Five alien achatinid land snails (Gastropoda, Eupulmonata) first reported in greenhouses of Italian botanical gardens Author Manganelli, Giuseppe 0000-0002-8453-280X Dipartimento di Scienze Fisiche, della Terra e dell’Ambiente, Università di Siena, Via Mattioli 4, 53100 Siena, Italy & NBFC (National Biodiversity Future Center), Palermo, Italy Author Benocci, Andrea 0000-0003-3145-215X Museo di Storia Naturale dell’Accademia dei Fisiocritici, Piazzetta S. Gigli 2, 53100 Siena, Italy Author Barbato, Debora 0000-0003-1105-1711 Dipartimento di Scienze Fisiche, della Terra e dell’Ambiente, Università di Siena, Via Mattioli 4, 53100 Siena, Italy & NBFC (National Biodiversity Future Center), Palermo, Italy Author Giusti, Folco 0000-0001-8722-4653 Dipartimento di Scienze Fisiche, della Terra e dell’Ambiente, Università di Siena, Via Mattioli 4, 53100 Siena, Italy text ZooKeys 2024 2024-07-29 1208 99 132 journal article 300348 10.3897/zookeys.1208.119147 06a147da-4f99-4a61-9c8a-db99a7f99164 BEF04EEA-B9D0-4220-9BC4-84208488CCF2 Subulina octona ( Bruguière, 1789 ) Bulimus octonus Bruguière, 1789: 325 . Type locality: “ … dans les îles Antilles. M. de Badier l’a trouvé abondamment à l’île de la Guadeloupe , & j’en ai vu chez M. d’Antic qui lui ont été envoyés de l’île de Saint-Domingue ”. Type material: presumed lost ( Smith 1992 ). Material examined. Italy • 112 shells and 2 spirit specimens; Trento , Tropical greenhouse of the Science Museum of Trento ( MUSE ); 46 ° 03 ' 45.16 " N , 11 ° 06 ' 50.08 " E ; 04 Jan. 2019 ; 10 Feb. 2019 ; 04 May 2019 ; D. Barbato , G. Bolzonella leg.; GMC 51197 • 29 shells; same locality; 01 Feb. 2022 ; D. Barbato , A. Benocci leg.; GMC 51188 • 1 shell; same locality; 09 Feb. 2023 ; D. Barbato , A. Benocci leg.; GMC 57353 • 1 shell; Padua , Biodiversity Garden ( Botanical Garden of Padua ); 45 ° 23 ' 52.59 " N , 11 ° 52 ' 50.37 " E ; 06 Mar. 2019 ; D. Barbato leg.; GMC 57374 . Description. Shell (Figs 7 , 8 , 28–30 ). Shell dextral, medium in size, imperforate, elongate, slender, conical, rather robust, pearly off-white, glossy or waxy and sub-transparent when fresh, with 7–9 slightly convex whorls, separated by rather deep and in places irregularly crenulate sutures. Apex obtuse, rounded, and smooth; last whorl ~ 1 / 3 of shell height. Aperture small, ~ 1 / 5 of shell height, ovate, slightly prosocline. Peristome interrupted, not thickened or reflected, with callous rim on parietum and columella; columella concave and obliquely truncate at base; outer margin straight in lateral view. Protoconch smooth; teleoconch with fine, wrinkled, irregular collabral growth lines. Shell dimensions: SH 12.1–16.0 mm; SD 3.3–4.1 mm ; AH 2.5–3.2 mm ; AW 1.9–2.4 mm . Shells of Subulina octona from the tropical greenhouse of the Science Museum of Trento ( MUSE ), D. Barbato & G. Bolzonella leg. 04 Jan. 2019. Female distal genitalia (Fig. 31 ). Free oviduct very short and wide. Bursa copulatrix sac-like, oval with short slender duct (as long as bursa copulatrix), initially not flared. Vagina very long and slender. Genital anatomy of Subulina octona from the tropical greenhouse of the Science Museum of Trento ( MUSE ), D. Barbato & G. Bolzonella leg. 04 Jan. 2019: 31 genitalia (hermaphrodite gonad excluded) 32 detail of proximal penial complex. Male distal genitalia (Figs 31 , 32 ). Vas deferens of varying diameter (proximal tract narrow, medial tract slightly wider and final tract very narrow), entering penial complex near proximal end. Penial complex consisting of epiphallus, penial caecum and penis. Epiphallus very short. Penial caecum very short (as long as epiphallus). Penis very long, divided distinctly into proximal and distal parts by difference in calibre, without penial sheath; proximal part longer (twice distal penis), slender and thin walled; distal penis shorter (half proximal penis) and thick, muscular walled. Penial retractor muscle bifid, one branch inserted on tip of penial flagellum, the other branch on tip of penial caecum. Genital atrium (Fig. 31 ). Very short. Remarks. Subulina octona is a well-known travelling snail that occurs worldwide ( Robinson 1999 ) but its native range is uncertain. It was described from Guadeloupe and Hispaniola and has been reported as native to tropical America ( Pilsbry 1946 ), the Caribbean ( Deisler and Abbott 1984 ) and Latin America ( Robinson 1999 ) but this was disputed on the grounds that the other species of the genus occur in Africa ( Bieler and Slapcinsky 2000 ). Gerlach (2006) regarded it as native to the Seychelles , based on a subfossil record from Aldabra reported by Gerlach and van Bruggen (1999) . Others suggested that it was originally from tropical America ( Griffiths and Florens 2006 ), south-east Asia ( Rumi et al. 2010 ) or Africa ( Breure et al. 2016 ; Hovestadt and van Leeuwen 2017 ). Multi-gene phylogenetic analysis of the achatinoid snails by Fontanilla et al. (2017) found that Subulina octona and Subulina striatella ( Rang, 1831 ) formed a monophyletic group belonging to an unsupported clade including only Old World species, but unfortunately the study included a small selection of subulinine genera, only one of which was from neotropical America. Subulina octona is now distributed widely in humid tropical and subtropical lowlands across the world. It occurs in Central America, the West Indies, South America, sub-Saharan Africa, West Indian Ocean islands, South, South-East, and East Asia , New Guinea , Australia , and Pacific islands. In the mid temperate latitudes of the northern hemisphere, it only occurs in greenhouses and hothouses (see Table 4 for details and references). Geographical distribution of Subulina octona . Asterisks indicate countries / islands where the species has been recorded only in greenhouses or very disturbed anthropogenic habitats.
Regions Countries / Islands References
North America United States * Dundee (1974) , Nekola (2014)
Central America Belize, Costa Rica, Guatemala, Honduras, Mexico, Nicaragua, Panama, and Salvador Thompson (2011)
West Indies Bahamas, Cuba, Hispaniola, Jamaica, and Lesser Antilles (Barbados, Curaçao, Guadeloupe, Martinique, Saint Barthélemy, Saint Martin, and Trinidad) Deisler and Abbott (1984) , Chase and Robinson (2001) , Rosenberg and Muratov (2006) , Espinosa and Ortea (2009) , Robinson et al. (2009) , Rutherford (2011) , Maceira et al. (2013) , Charles (2015) , Delannoye et al. (2015) , Breure et al. (2016) , Herrera-Uria (2016) , Hovestadt and van Leeuwen (2017) , Hovestadt and Neckheim (2020) , Espinosa and Robinson (2021)
South America Brazil, Columbia, Ecuador, Peru, Suriname, and Venezuela Baker (1927) , Marcus and Marcus (1968) , van Regteren Altena (1975) , Simone (2006) , Rumi et al. (2010) , Breure et al. (2022 a )
Atlantic Ocean Bermuda Bieler and Slapcinsky (2000)
Europe Austria *, Czech Republic *, Denmark *, Great Britain *, Ireland *, Italy *, Netherlands *, and Sweden * Kerney and Cameron (1979) , von Proschwitz (1994 , 2016 ), Juricková (2006) , Da Sois (2015) , Reischütz et al. (2018) , Anderson and Rowson (2020) , Horsák et al. (2020) , this paper
Africa South Africa, Tanzania, and Zimbabwe van Bruggen (1981) , Rowson (2007) , Herbert (2010)
Indian Ocean Aldabra, Madagascar, Maldives, Mascarene, Pemba, and Seychelles Probst (2001) , Gerlach (2006) , Griffiths and Florens (2006) , Rowson (2007) , Emberton and Griffiths (2009) , Rowson et al. (2010) , Gittenberger and van Bruggen (2013) , Gittenberger et al. (2019)
South Asia India and Sri Lanka Ranawana (2006) , Raheem et al. (2014)
South-East Asia Indonesia, Peninsular Malaysia, Sabah in Malaysian Borneo, Singapore, and Vietnam Schileyko (2011) , Tan et al. (2015) , Foon et al. (2017) , Phung et al. (2017) , Nurinsiyaha and Hausdorf (2019)
East Asia Dongsha Islands and Japan * Minato (1988) , Wu et al. (2007)
Oceania Australia, New Guinea, and Pacific islands (American Samoa, Belau / Palau, Cook Islands, Federated States of Micronesia, Fiji, French Polynesia, Galapagos Islands, Guam, Hawaii, Marshall Islands, New Caledonia, Northern Mariana Islands, Pitcairn Islands, Samoa, Solomon Islands, Tonga, and Vanuatu) Cowie (2000 , 2001 ), Wiktor (2003) , Shea (2007) , Brook et al. (2010) , Rundell (2010) , Stanisic et al. (2010) , Brodie and Barker (2012) , Kerr and Bauman (2013) , Brook (2014) , Miquel and Herrera (2014) , Cowie et al. (2017)
The distal genitalia of MUSE specimens show a general scheme identical to that described by Baker (1927: 3–4 , pl. 20, fig. 99), Marcus and Marcus (1968: 189–190) and Araújo and Bessa (1993: 493–495 , figs 7–11), but differing in the size of the penial complex from that described by Wiegmann (1894: 214–216 , pl. 16, fig. 3; reproduced by Pilsbry 1946: 173 , fig. 83 h), Schileyko (1999 : fig. 662 BC ) and Gittenberger and van Bruggen (2013: 250) . Instead of a very short penial complex, in agreement with the first description by Baker (1927) , MUSE specimens have a long slender penial complex consisting of a short proximal portion (the epiphallus and the penial caecum closely juxtaposed to each other), a long slender medial portion (the proximal penis) and a short swollen distal portion (the distal penis). In particular, based on the male genitalia of a specimen from Dunoon ( Guyana ) mounted in glycerine jelly and viewed by transmitted light, Baker (1927) described the proximal portion as consisting of a flagellar appendix [the penial caecum] and a very short, thick walled tract [the epiphallus]; the vas deferens entering the penial complex at the proximal end of the epiphallus; the penial retractor joining at the tip of penial caecum; a rather elongate papilla present at the internal opening of the epiphallus into the proximal penis. Baker also described a penial sheath enveloping the distal penis joined by a muscular branch originating from the right lower tentacle retractor; finally he interpreted the structure that Wiegmann (1894) described and figured as the penis as being only the distal penis surrounded by a heavy muscular sheath. The small size and the very fine structure of the sections of the proximal portion of the penial complex make dissection difficult and differentiation of its components elusive. Our results substantially agree with Baker’s description. The differences are: the vas deferens enters the penial complex near the base and not at the tip of the epiphallus; the penial retractor consists of two branches, one joined to the epiphallus, the other to the penial caecum; the small size of the proximal penis makes the penial papilla impossible to detect by stereomicroscope; a classical penial sheath (such as that of Allopeas and Paropeas ) is absent, although a muscular branch from the right lower tentacle retractor joins the distal penis directly on the penial wall. Unfortunately, the scarcity of material prevented a more careful anatomical examination. Some uncertainties about its real organisation and the meaning of such differences among the various anatomical reports therefore remain. Multi-gene phylogenetic analysis of the achatinoid snails by Fontanilla et al. (2017) found that the genus, as currently conceived, is polyphyletic because the three Subulina species examined did not cluster together. The meaning of variation in penis size in Subulina octona is also uncertain. Wiegmann (1894) ventured that the extreme reduction of the male distal genitalia was related to “ unisexuality ” or sequential hermaphroditism (... dass die betreffenden Thiere durch Verkümmerung des männlichen Theils der Genitalien eingeschlechtig geworden sind, oder aber dass die weibliche Geschlechtsreife der männlichen vorausgeht). Others, such as Baker (1927) , supposed that the species was a sequential hermaphrodite, but whereas Wiegmann saw it as protogynous, Baker viewed it as protandrous. Subulina octona is actually a facultatively self-fertilising egg-retaining species showing no evidence of sequential hermaphroditism ( Bessa and Araújo 1995 ; D’Ávila et al. 2018 ). Thus the reduced penis may be related to loss of biparental reproduction as already supposed by Wiegmann. However this may be because Subulina octona is a complex of species. More research is needed to address these questions. Subulina octona is common in the tropical greenhouse of MUSE , and has been found in the Biodiversity Garden (Botanical Garden of Padua), where only one specimen was collected. This is the first report from Italy .