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Not in the Least Concern: Anthropogenic Influences on a South-East Asian Apple Snail Pila Scutata (Ampullariidae)

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Not in the Least Concern: Anthropogenic Influences on a South-East Asian Apple Snail Pila Scutata (Ampullariidae) Not in the Least Concern: anthropogenic influences on a South-east Asian apple snail Pila scutata (Ampullariidae) T ING H UI N G ,SIONG K IAT T AN,AMIRRUDIN A HMAD,DO V AN T U R AVINDRA C. JOSHI,WENDY Y. WANG,HEOK H UI T AN and D ARREN C.J. YEO Abstract South-east Asian apple snails, Pila spp., have been Keywords Cryptogenic species, freshwater snails, human declining since the introduction of globally invasive, confa- introductions, Peninsular Malaysia, Pila scutata,Singapore, milial South American Pomacea spp., yet Pila ecology re- threat status mains poorly studied, with most occurrence records Supplementary material for this article is available at unconfirmed. Pila scutata, a previously widespread species, https://doi.org/./S presumed native to the Malay peninsula and assessed as Least Concern in the IUCN Red List, was formerly harvested for food, and may have experienced anthropogenic translo- cations. We surveyed the Malay peninsula (specifically Introduction Peninsular Malaysia and Singapore) to investigate the cur- rent distribution and genetic diversity of P. scutata. Six po- lthough invertebrates comprise % of known species, pulations were found in Singapore, but only one in the conservation status of , % is known (Collen et al., A Peninsular Malaysia. Mitochondrial COI and S sequen- ). Amongst invertebrates the freshwater gastropods are cing revealed that the Malaysian population shared a single most at risk: at least % of assessed species are considered haplotype of both genes with the Singapore populations threatened, with the potential threat level ranging from % ( km distant). This low genetic diversity could stem (assuming no Data Deficient species are threatened) to % from a recent anthropogenic introduction, which brings (assuming all Data Deficient species are threatened; Collen into question the true native range of P. scutata and, coupled et al., ). Hotspots of freshwater gastropod diversity in- with poorly resolved taxonomy of the genus, necessitates a clude the ancient lakes of Sulawesi, Indonesia and the reassessment of its IUCN Red List status. Introduced popu- Mekong basin (Strong et al., ). Despite the high diver- lations pose a dilemma, and the lack of genetic diversity is of sity of freshwater molluscs in South-east Asia, research has concern in light of Pila decline throughout South-east Asia. mostly focussed on the zoonotic parasites they host, with lit- Our results highlight that conservation management of tle other emphasis beyond inventories of the molluscan P. scutata and its congeners must therefore be better in- hosts (e.g. Palmieri et al., ; Burch & Lohachit, ; formed by greater taxonomic resolution and more compre- Attwood, ). hensive investigations of their ecology, both in native and Among the known parasite hosts are Ampullariidae, the introduced ranges. largest freshwater snails in South-east Asia (Komalamisra et al., ; Hayes et al., ). Up to ampullariid species of the genus Pila, and multiple synonyms, have been re- corded from the region (Cowie, ). The confused tax- TING HUI NG* and DARREN C.J. YEO (Corresponding author) Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, onomy has complicated the understanding of species Singapore 117543, Republic of Singapore. E-mail [email protected] distributions, and other than a few important studies in SIONG KIAT TAN,WENDY Y. WANG and HEOK HUI TAN Lee Kong Chian Natural the s and s (Keawjam, , a,b; Pagulayan & History Museum, National University of Singapore, Singapore, Republic of Remigio, ), the current status of Pila in South-east Asia Singapore remains largely unknown. In contrast, the introduced South AMIRRUDIN AHMAD School of Marine and Environmental Sciences, Universiti Malaysia Terengganu, Terengganu, Malaysia American confamilials, Pomacea spp., have been well stud- ied because of their impacts in paddy fields (Isnaningsih & DO VAN TU Department of Aquatic Ecology and Environment, Institute of Ecology and Biological Resources, Viet Nam Academy of Science and Marwoto, ; Nghiem et al., ; Joshi et al., ). There Technology, Ha Noi, Viet Nam have been numerous anecdotal accounts of the decline of RAVINDRA C. JOSHI† Pampanga State Agricultural University, Magalang, Pila species since the introduction of Pomacea spp. (e.g. Pampanga, Philippines Halwart, ; Marwoto et al., ), but the neglect of *Present address: Department of Biology, Faculty of Science, Chulalongkorn Pila taxonomy has made it difficult to ascertain the status University, Pathumwan, Bangkok, Thailand †Also at: University of South Pacific, Suva, Fiji of the species. Although population trends of South-east Received August . Revision requested November . Asian Pila species are unknown, seven species have been as- Accepted March . First published online November . sessed as Least Concern (IUCN, ). Oryx, 2019, 53(2), 230–238 © 2018 Fauna & Flora International doi:10.1017/S0030605318000443 Downloaded from https://www.cambridge.org/core. IP address: 170.106.35.76, on 29 Sep 2021 at 05:53:08, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605318000443 South-east Asian apple snail 231 One such species is Pila scutata (Sri-Aroon & Richter, Methods ), with which various synonyms have been associated (Low et al., ; Ng et al., ; Cowie, ). It is reported Surveys and data collection to be widely distributed across South-east Asia (Low et al., ), but some occurrences are unconfirmed and others Records of P. scutata and other congeners from Singapore are probably misidentifications. For example, Keawjam and Peninsular Malaysia (collectively referred to here as () concluded from extensive surveys of Thailand am- the Malay peninsula) were obtained from available literature pullariids that previous records (Brandt, )ofP. scutata (Supplementary Table ). Specimens in the Zoological were Pila gracilis that lacked bands. Hayes et al. (b) re- Reference Collection (ZRC) of the Lee Kong Chian Natural ported on a previous misidentification of P. scutata (as Pila History Museum at the National University of Singapore conica) from Viet Nam. Further south, the distribution of were examined. Records and photographs of type material P. scutata in Peninsular Malaysia has not been mapped, of P. scutata and its synonyms (following Cowie, ), but it has been reported to be common across the peninsula and of other Pila species, were also obtained from the follow- (van Benthem Jutting, ; Berry, ). In Singapore, ing collections: the Australian Museum, Sydney (AMS), the P. scutata was formerly widespread and common in ponds Academy of Natural Sciences, Philadelphia (ANSP), the and ditches (e.g. Ponniah, ; Johnson, ; H.E. Ng, Field Museum, Chicago (FMNH), the Forest Research Insti- pers. comm.), but by the early s the species remained tute Malaysia, Kuala Lumpur, Malaysia (FRIM), the Natural extant in only a small number of localities (Clements History Museum, London (NHMUK), the Zoological Survey et al., ). It was also reportedly declining in Peninsular of India, National Zoological Collection India, Kolkata Malaysian rice fields (Joshi et al., ). (NZSI), the Forschungsinstitut und Naturmuseum Sencken- Early records of P. scutata were from streams and rivers berg, Frankfurt (SMF), the University of Michigan Museum (e.g. de Morgan, ,asAmpullaria wellesleyensis), but later of Zoology, Ann Arbor (UMMZ), and the Zoologisches surveys failed to find it in natural, undisturbed habitats (Tan Museum Hamburg (ZMH). et al., ; D.S. Johnson, unpubl. manuscript, based on work Based on records from these sources, we surveyed known in the s and early s). Records from the s indi- ampullariid localities in the Malay peninsula from August cated that P. scutata was associated with anthropogenic ha- to March . Opportunistic sampling was also carried bitats, such as fishponds, throughout the Malay peninsula out at other potentially suitable habitats, including water bod- (Johnson, ). Up to the mid th century the species ies around limestone outcrops, ditches, rice fields and ponds. was a common food item for local communities, and for live- Samples from one additional population in Singapore were stock feed (Ponniah, ; Lim et al., ). Its popularity as a obtained from Daniel J.J. Ng. Comparative material from protein source suggests that it was either naturally wide- Java in Indonesia was obtained from the collection of the spread (and abundant) or widely translocated by people, or Zoologisches Museum Berlin, Germany (the type locality of both. This species has also been introduced to Pacific islands P. scutata is Pardana in Java; Mousson, ), and other ma- (Cowie, , ; Smith, ) purportedly as food, via the terial was collected from the Philippines and Viet Nam (re- Philippines (Cowie, ; Tran et al., ). The introduced gions where P. scutata has previously been recorded; population in Hawaii has very low mitochondrial DNA di- Pagulayan & Remigio, ; Jørgensen et al., ). versity (Tran et al., ), as has been recorded for many non-native taxa that experience a genetic bottleneck during DNA analysis the introduction stage (Dlugosch & Parker, ). Despite being considered indigenous to Singapore (Ng, We extracted total genomic DNA from the foot tissue of at ; Chan, ; Tan et al., ), considering the near- least individuals of each P. scutata population, and at exclusive occurrence of P. scutata in man-made or disturbed least one individual of other Pila species obtained. We habitats, it is possible that its current
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