaeological and palaeontological evidence higher body whorl and a more distinct striation suggested its origin in the Old World tropics (Fig. 1b, c). Paropeas achatinaceum grows (Christensen & Weisler, 2013). It has been in- much larger than O. hannense and has a less troduced widely across tropical and subtropical regular striation. In fact, O. hannense can be areas of Asia, Australia, Polynesia, Central and easily distinguished from the other species South America, including many islands in the dealt with here by the backward curve of the Caribbean region, and much of southeastern edge of the aperture where it joins the suture U.S.A. (e.g., Dundee, 1971; Cowie, 1997; Neu- (indicated at Fig. 1e by an arrow; compare with bert, 1998; Robinson, 1999; Boyko & Cordeiro, Fig. 1c). Both S. octona and S. striatella grow 2001; Capinera, 2017). However, surprisingly, much larger, and their apices are much larger only a few records have been published from

FIG. 2. The current distribution of Paropeas achatinaceum adapted from the Global Biodiversity Infor- mation Facility (GBIF, 2019) and the on-line database of the Museum of Florida (Discover Life 2019b). The white cross shows the European record mentioned in the text.

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Europe. It seems that the first record ever made b; Schmidt, 1959). Although the taxonomic sta- in Europe was by L. Dawes in 1917 in England tus of A. mauritianum is very confused, some (Headington Hill gardens, Oxford). Eleven authors have treated it, or at least listed it, as empty shells are deposited in the NHMUK J. a separate species (e.g. Baker, 1945; Cowie, W. Taylor Collection (Accession number 2130). 1997; Burke 2013). Others suggest placing it Originally identified asOpeas goodallii (Miller) in the synonymy of A. clavulinum (e.g., Griffiths they were subsequently identified asA. gracile & Florens, 2006) or actually do so either for A. by Naggs (1990a). The first published record mauritianum overall (e.g., von Proschwitz, 1994; was made in Germany (Botanischen Garten using the erroneous spellings “mauritanum” and Berlin-Dahlem) by Jaeckel & Plate (1967). This “mauritanus”) or for A. mauritianum auct. non record was also cited by Kerney et al. (1983) Pfeiffer, 1853 more specifically (e.g., Kerney and probably was the basis for including A. et al., 1983; Waldén, 1985; Leiss & Reischütz, gracile (as Lamellaxis gracilis) in the DAISIE 1996) [but see Gittenberger & Van Bruggen list of alien species in Europe (Olenin & Didzi- (2013) regarding this synonymy]. Even the ulis, 2009). Subsequently, more records were publication year of the original description of published in the early 2010s from several Pfeiffer’s Bulimus mauritianus is a source of places in Austria (Reischütz, 2012; Reischütz confusion because the literature mentions 1847 et al., 2012, 2018) and England (Preece & (e.g., Griffiths & Florens, 2006), 1852 (e.g., White, 2012). Da Sois (2015) reported in his Burke, 2013), 1853 (e.g., MolluscaBase), and undergraduate thesis a record of Lamellaxis cf. 1854 (e.g., Cowie, 1997). We follow - gracilis (Hutton, 1834) from one of the green- Base in using 1853 as publication year since houses of the Hortus Botanicus in Leiden, Pfeiffer’s “original” description ofB. mauritianus The Netherlands. Two European records of in the Proceedings of the Zoological Society A. gracile reported on the Discover Life map of London, 1852, Part XX, p. 150, was effec- (Discover Life, 2019a) were wrongly attributed tively only published in 1854 (Waterhouse in as they were from overseas territories, that is, Duncan, 1937), that is, one year after Pfeiffer’s Bermuda for England, and the Loyalty Islands “subsequent” description of this species in the of New Caledonia for France (confirmed by Systematisches Conchylien-Cabinet von Martini John Slapcinsky in litt., 18 October 2019). It ap- und Chemnitz, 1(13) p. 86 no. 99, in 1853 (Coan pears that the species is spreading in Europe, & Kabat, 2015). We also follow MolluscaBase although the extent to which it may have been in regarding A. mauritianum (Pfeiffer, 1853) as overlooked and/or misidentified in the past is a junior synonym of A. clavulinum (Potiez & unknown. In addition, A. gracile (Hutton, 1834) Michaud, 1838), because the three syntypes of may be a species complex (e.g., Gittenberger Bulimus mauritianus Pfeiffer, 1853, are identical & Van Bruggen, 2013), whose taxonomy may to A. clavulinum (Budha et al., 2015; but with be further complicated by the fact that some erroneous reference to one, instead of three subulinines can reproduce uniparentally (e.g., syntypes, see Naggs, 1990b). Schmidt, 1959; Ev. Marcus & Er. Marcus, 1968; Leptinaria unilamellata (d’Orbigny, 1838), de Almeida Bessa & de Barros Araújo, 1995; native to tropical South America, was recently de Almeida & de Almeida Bessa, 2001; Pilate observed in the rainforest house of the science et al., 2013), including A. gracile (e.g., Biswas center Universeum, Göteborg, Sweden, where et al., 1976; Subba Rao et al., 1980; Capinera, it is now extinct after having survived from 2004 2017). Therefore, some populations may con- to 2014 (von Proschwitz, 2016). The name He- sist of clones or homozygous strains, for which lix unilamellata d’Orbigny, 1838, is here used, the biological species concept may be difficult because the older Helix unilamellata d’Orbigny, to apply (e.g., Prévot et al., 2013). 1835 is a nomen nudum (Delannoye et. al., Allopeas mauritianum ( Pfeiffer, 1853), a spe- 2015; von Proschwitz, 2017). Von Proschwitz cies described from the island of Mauritius, was (2017) suggested that this species should be reported from several greenhouses in the Neth- referred to as Leptinaria lamellata (Potiez & erlands (Meeuse & Hubert, 1949), the botanical Michaud, 1835). However, as it is not clear if gardens in Belfast, U.K. (Meeuse & Hubert, Achatina lamellata Potiez & Michaud, 1835, is 1949), the “pálmház” (palmhouse) in the zoo of conspecific with Helix unilamellata d’Orbigny, Budapest, Hungary (Pintér & Suara, 2004), and 1838, and as the exact publication year of Potiez the greenhouses of both the Botanischer Garten & Michaud’s A. lamellata is still debated (see in Rostock and the Palmengarten in Frankfurt Falkner et al., 2002; Kadolsky, 2012), we use the am Main, Germany (Plate & Frömming, 1953a, name L. unilamellata (d’Orbigny, 1838).

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Leptinaria urichi (Smith, 1896), a species ACKNOWLEDGEMENTS described from Trinidad, was reported from Kew Gardens in London (Tomlin, 1916), the We are grateful to John Slapcinsky (Florida Cambridge Botanic Garden (Brindley, 1904), Museum of Natural History, Gainesville, and the Royal Botanical Garden, Edinburgh U.S.A.) for his investigation of the two mis- (Baker, 1945). However, the status of this placed European records of A. gracile and taxon is still unclear; it has been treated as a Jonathan Ablett (The Natural History Museum, separate species (e.g., Robinson et al., 2011; London, U.K.) for sending collection data Rutherford, 2014), whereas Baker (1945) sus- about the A. gracile record from Oxford. Peter pected it to be synonymous with A. clavulinum. Reischütz (Horn, Austria) provided literature Some authors accepted this latter synonymy on A. gracile in Austria. Brigitte Segers (Royal without further comments (Kerney et al., 1983; Belgian Institute of Natural Sciences, Brus- Waldén, 1985; both with the erroneous generic sels, Belgium) looked up subulinine material spelling Leptiniaria). in the Dautzenberg collection. Robert Cowie South American Allopeas micra (d’Orbigny, and one anonymous reviewer significantly 1835) was reported and illustrated from the improved this study with their comments and greenhouses of the Jardin des Plantes in Paris, recommendations on the earliest version of France [as Stenogyra octonoides (Adams, the manuscript. 1845)] (Dautzenberg, 1896; Dollfus et al., 1896), and without any reference or locality information, but with doubt by Eichler (1952). LITERATURE CITED Boettger (in Eichler, 1952) commented that reports of A. micra probably refer to A. cla- Albrecht, C. & S. Meng, 1997, Die Schnecken der vulinum, although 20 years before, Boettger Gewächshausanlagen des Erfurter Erwerbs- (1932) had referred to Dautzenberg (1896) gartenbaus (Mollusca: Gastropoda). Thüringer and Dollfus et al. (1896) for the records of A. Faunistische Abhandlungen, 4: 33–43. Anderson, R., 2005, An annotated list of the non- micra and O. pumilum [now O. hannense] in the marine Mollusca of Britain and Ireland. Journal greenhouses of the Jardin des Plantes in Paris. of Conchology, 38: 607–638. Nevertheless, based on Eichler (1952), Geiter Auffenberg, K. & L. A. Stange, 1988, The Subu- et al. (2002) included A. micra among the neo- linidae of Florida. Florida Department of Agricul- zoa of Germany, though with doubtful status. ture and Consumer Services, Division of Plant The species was also listed among alien spe- Industry, Entomology Circular, 305: 4 pp. cies in Europe in the DAISIE project (Olenin & Baker, H. B., 1945, Some American Achatinidae. The Nautilus, 58: 84–92. Didziulis, 2009). As far as we know, there are Barker, G. M., 2001, Gastropods on Land: Phy- no other records of A. micra in Europe. logeny, Diversity and Adaptive Morphology. beckianum (Pfeiffer, 1846), is Pp. 1–146, in: G. M. Barker, ed., The biology probably native to the Caribbean Basin and of terrestrial molluscs. CABI Publishing, United was reported from the port of Hamburg, Ger- Kingdom, 558 pp. many (Kraepelin, 1901, as Stenogyra caraca- Biswas, S. K., R. Rahmna & T. R. Mitra, 1976, Observations on the breeding habits of Opeas sensis Reeve) and from a greenhouse in York, gracile (Hutton) (Gastropoda: Subulinidae). U.K. (Jackson, 1926). Journal of Conchology, 29: 69–70. Finally, Dautzenberg (1896) and Dollfus et Boettger, C. R., 1932, Die Besiedlung neu ange- al. (1896) also published a record of another legter Warmhäuser durch Tiere. Ein Beitrag zur subulinine, under the name “Stenogyra (Spi- Frage der Bildung von Gewächshausfaunen. raxis) venusta Morelet”, from the greenhouses Zeitschrift für Morphologie und Ökologie der Tiere, 24: 394–407. of the Jardin des Plantes in Paris. However, C. Boyko, C. B. & J. R. Cordeiro, 2001, The ter- R. Boettger considered it unidentifiable with restrial Mollusca of Easter Island (Gastropoda, certainty, “probably a species belonging to ). Basteria, 65: 17–25. Opeas or Lamellaxis” (Eichler, 1952). Brindley, H. H., 1904, The Mollusca of Cam- Obviously, if the invasion biology of these bridgeshire. Pp. 114–138, in: J. E. Marr & A. E. subulinine species is to be better understood Shipley, eds., Handbook to the natural history of and monitored, then there is a need for a more Cambridgeshire. University Press, Cambridge, VIII + 260 pp. comprehensive taxonomic framework inte- Brook, F. J., 2010, Coastal landsnail fauna of grating not only shell morphology but internal Rarotonga, Cook Islands: systematics, diversity, anatomy, especially of the reproductive tract, biogeography, faunal history, and environmental and molecular data. influences. Tuhinga, 21: 161–252.

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