Occasional

Molluscan Papers

ISSN 17938716 (online)

ISSN 17938708 (print)
Volume 5: 19
Date of publication:
10 August 2016

Publishing on Malacology in the Sundaland Region

www.molluscan.com/omp

http://zoobank.org/urn:lsid:zoobank.org:pub: 074688385A16497392D6B7D14E5B0C86

Research Article

Making its way down the Peninsula: Discovery of the nonnative 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
Lee Kong Chian Natural History Museum, National University of Singapore,
Conservatory Drive, Singapore 117377, Republic of Singapore
3VBox 888313, Singapore 919191, Republic of Singapore
4Corresponding author: nhmtsk@nus.edu.sg
1
2

Abstract

The nonindigenous 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 lifethreatening condition. Urgent management to control or
eradicate the species is desired to curb its spread. Its distribution and status in Peninsular Malaysia is briefly discussed.

http://zoobank.org/urn:lsid:zoobank.org:pub:40DA12F4C8914FD6BA037733649D9CCD

Introduction

The introduction of nonindigenous 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 & GarcaBerthou, 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
indigenous species be promptly reported for successful
implementation of control and eradication measures.

Fig. 1. Fence of the former Mandai Orchid Garden, where

Cryptozona siamensis was found. (Photograph: L.H.S. Nguang).

Numerous nonindigenous molluscs have been

introduced to Singapore over the years (e.g. Morton & KS
Tan, 2006; SK Tan & Clements, 2011; SK Tan et al., 2012;
Ng et al., 2014a, 2014b, 2015). Here, we report the
recent discovery in Singapore of a new nonindigenous
terrestrial snail, Cryptozona siamensis (L. Pfeiffer, 1856).
This species, which is native to Thailand, was not
recorded in previous intensive studies of the terrestrial
molluscs of Singapore (Lim, 1969; Ho, 1995; SK Tan et
al., 2012). Its distribution and status in the Malay
Peninsula, is also briefly examined and discussed.

To cite this publication:

Tan SK, Chan SY, Nguang LHS & Low MEY (2016) Making its way down
the Peninsula: Discovery of the nonnative Cryptozona siamensis (L.
Pfeiffer, 1856) in Singapore, with a note on its status in Peninsular
Malaysia (Helicarionoidea: Ariophantidae). Occasional Molluscan
Papers, 5: 19.

the Author(s) and this is an open access article distributed under the
terms of the Creative Commons Attribution License 4.0 (CCBYNCSA
4.0), which permits the copying, distribution and transmission of the

Specimens were collected as voucher material and

deposited in the Zoological Reference Collection (ZRC)
of the Lee Kong Chian Natural History Museum, National
University of Singapore (12 ex. [including 5 juveniles + 1
fragment] (ZRC.MOL.6497), 2 May 2016; 9 ex. [empty
shells] (ZRC.MOL.6546), 20 May 2016; 16 ex. [empty
shells, including 5 broken] (ZRC.MOL.6547), 22 May
2016). Additional comparative material used in this
study is from the collection of S.Y. Chan (CSY), the second
author. Abbreviations used are SH for shell height and
SW for shell width. Shell height is defined as the
distance from the apex to the lowest part of the basal
side of the peristome, and shell width is the distance
between the edges of the widest part of the body whorl
perpendicular to the coiling axis. All measurements are
in millimetres (mm).

Observations

Cryptozona siamensis (L. Pfeiffer, 1856) was first

encountered by chance, on the 2 May 2016, along the

Occasional Molluscan Papers 5 (2016)

Fig. 2. The nonindigenous Cryptozona siamensis feeding on a decomposing leaf on the ground. (Photograph: S.K. Tan).

perimeter fence of the former Mandai Orchid Garden

premises (Fig. 1), parallel to Mandai Lake Road
(12426.8N 1034659.2E). The snails were seen
crawling and foraging actively, amongst leaf litter and
vegetation between the chainlink fence and footpath,
following a heavy downpour in the afternoon.
Individuals were observed feeding on plant matter on
the ground (Fig. 2). Two similarlooking species, the
native Quantula striata (Gray, 1834), and an unidentified
ariophantid, provisionally assigned to the genus Sarika
GodwinAusten, 1907, were found sympatrically (Fig. 3).

about a hundred empty shells were found, and it may

even be considered an infestation. The adjacent
secondary forest to the north and west of the site were
also surveyed. However, no evidence of its presence was
found in the forested areas, which suggests that the snail
remains localised to the premises of the former Mandai
Orchid Garden.


Cryptozona siamensis (L. Pfeiffer, 1856)
(Figs. 26, 8)

Type locality. Thailand [Siam].

Diagnosis. Shell medium sized (to >30 mm in shell
width), discoidal with a low spire. Colour twotoned,
dorsal part light brown, ventral light straw; dark reddish
brown spiral band usually present where the two tones
meet just above the periphery. Surface with fine
reticulate sculpture created by very fine dense axial
grooves (or growth lines) intersected by fine incised
spiral lines, above the periphery; ventral surface rather
smooth and somewhat shiny, with irregular growth
lines. Animal grey in colour, headfoot reticulated; the
recessed parts and the upper (eyestalks) and lower
tentacles darker; mantle, basal part of foot, and
posterior tip around the caudal mucous horn, pale
whitishgrey.

The site where Cryptozona siamensis was found was

surveyed again on the 20 May and 22 May 2016. The
second trip yielded over 20 empty shells on the ground
amongst leaf litter and vegetation, along the same fence.
At least twenty live snails, including more than a dozen
juveniles (SW <10 mm), were observed. More empty
shells and live animals were found during the third
survey. Live snails were mostly found amongst leaf litter.
The undersides of large leaves that are slightly raised in
the middle somewhat like a tent seem to be preferred
roosts for these animals. It was also noted that many
empty shells are broken in ways that suggest predation
by birds or small mammals (Fig. 4; also see Foon et al.,
2014).

Cryptozona siamensis is apparently well established at

this locality. Altogether, a few dozen live snails, and
3
2

Tan et al. Cryptozona siamensis in Singapore

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

Remarks. In Singapore, Cryptozona siamensis (L.

Pfeiffer, 1856) is unlikely to be confused with other
terrestrial snail species upon inspection. The shell
characteristics (distinctly twotoned shell, separated by
a spiral band above the periphery, and fine reticulate
sculpture on the dorsal surface) of Cryptozona siamensis
is quite unmistakable (Figs. 56). Compared to the two
similarlooking species it was found with, Cryptozona
siamensis can also be distinguished from Quantula
striata by its more rounded periphery. The shell colour
of the latter tends to be more variable; from very light
pale beige to dark reddish brown (Fig. 7, AF; see also
SK Tan et al., 2012). Sarika sp. can be easily identified by
its smooth and uniformly brown shell (Fig. 7, GI).


Discussion

found along the perimeter fence of the former premises of

a commercial orchid distributor. This could also imply
that Cryptozona siamensis may have remained undetected
in Singapore for at least half a decade because the grounds
were vacated in 2011. Additional surveys are necessary
to determine whether this species is confined to the single
population discovered, is present in other nurseries, or is
already widespread.

Cryptozona siamensis has been reported as one of the

pest species intercepted in the United States of America
(Meissner et al., 2009). Two of its congeneric relatives
are treated as agricultural and horticultural pests in
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
variety of habitats, from forests to urban areas, in
Thailand (Panha et al., 2009). Besides being a potential
plant pest, Cryptozona siamensis is a known to be an
intermediate host for the rat lungworm, a parasitic
nematode, which is a major cause of eosinophilic
meningitis, which is potentially lifethreatening
(Bowden, 1981; Cowie, 2013; Vitta et al., 2016). Humans
may be infected through ingestion or contact with
infected snails, or indirectly through the consumption of
contaminated fresh produce, such as vegetables
(Bowden, 1981; Tsai et al., 2004).

Potential pathway of introduction and impact of

Cryptozona siamensis in Singapore. One of the more
common pathways of introduction for nonindigenous
terrestrial molluscs is through agricultural and
horticultural trade activities (Cowie, 1998; Meissner et al.,
2009; Herbert, 2010). An accidental introduction through
horticultural trade activities is regarded as most likely for
the Cryptozona siamensis (L. Pfeiffer, 1856) in Singapore.
The supposition is not unreasonable as the snails were
4
3

Occasional Molluscan Papers 5 (2016)

(Prasankok & Panha, 2011; AbuBakar et al., 2014),

there is little doubt that it is nonindigenous 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 mid1990s 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.

Cryptozona siamensis is thus likely to have been
introduced inadvertently through human activities to
Peninsular Malaysia sometime between the late1990s
to late 2000s. At Cinta Manis, near Bentong in Pahang,
this species is now one of the most common terrestrial
snails in humanmodified landscape, in or surrounded
by plantations and farms (T.S. Liew & J.K. Foon, pers.
comm.; Fig. 8). Apart from the two aforementioned
localities (some 300 km apart), the current range and
distribution of Cryptozona siamensis in Peninsular
Malaysia is not known. Assuming that the populations
remain localised, preventing their further spread, and
eradication or management strategies should be given
priority.

Fig. 4. Some broken shells of Cryptozona siamensis that show

signs of predation. (Photograph: S.Y. Chan).

Invasive species are known as a leading cause in animal

extinctions (Clavero & GarcaBerthou, 2005), and it is
difficult to predict whether Cryptozona siamensis will
eventually become invasive. If it can be determined that
Cryptozona siamensis in Singapore is restricted to the
vicinity of the former Mandai Orchid Garden, urgent
management to control or eradicate the species would
be desired based on the precautionary principle. The site
is located at the boundary of the Central Catchment
Nature Reserve (CCNR), and control or eradication
attempts will be extremely difficult (or even impossible)
should this species penetrate the forest and becomes
widespread. In addition to eradication efforts, a
concerted effort is needed to elucidate the pathways by
which such nonnative species are finding their way into
the Republic.

Acknowledgements
The manuscript was improved by the comments and
suggestions of ThorSeng Liew, who also provided the
image of Cryptozona siamensis from Cinta Manis used
here. Thanks are also due to Junn Kitt Foon for sharing
his field observations.

Distribution of Cryptozona siamensis, and its status

in Peninsular Malaysia. Cryptozona siamensis (L.
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;
Prasankok & Panha, 2011). Prasankok & Panha (2011)
stated that Cryptozona siamensis is a cosmopolitan
species or widely distributed throughout Indochina.
However, this may be an overgeneralisation and until
very recently, there were no reports of this species from
the adjacent areas such as Myanmar, Cambodia, Laos,
Vietnam, and Peninsular Malaysia (e.g., Moellendorff,
1886; Fischer, 1891; Dall, 1897; Collinge, 1902;
Blandford & GodwinAusten, 1908; Laidlaw, 1933;
Solem, 1966; Maassen, 2001; Schileyko, 2011). In
Thailand, the species occurs commonly in newly
developed areas and habitats associated with human
activities, and a surprisingly high level of genetic
homogeneity among populations throughout Thailand
has been shown (Prasankok & Panha, 2011). It is
therefore possible that the widespread distribution of
Cryptozona siamensis in Thailand today is largely due to
anthropogenic activities.

References

AbuBakar SB, Razali NM, Naggs F, Wade C, MohdNor SA &

Tan SHA (2014). The mitochondrial 16s rRNA reveals high
anthropogenic influence on land snail diversity in a
preliminary island survey. Molecular Biology Reports,
41(3): 17991805.
Berry AJ (1963) An introduction to the nonmarine molluscs of
Malaya. Malayan Nature Journal, 17(1): 117.
Blandford WT & GodwinAusten HH (1908) The fauna of
British India, including Ceylon and Burma: Mollusca.
Testacellidae and Zonitidae. Taylor and Francis, London,
xxxii + 311 pp.
Bowden DK (1981) Eosinophilic meningitis in the New
Hebrides: two outbreaks and two deaths. American Journal
of Tropical Medicine and Hygiene, 30(5): 11411143.
Byers JE (1999) The distribution of an introduced mollusc and
its role in the longterm demise of a native confamilial
species. Biological Invasions, 1(4): 339352.
Carlsson NOL, Brnmark C & Hansson LA (2004) Invading
herbivory: The golden apple snail alters ecosystem
functioning in Asian wetlands. Ecology, 85(6): 1575
1580.

Although the presence of Cryptozona siamensis in

Peninsular Malaysia was mentioned in recent studies
4
3

Tan et al. Cryptozona siamensis in Singapore

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).
Clavero M & GarcaBerthou E (2005) Invasive species are a
leading cause of animal extinctions. Trends in Ecology and
Evolution, 20(3): 110.
Collinge WE (1902) On the nonoperculate land and
freshwater molluscs collected by members of the Skeat
Expedition in the Malay Peninsula, 18991900. Journal of
Malacology, 9(3): 7195, pls. 46.

Chan SY (1997) Nonmarine mollusks from Selangor, West

Malaysia, with a comparison note on introduced species.
Club Conchylia Informationen, 29: 3546.
Chan SY (1998a) A brief collecting trip to Perak, West
Malaysia: Part one. Papustyla, 12(4): 45.
Chan SY (1998b) A brief collecting trip to Perak, West
Malaysia: Part two. Papustyla, 12(1): 12.
5
4

Occasional Molluscan Papers 5 (2016)

Fig. 6. Cryptozona siamensis from Thailand: AC, Ranong (CSY 393.3.3.1 [SH 15.3 SW 27.4]); DF, Krabi (CSY 393.3.3.2 [SH 14.3
SW 23.8]); GI, Phuket Island (CSY uncat. [SH 13.7 SW 24.7]). Scale bar = 10 mm. (Photograph: S.K. Tan).
Dall WH (1897) Note of landshells from the Malay Peninsula.
Nautilus, 11(4): 3738.
Davison GWH (1995) The terrestrial mollusca fauna of
Temengor Forest Reserve, Hulu Perak, Malaysia. Malayan
Nature Journal, 48: 233248.
Fischer P (1891) Catalogue et distribution gographique des
Mollusques terrestres, fluviatilies & marins dune partie de
lIndoChine (Siam, Laos, Cambodge, Cochinchine, Annam,
Tonkin). Dejussieu Pre et Fils, Autun, 186 pp.
Foon JK, Tan SK & Chan SY (2014) Possible rodent and avian
predation of tree snail Amphidromus atricallosus
perakensis. Singapore Biodiversity Records, 2014: 4041.

Collinge WE (1903) Report on the nonoperculate land

Mollusca. Fasciculi Malayenses: Zoology, 2: 205218.
Cowie RH (1998) Patterns of introduction of nonindigenous
nonmarine snails and slugs in the Hawaiian Islands.
Biodiversity and Conservation, 7(3): 349368.
Cowie RH (2001) Invertebrate invasions on Pacific Islands and the
replacement of unique native faunas: a synthesis of the land
and freshwater snails. Biological Invasions, 3(2): 119136.
Cowie RH (2013). Pathways for transmission of
angiostrongyliasis and the risk of disease associated with
them. Hawaii Journal of Medicine & Public Health,
72(supp. 2): 7074.

6
3

Tan et al. Cryptozona siamensis in Singapore

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

Ocean: Supplementary to Messrs. Theobald and Hanleys

Conchologia Indica. Taylor and Francis, London, pp. 149238.
Gray JE (1834) Characters of a new genus of Mollusca
(Nanina). Proceedings of the Zoological Society of London,
1834(19): 5859.
Herbert DG (2010) The introduced terrestrial Mollusca of
South Africa. SANBI Biodiversity Series 15. South African
National Biodiversity Institute, Pretoria, vi + 108 pp.
Ho WH (1995) A review of the landsnail fauna of Singapore.
Raffles Bulletin of Zoology, 43(1): 91113.

Gherardi F & Angiolini C (2004) Eradication and control of

invasive species. In: Gherardi F, Cortj C & Gualtieri M (eds.).
Biodiversity Conservation and Habitat Management.
Volume 1. Encyclopaedia of Life Support Systems (EOLSS).
UNESCO and EOLSS Publishers, Paris, pp. 271299.
GodwinAusten HH (1907) Land and freshwater Mollusca of India,
vol. II (10). In: Blandford WT (ed.), Land and freshwater
Mollusca of India, including South Arabia, Baluchistan,
Afghanistan, Kashmir, Nepal, Burmah, Pegu, Tenasserim,
Malay Peninsula, Ceylon, and other islands of the Indian

7
4

Occasional Molluscan Papers 5 (2016)

Fig. 8. Cryptozona siamensis found on cultivated land at Cinta Manis, Pahang, in 2010. (Photograph: T.S. Liew)
Ng TH, Tan SK & Yeo DCJ (2014b) The Taxonomy, Distribution and
Introduction History of the Earliest Reported Alien
Freshwater Mollusc in Singapore Sinotaia guangdungensis
(Gastropoda: Viviparidae). Malacologia, 57(2): 401408.
Ng TH, Tan SK & Yeo DCJ (2015) Clarifying the identity of the
longestablished, globallyinvasive Physa acuta Draparnaud,
1805 (Gastropoda: Physidae) in Singapore. BioInvasion
Records, 4(3): 189194.
Panha S, Sutcharit C, Tongkerd P & Naggs F (2009) An Illustrated
Guide to the Land Snails of Thailand. Biodiversity Research
and Training Program, 12 pp.
Pfeiffer L (1856) Descriptions of twentyfive new species of land
shells, from the collection of H. Cuming, Esq. Proceedings of
the Zoological Society of London, 1856(302): 3236.
Raut SK & Ghose KC (1984) Pestiferous Land Snails of India.
Zoological Survey of India, Technical Monograph, 11: 1
151, pls. 117.
Schileyko AA (2011) Checklist of land pulmonate molluscs of
Vietnam (Gastropoda: Stylommatophora). Ruthenica, 21:
168.
Simberloff D (2010) Invasive species. In: Sodhi NS & Ehrlich PR
(eds.), Conservation Biology for All. Oxford University
Press, Oxford, pp. 131152.
Solem A (1966) Some nonmarine mollusks from Thailand,
with notes on classification of the Helicarionidae. Spolia
Zoologica Musei Hauniensis, 24: 7110, pls. 13.
Stoliczka F (1873) On the landshells of Penang Island, with
descriptions of the animals and anatomical notes; part
second, Helicacea. Journal of the Asiatic Society of Bengal,
42(1): 1138.

Laidlaw FF (1932) Notes on Ariophantidae from the Malay

Peninsula, with descriptions of new genera. Proceedings of
the Malacological Society of London, 20(2): 8094.
Laidlaw FF (1933) A list of the land and freshwater Mollusca
of the Malay Peninsula. Journal of the Malayan Branch of
the Royal Asiatic Society, 11(2): 211234.
Lim KYR (1969) The terrestrial molluscs of Singapore. Degree
of Bachelor of Science with Honours in Zoology thesis,
Department of Zoology, University of Singapore, 241 pp.
Lv S, Zhang Y, Liu HX, Hu L, Yang K, Steinmann P, Chen Z, Wang
LY, Utzinger J & Zhou XN (2009) Invasive snails and an
emerging infectious disease: results from the first national
survey on Angiostrongylus cantonensis in China. PLoS
Neglected Tropical Diseases, 3(2): e368.
Maassen WJM (2001) A preliminary checklist of the non
marine mollusks of Malaysia: a hand list. De Kreukel, Extra
Editie, 2001: 1155.
Meissner H, Lemay A, Bertone C, Schwartzburg K, Fergusen L &
Newton (2009) Evaluation of pathways for exotic plant pest
movement into and within the greater Caribbean region.
Caribbean Invasive Species Working Group (CISWG) and
Plant Epidemiology and Risk Analysis Laboratory (PERAL),
Center for Plant Health Science and Technology (CPHST),
United States Department of Agriculture (USDA), v + 267 pp.
Morton B & Tan KS (2006) Brachidontes striatulus (Bivalvia:
Mytilidae) introduced into Singapore, Raffles Bulletin of
Zoology, 54(2): 435439.
Ng TH, Tan SK & Low MEY (2014a) Singapore Mollusca: 7. The
family Ampullariidae (Gastropoda: Caenogastropoda:
Ampullarioidea). Nature in Singapore, 7: 3147.
8
3

Tan et al. Cryptozona siamensis in Singapore

with an appendix on cave shells. Bulletin of the Raffles

Museum, 19: 5077.
van Benthem Jutting WSS (1960) Some notes on land and
freshwater Mollusca of Malaya. Basteria, 24: 1020.
Vitta A, Polsut W, Fukruksa C, Yimthin T, Thanwisai A &
Dekumyoy P (2016) Levels of infection with the lungworm
Angiostrongylus cantonensis in terrestrial snails from
Thailand, with Cryptozona siamensis as a new intermediate
host. Journal of Helminthology, doi:10.1017/S0022149
X15001042.
von Moellendorff OF (1886) The landshells of Perak. Journal of
the Asiatic Society of Bengal, 55(part 2, no. 2): 299316.

Sykes ER (1902) On a collection of land and fresh water shells

from Kelantan, Malay Peninsula. Journal of Malacology,
9(2): 6063.
Tan SK, Chan SY & Clements GR (2012) A guide to snails and
other nonmarine molluscs of Singapore. Science Centre
Singapore, Singapore, 176 pp.
Tan SK & GR Clements (2011) Limicolaria flammea (Mller,
1774), another potentially invasive African land snail in
tropical Asia. Tropical Conservation Science, 4(1): 97102.
TenisonWoods JE (1888) Malaysian land and freshwater
Mollusca. Proceedings of the Linnean Society of New South
Wales, ser. 2, 3(3): 10031095.
Tsai HC, Lee S SJ, Huang CK, Yen CM, Chen ER & Liu YC
(2004) Outbreak of eosinophilic meningitis associated
with drinking raw vegetable juice in southern Taiwan.
American Journal of Tropical Medicine and Hygiene, 71(2):
222226.
van Benthem Jutting WSS (1949) On a collection of nonmarine
Mollusca from Malaya in the Raffles Museum, Singapore,

94

Occasional Molluscan Papers 5 (2016)

10
3