ISSN 1793‐8716 (online) Occasional Molluscan Papers ISSN 1793‐8708 (print) Volume 5: 1–9 Publishing on Malacology in the Sundaland Region Date of publication: www.molluscan.com/omp http://zoobank.org/urn:lsid:zoobank.org:pub: 07468838‐5A16‐4973‐92D6‐B7D14E5B0C86 10 August 2016

Research Article

Making its way down the Peninsula: Discovery of the non‐native Cryptozona siamensis (L. Pfeiffer, 1856) in Singapore, with a note on its status in Peninsular Malaysia (Helicarionoidea: Ariophantidae) Siong Kiat Tan1,4, Sow Yan Chan2, Leo H.S. Nguang2 & Martyn E. Y. Low1 1Lee Kong Chian Natural History Museum, National University of Singapore, 2Conservatory Drive, Singapore 117377, Republic of Singapore 3VBox 888313, Singapore 919191, Republic of Singapore 4Corresponding author: [email protected]

Abstract

The non‐indigenous Cryptozona siamensis is reported for the first time from Singapore. This terrestrial snail was discovered from the site of a former plant nursery that borders the Central Catchment Nature Reserve, and is believed to have been accidentally introduced through horticultural trade activities. Cryptozona siamensis is a potential plant pest and is known to be a host of the parasite that causes human eosinophilic meningitis, a potentially life‐threatening condition. Urgent management to control or eradicate the is desired to curb its spread. Its distribution and status in Peninsular Malaysia is briefly discussed.

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Introduction

The introduction of non‐indigenous molluscs has long been known to negatively impact native biodiversity and natural ecosystems, being possible plant pests that may cause economic losses, and posing risks to human health (e.g., Mead, 1961; Byers, 1999; Cowie, 2001; Carlsson et al., 2004; Clavero & García‐Berthou, 2005; Lv et al., 2009). It is also known that the eradication of invasive species is likely to be successful only in the earliest stages before the species becomes widespread and endemic (Gherardi & Angiolini, 2004; Simberloff, 2010). It is therefore imperative that discoveries of new non‐ Fig. 1. Fence of the former Mandai Orchid Garden, where indigenous species be promptly reported for successful Cryptozona siamensis was found. (Photograph: L.H.S. Nguang). implementation of control and eradication measures. Specimens were collected as voucher material and Numerous non‐indigenous molluscs have been deposited in the Zoological Reference Collection (ZRC) introduced to Singapore over the years (e.g. Morton & KS of the Lee Kong Chian Natural History Museum, National Tan, 2006; SK Tan & Clements, 2011; SK Tan et al., 2012; University of Singapore (12 ex. [including 5 juveniles + 1 Ng et al., 2014a, 2014b, 2015). Here, we report the fragment] (ZRC.MOL.6497), 2 May 2016; 9 ex. [empty recent discovery in Singapore of a new non‐indigenous shells] (ZRC.MOL.6546), 20 May 2016; 16 ex. [empty terrestrial snail, Cryptozona siamensis (L. Pfeiffer, 1856). shells, including 5 broken] (ZRC.MOL.6547), 22 May This species, which is native to Thailand, was not 2016). Additional comparative material used in this recorded in previous intensive studies of the terrestrial study is from the collection of S.Y. Chan (CSY), the second molluscs of Singapore (Lim, 1969; Ho, 1995; SK Tan et author. Abbreviations used are “SH” for shell height and al., 2012). Its distribution and status in the Malay “SW” for shell width. Shell height is defined as the Peninsula, is also briefly examined and discussed. distance from the apex to the lowest part of the basal

side of the peristome, and shell width is the distance

To cite this publication: between the edges of the widest part of the body whorl Tan SK, Chan SY, Nguang LHS & Low MEY (2016) Making its way down perpendicular to the coiling axis. All measurements are the Peninsula: Discovery of the non‐native Cryptozona siamensis (L. in millimetres (mm). Pfeiffer, 1856) in Singapore, with a note on its status in Peninsular Malaysia (Helicarionoidea: Ariophantidae). Occasional Molluscan Papers, 5: 1–9. Observations © the Author(s) and this is an open access article distributed under the terms of the Creative Commons Attribution License 4.0 (CC‐BY‐NC‐SA Cryptozona siamensis (L. Pfeiffer, 1856) was first 4.0), which permits the copying, distribution and transmission of the encountered by chance, on the 2 May 2016, along the

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Fig. 2. The non‐indigenous Cryptozona siamensis feeding on a decomposing leaf on the ground. (Photograph: S.K. Tan). perimeter fence of the former Mandai Orchid Garden about a hundred empty shells were found, and it may premises (Fig. 1), parallel to Mandai Lake Road even be considered an infestation. The adjacent (1°24′26.8″N 103°46′59.2″E). The snails were seen secondary forest to the north and west of the site were crawling and foraging actively, amongst leaf litter and also surveyed. However, no evidence of its presence was vegetation between the chain‐link fence and footpath, found in the forested areas, which suggests that the snail following a heavy downpour in the afternoon. remains localised to the premises of the former Mandai Individuals were observed feeding on plant matter on Orchid Garden. the ground (Fig. 2). Two similar‐looking species, the native striata (Gray, 1834), and an unidentified ariophantid, provisionally assigned to the genus Sarika Cryptozona siamensis (L. Pfeiffer, 1856) Godwin‐Austen, 1907, were found sympatrically (Fig. 3). (Figs. 2–6, 8)

The site where Cryptozona siamensis was found was Type locality. Thailand [“Siam”]. surveyed again on the 20 May and 22 May 2016. The second trip yielded over 20 empty shells on the ground Diagnosis. Shell medium sized (to >30 mm in shell amongst leaf litter and vegetation, along the same fence. width), discoidal with a low spire. Colour two‐toned, At least twenty live snails, including more than a dozen dorsal part light brown, ventral light straw; dark reddish juveniles (SW <10 mm), were observed. More empty brown spiral band usually present where the two tones shells and live were found during the third meet just above the periphery. Surface with fine survey. Live snails were mostly found amongst leaf litter. reticulate sculpture created by very fine dense axial The undersides of large leaves that are slightly raised in grooves (or growth lines) intersected by fine incised the middle somewhat like a tent seem to be preferred spiral lines, above the periphery; ventral surface rather roosts for these animals. It was also noted that many smooth and somewhat shiny, with irregular growth empty shells are broken in ways that suggest predation lines. grey in colour, head‐foot reticulated; the by birds or small mammals (Fig. 4; also see Foon et al., recessed parts and the upper (eyestalks) and lower 2014). tentacles darker; mantle, basal part of foot, and posterior tip around the caudal mucous horn, pale Cryptozona siamensis is apparently well established at whitish‐grey. this locality. Altogether, a few dozen live snails, and 3 2

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Fig. 3. The three species of similar‐looking snails, Sarika sp. (on the left), Cryptozona siamensis (upper, middle), and (right), found at the locality. (Photograph: S.K. Tan).

Remarks. In Singapore, Cryptozona siamensis (L. found along the perimeter fence of the former premises of Pfeiffer, 1856) is unlikely to be confused with other a commercial orchid distributor. This could also imply terrestrial snail species upon inspection. The shell that Cryptozona siamensis may have remained undetected characteristics (distinctly two‐toned shell, separated by in Singapore for at least half a decade because the grounds a spiral band above the periphery, and fine reticulate were vacated in 2011. Additional surveys are necessary sculpture on the dorsal surface) of Cryptozona siamensis to determine whether this species is confined to the single is quite unmistakable (Figs. 5–6). Compared to the two population discovered, is present in other nurseries, or is similar‐looking species it was found with, Cryptozona already widespread. siamensis can also be distinguished from Quantula striata by its more rounded periphery. The shell colour Cryptozona siamensis has been reported as one of the of the latter tends to be more variable; from very light pest species intercepted in the United States of America pale beige to dark reddish brown (Fig. 7, A–F; see also (Meissner et al., 2009). Two of its congeneric relatives SK Tan et al., 2012). Sarika sp. can be easily identified by are treated as agricultural and horticultural pests in its smooth and uniformly brown shell (Fig. 7, G–I). India (Raut & Ghose, 1984). Little information is available on the status of Cryptozona siamensis as a pest, but it may become a plant pest as it is adaptable to a Discussion variety of habitats, from forests to urban areas, in Thailand (Panha et al., 2009). Besides being a potential Potential pathway of introduction and impact of plant pest, Cryptozona siamensis is a known to be an Cryptozona siamensis in Singapore. One of the more intermediate host for the rat lungworm, a parasitic common pathways of introduction for non‐indigenous nematode, which is a major cause of eosinophilic terrestrial molluscs is through agricultural and meningitis, which is potentially life‐threatening horticultural trade activities (Cowie, 1998; Meissner et al., (Bowden, 1981; Cowie, 2013; Vitta et al., 2016). Humans 2009; Herbert, 2010). An accidental introduction through may be infected through ingestion or contact with horticultural trade activities is regarded as most likely for infected snails, or indirectly through the consumption of the Cryptozona siamensis (L. Pfeiffer, 1856) in Singapore. contaminated fresh produce, such as vegetables The supposition is not unreasonable as the snails were (Bowden, 1981; Tsai et al., 2004).

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(Prasankok & Panha, 2011; Abu‐Bakar et al., 2014), there is little doubt that it is non‐indigenous there. No historical records were found in the literature (e.g., Stoliczka, 1873; von Moellendorff, 1886; Tenison‐ Woods, 1888; Dall, 1897; Collinge, 1902, 1903; Sykes, 1902; Laidlaw, 1932, 1933; van Benthem Jutting, 1949, 1960; Berry, 1963; Chan, 1997, 1998a, 1998b; Davison, 1998; Maassen, 2001), and this species was never found in our past terrestrial molluscan diversity surveys of Peninsular Malaysia from the mid‐1990s to early 2000s (S.Y. Chan et al., unpub. data), which included the exact localities, Cinta Manis (also as Bukit Chintamani or Chintamanis in the literature) and Pulau Langkawi, mentioned by Prasankok & Panha (2011) and Abu‐ Bakar et al. (2014) respectively.

Fig. 4. Some broken shells of Cryptozona siamensis that show signs of predation. (Photograph: S.Y. Chan). Cryptozona siamensis is thus likely to have been introduced inadvertently through human activities to Peninsular Malaysia sometime between the late‐1990s Invasive species are known as a leading cause in animal to late 2000s. At Cinta Manis, near Bentong in Pahang, extinctions (Clavero & García‐Berthou, 2005), and it is this species is now one of the most common terrestrial difficult to predict whether Cryptozona siamensis will snails in human‐modified landscape, in or surrounded eventually become invasive. If it can be determined that by plantations and farms (T.S. Liew & J.K. Foon, pers. Cryptozona siamensis in Singapore is restricted to the comm.; Fig. 8). Apart from the two aforementioned vicinity of the former Mandai Orchid Garden, urgent localities (some 300 km apart), the current range and management to control or eradicate the species would distribution of Cryptozona siamensis in Peninsular be desired based on the precautionary principle. The site Malaysia is not known. Assuming that the populations is located at the boundary of the Central Catchment remain localised, preventing their further spread, and Nature Reserve (CCNR), and control or eradication eradication or management strategies should be given attempts will be extremely difficult (or even impossible) priority. should this species penetrate the forest and becomes widespread. In addition to eradication efforts, a concerted effort is needed to elucidate the pathways by Acknowledgements which such non‐native species are finding their way into The manuscript was improved by the comments and the Republic. suggestions of Thor‐Seng Liew, who also provided the image of Cryptozona siamensis from Cinta Manis used Distribution of Cryptozona siamensis, and its status here. Thanks are also due to Junn Kitt Foon for sharing in Peninsular Malaysia. Cryptozona siamensis (L. his field observations. Pfeiffer, 1856) is known to be native to Thailand, and is regarded as one of the most common and widespread snail species there (Pfeiffer, 1856; Panha et al., 2009; References Prasankok & Panha, 2011). Prasankok & Panha (2011) stated that Cryptozona siamensis is a cosmopolitan Abu‐Bakar S‐B, Razali NM, Naggs F, Wade C, Mohd‐Nor S‐A & species or widely distributed throughout Indochina. Tan SHA (2014). The mitochondrial 16s rRNA reveals high However, this may be an overgeneralisation and until anthropogenic influence on land snail diversity in a very recently, there were no reports of this species from preliminary island survey. Molecular Biology Reports, the adjacent areas such as Myanmar, Cambodia, Laos, 41(3): 1799–1805. Vietnam, and Peninsular Malaysia (e.g., Moellendorff, Berry AJ (1963) An introduction to the non‐marine molluscs of Malaya. Malayan Nature Journal, 17(1): 1–17. 1886; Fischer, 1891; Dall, 1897; Collinge, 1902; Blandford WT & Godwin‐Austen HH (1908) The fauna of Blandford & Godwin‐Austen, 1908; Laidlaw, 1933; British India, including Ceylon and Burma: . Solem, 1966; Maassen, 2001; Schileyko, 2011). In Testacellidae and Zonitidae. Taylor and Francis, London, Thailand, the species occurs commonly in newly xxxii + 311 pp. developed areas and habitats associated with human Bowden DK (1981) Eosinophilic meningitis in the New activities, and a surprisingly high level of genetic Hebrides: two outbreaks and two deaths. American Journal homogeneity among populations throughout Thailand of Tropical Medicine and Hygiene, 30(5): 1141–1143. has been shown (Prasankok & Panha, 2011). It is Byers JE (1999) The distribution of an introduced mollusc and therefore possible that the widespread distribution of its role in the long‐term demise of a native confamilial species. Biological Invasions, 1(4): 339–352. Cryptozona siamensis in Thailand today is largely due to Carlsson NOL, Brönmark C & Hansson L‐A (2004) Invading anthropogenic activities. herbivory: The golden apple snail alters ecosystem functioning in Asian wetlands. Ecology, 85(6): 1575– Although the presence of Cryptozona siamensis in 1580. Peninsular Malaysia was mentioned in recent studies

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Fig. 5. Cryptozona siamensis (ZRC.MOL.6479 [SH 16.0 × SW 30.1]) from Mandai Lake Road, Singapore. Scale bar = 10 mm. (Photograph: S.K. Tan).

Chan SY (1997) Non‐marine mollusks from Selangor, West Clavero M & García‐Berthou E (2005) Invasive species are a Malaysia, with a comparison note on introduced species. leading cause of animal extinctions. Trends in Ecology and Club Conchylia Informationen, 29: 35–46. Evolution, 20(3): 110. Chan SY (1998a) A brief collecting trip to Perak, West Collinge WE (1902) On the non‐operculate land and Malaysia: Part one. Papustyla, 12(4): 4–5. freshwater molluscs collected by members of the “Skeat Chan SY (1998b) A brief collecting trip to Perak, West Expedition” in the Malay Peninsula, 1899–1900. Journal of Malaysia: Part two. Papustyla, 12(1): 1–2. Malacology, 9(3): 71–95, pls. 4–6.

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Fig. 6. Cryptozona siamensis from Thailand: A–C, Ranong (CSY 393.3.3.1 [SH 15.3 × SW 27.4]); D–F, Krabi (CSY 393.3.3.2 [SH 14.3 × SW 23.8]); G–I, Phuket Island (CSY uncat. [SH 13.7 × SW 24.7]). Scale bar = 10 mm. (Photograph: S.K. Tan).

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Fig. 7. Quantula striata and Sarika sp., shown for comparison: A–F, Quantula striata (ZRC.MOL. 3249 [A–C, SH 16.8 × SW 26.6; D– F, SH 15.5 × SW 26.1]), Bukit Brown; G–I, Sarika sp. (ZRC.MOL.6496 [SH 12.3 × SW 23.7]), Mandai Lake Road. Scale bar = 10 mm. (Photograph: S.K. Tan).

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Fig. 8. Cryptozona siamensis found on cultivated land at Cinta Manis, Pahang, in 2010. (Photograph: T.S. Liew)

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