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The slugs and semislugs of Sabah, Malaysian Borneo (Gastropoda, Pulmonata: Veronicellidae, Rathouisiidae, Ariophantidae, Limacidae, Philomycidae)
Abstract and Figures
As a part of an inventory of the terrestrial malacofauna of the Malaysian state of Sabah (northern Borneo), the slugs and semislugs were given particular attention. Except for several exotic and presumed exotic species, slugs and semislugs are generally rare and infrequently encountered , mostly at high altitudes, where several short-range endemics appear to exist. We describe one new species, viz: Ibycus rachelae nov. spec. (Ariophantidae). We furthermore present new records and characters for identification of other species, namely: the veronicellids Laevicaulis alte (Férussac, 1821), Valiguna flava (Heynemann, 1885), and Semperula wallacei (Issel, 1874), the rathouisiid Atopos punctata Collinge, 1902, the ariophantids Microparmarion pollonerai Collinge & Godwin Austen, 1895, M. simrothi Collinge & Godwin Austen, 1895, Parmarion martensi Simroth, 1893, and Philippinella möllendorffi (Collinge, 1899), the limacid Deroceras retic-ulatum (Müller, 1774), and the philomycids Meghimatium striatum (Van Hasselt, 1824), M. uni-forme Laidlaw, 1937, and M. pictum (Stoliczka, 1872). For the genus Meghimatium, our taxono-my is based on a molecular phylogenetic reconstruction, which we present. Finally, we provide reports and illustrations on several species for which the available material is currently insufficient for formal identification, namely, an unidentified Atopos (Rathouisiidae), for which only juveniles (preying on Opisthostoma) were found, a second unidentified Atopos (Rathouisiidae) and an unidentified Microparmarion (Ariophantidae) for each of which only a single adult was available, as well as an unidentified Parmarion (Ariophantidae) known only from a photograph .
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... Shell visible through a left-lateral, crescent-shaped lumen in the mantle; mantle-edge on the right side with a large circular lobe. Schilthuizen & Liew 2008 ( fig. 102a-d, 106a, map 20f) Schilthuizen & Liew 2008: 296;Liew et al. 2010: Online Supporting Information, Appendix S1. -Type from Malaysia, Sabah, mount Kinabalu. ...
... Note. Because of molecular and anatomical data, Schilthuizen & Liew (2008) suspect that Meghimatium pictum is a compound entity in the present delimitation. Cross diagnosis. ...
... a-d. Ibycus rachelaeSchilthuizen & Liew, 2008, a. Juvenile animal, reconstructed from specimen preserved in alcohol, right lateral view, animal 19 mm long, b. Dorsal view, c. ...
... In general, when molecular data are processed, a comparison with identified reference sequences is required. The body colour of the genus Meghimatium, which has been often considered a diagnostic character within the genus (Simroth 1903, Minato 1976), exhibits high diversity even within a population (Wiktor et al. 2000, Schilthuizen & Liew 2008, Ito et al. 2023, and relying solely on body colour for identification can lead to misidentifications (Ito et al. 2023). Occurrence records primarily based on observation data, such as those from iNaturalist, can contribute to misunderstandings of the distributions. ...
... Meghimatium pictum from continental China, Taiwan, and Japan exhibits haplotypic diversities in the CO1 phylogeny (Fig. 3), indicating potential native distributions in these regions. In addition, although the sequences are not available in GenBank, M. pictum from Borneo displayed high phylogenetic diversity (Schilthuizen & Liew 2008), suggesting it is native there. The molecular data for M. pictum from South Korea are quite limited, but the South Korean M. pictum has a unique genetic character based on the 28S haplotype (Fig. 3) and the previous 16S phylogeny in Ito et al. (2023). ...
... Semperula wallacei (Issel, 1874) is a small veronicellid, having a body length of approximately 40 mm and width of approximately 20 mm. This species can be identified based on both its reproductive system characteristics and molecular markers (Gomes & Thomé, 2001;Schilthuizen & Liew, 2008;Gomes et al., 2010). Semperula wallacei occurs in Australia, China, Fiji, Sarawak, Sulawesi, Sumatra, Samoa, Vanuatu (Gomes & Thomé, 2001), American Samoa (Kim et al., 2016), and Japan (Hirano et al., 2019). ...
... The wide geographical distribution of S. wallacei in the Pacific Basin and its known proximity to human habitations suggest that it may be a potentially important intermediate host of A. cantonensis. Schilthuizen & Liew (2008) mentioned that, although the holotype of S. wallacei is from Sarawak and was collected during a period when alien species introductions resulting from anthropogenic activity were still relatively rare, this species appears not to be native to Borneo because it is only found in disturbed vegetation near human habitation, being present in and around most towns and cities of Sabah, as well as more widely in Southeast Asia and the Pacific islands. ...
Semperula wallacei (Issel, 1874) is a species of terrestrial slug that occurs in southeast China and the Pacific Basin and is the only species of its genus that occurs beyond the Oriental region and to the east of Wallace’s line in the Australian region, where it has probably been introduced. In this study, we report for the first time S. wallacei as an intermediate host for Angiostrongylus cantonensis (Chen, 1935) based on histological and molecular analyses of slugs from Tuamasaga, Samoa, deposited at the Medical Malacological Collection (Fiocruz-CMM). DNA was obtained from the deparafinized tissues scraped from specimen slides. Polymerase chain reaction and restriction fragment length polymorphism (PCR-RFLP) targeted to the internal transcribed spacer 2 ( ITS2 ) region were carried out using the restriction enzyme Cla I. The RFLP profile observed for our larval specimen of S. wallacei was identical to the profile previously established for A. cantonensis , demonstrating that S. wallacei can be naturally infected with A. cantonensis and is likely to be an intermediate host for this parasitic nematode species in the field. The potential for geographical range expansion of S. wallacei in the Pacific Basin, its small size, and the general role of veronicellids as crop pests and hosts of nematodes, indicate the significance of S. wallacei as an invasive species in the Pacific Basin. Our work also highlights the importance of biological collections for investigating the environmental impact of invasive species on agriculture, public health, and biodiversity conservation.
... Becoming a slug through the reduction of the shell has occurred multiple times among the stylommatophoran land snails; this has occurred particularly frequently within the limacoid snail families Ariophantidae Godwin-Austen, 1883, Helicarionidae Bourguignat, 1877, and Urocyclidae Simroth, 1889(Solem 1966Hausdorf 1998;Hyman et al. 2007;Hyman and Köhler 2020). This process, so-called 'limacization', has also produced intermediate forms between slugs and snails, known as 'semislugs', which are characterized by the presence of an external shell with a reduced number of whorls, and a loss of the ability to completely withdraw its body under the protective shell (Collinge 1902;Blanford and Godwin-Austen 1908;Solem 1966;Barker 2001;Schileyko 2003;Schilthuizen and Liew 2008;Hyman and Köhler 2020). In addition, semislugs tend to show extensive development of the mantle lobes that can completely cover its shell, providing an increased surface area for gaseous exchange (Tillier 1983;Barker 2001). ...
... Convergence in shell characters has been demonstrated in Australian helicarionids (Hyman and Köhler 2020). The lack of reproductive information has created a profound inaccuracy in their recognition and delimitation (e.g., Blanford and Godwin-Austen 1908;Solem 1966;Schilthuizen and Liew 2008;Hyman and Ponder 2010;Hyman and Köhler 2020). At present, anatomy-based approaches or those integrating molecular analyses are likely to more successfully resolve these taxonomic problems. ...
Knowledge of Thai semislugs remains scarce, especially the dancing semislug genus Cryptosemelus. Prior to the present study, only a single species has been recognized with little available information. To address this knowledge gap, we surveyed for semislugs in western and southern Thailand, which yielded three species belonging to the genus Cryptosemelus . The little-known type species C. gracilis is redescribed herein, including a comparison with the type specimens. Two additional species, C. betarmon sp. nov. and C. tigrinus sp. nov. , are described as new to science. All three species are characterized by differences in their genital anatomy, especially with respect to anatomical details of the penis, epiphallus, and spermatophore. In addition, C. tigrinus sp. nov. differs from C. gracilis and C. betarmon sp. nov. in the mantle color pattern.
... Veronicellidae Gray, 1840, known as 'leatherleaf slugs', belong to the systellommatophoran group, which can be easily recognised by having a flat body, dorsal (notum) covered by a thick mantle, ventral (hyponotum) with a narrow foot inside the pedal groove, and two pairs of tentacles: upper contractile tentacles and lower bifid tentacles (Gray 1840;Schilthuizen and Liew 2008). They are herbivorous, feeding on fresh and decaying plants, and can be found in both anthropogenic and natural habitats under tree logs, leaves, and other objects on the ground (Barker 2001). ...
The poorly studied leatherleaf slug genus Valiguna in Thailand was carefully investigated. Members of this genus are phenotypically similar, making their identification very challenging. This study clarifies the taxonomic status of all Valiguna species in Thailand by combining morphological and anatomical studies with DNA barcoding. Monophyly of all Valiguna species was confirmed by analysis of the mitochondrial COI data and that all Valiguna species have the acropleurocaulis type of penis. Currently, three Valiguna species are recognised: V. siamensis, V. semicerina Mitchueachart & Panha, sp. nov., and V. crispa Mitchueachart & Panha, sp. nov. that are new to science. For distinct characteristics, V. siamensis is characterised by having a cylindrical penis and honeycomb-like glans, V. semicerinasp. nov. has a lanceolate penis with half honeycomb-like glans, and V. crispasp. nov. has a cylindrical penis with wavy-like glans. In addition, more detailed descriptions of the radula and genitalia of all three species and their distribution are also carefully presented, enhancing the understanding of this leatherleaf slug genus in Thailand.
... The genus Meghimatium comprised phenotypically highly variable, shell-less slugs and is widely distributed in East and South Asia (Azuma, 1995;Schilthuizen and Liew, 2008;Tsai et al., 2011;Tsai and Wu, 2008;Wiktor et al., 2000). In Japan, three species of this genus have been described based on body colour, jaw, radula, and genital morphology: M. bilineatum (Benson, 1842), M. fruhstorferi (Collinge, 1901), and M. ninosawaensis Azuma, Azuma and Okamura, 2001 (Table 1). ...
East Asia, specifically the Japanese Archipelago, is a biodiversity hotspot of both vertebrates and invertebrates. Mollusks represent a burst of species diversity in this region due to the effects of biotic and abiotic factors on their morphological traits, such as shell shape and size. However, the evolutionary history of terrestrial slugs in East Asia remains unknown. In the present study, we investigated the molecular phylogeny of terrestrial slugs of the genus Meghimatium. This genus includes three described and eight undescribed species, and our study used all except for two. Based on phylogeny and the species delimitation tests, the genus Meghimatium was split into many putative species, suggesting higher species diversity than previously thought based on morphological and anatomical studies and that almost undescribed species may be inappropriate. Therefore, morphological traits, such as body size and colour, conventionally considered for classification may easily vary or be similar across geographic region. Moreover, the divergence time of this genus is almost concordant with the geographical time scale of the formation of the Japanese mainland. Our findings suggest that molecular phylogenetics helps classify Japanese Meghimatium slugs, but comprehensive taxonomic revisions using multi-locus analyses are needed.
... About 30 named species from South-East Asia to New Guinea and northern Australia are attributed to Atopos (lists of Atopos species are given by: Heynemann, 1906: 37-38;Collinge, 1908: 119;Hoffmann, 1926: 26-27; another species, overlooked in these lists, needs to be added: Atopos gravelyi Ghosh, 1915). MolluscaBase (2021) reports 23 species (although one, A. heynemanni (Simroth, 1891), as taxon inquirendum), but as stressed by De Wilde (1984), Wiktor (2003), Schilthuizen & Liew (2008) and Tan & Chan (2009), a modern revision of Atopos speciography is still lacking. Despite many detailed studies on their anatomy, most earlier contributions did not consider gross genital morphology, often dealing more with the histological structure of the organs (Simroth, 1891;Sarasin & Sarasin, 1899;Collinge, 1902aCollinge, , 1903Ghosh, 1912Ghosh, , 1913Ghosh, , 1914Ghosh, , 1915Odhner, 1917;Laidlaw, 1940;De Wilde, 1984;Wiktor, 2003). ...
A small slug found in the tropical greenhouse of the Science Museum (MUSE) of Trento (Italy) turned out to be a species of the little-known systellommatophoran family Rathouisiidae. We undertook detailed comparative anatomical and molecular studies using specimens of the MUSE slug, Rathouisia sinensis, and sequences of other systellommatophoran species deposited in GenBank to conduct a systematic and phylogenetic assessment. Analysis of the genitalia of the MUSE slug and R. sinensis revealed an unusual triaulic tritrematic structure: two separate female ducts – one for egg release (oviduct), the other for intake of allosperm (vagina) – and a separate male duct for autosperm release. Analysis of the nucleotide sequences of several mitochondrial (COI, 16S rDNA) and nuclear (18S rDNA, ITS2 flanked by 5.8S and 28S rDNA fragments, H3) gene fragments supported assignation of the MUSE slug to Rathouisiidae, but also its distinction from the other rathouisiid genera Atopos, Granulilimax, Rathouisia and an undescribed genus from the Ryukyu Islands (Japan). Therefore, we decided to describe the MUSE slug as a new species in a new genus: Barkeriella museensis gen. et sp. nov. The species is certainly an alien introduced into the tropical greenhouse of MUSE, but its origin is unknown and calls for further investigation.
The cosmopolitan terrestrial slug, Deroceras laeve (O. F. Müller, 1774), is reported in the Philippines for the first time and characterized through morphology, morphometrics, and cytochrome oxidase subunit I (COI) gene analysis. Slug samples were recovered from two administrative regions in Mindanao, Philippines. In Region X, there were two sites: Misamis Oriental (Gingoog, 664 m a.s.l.; Claveria, 937 m a.s.l.) with farms planted with cabbage (Brassica oleracea), radish (Raphanus sativus), and eggplant (Solanum melongena); and Bukidnon (Talakag, 1410 m a.s.l.) planted with cabbage. In Region XI, specimens were collected from potted ornamentals in five nurseries along the Kapatagan road, Davao del Sur, 1000-1200 m a.s.l. The external morphology of the specimens matched the published descriptions, and their identity was further confirmed by their partial COI sequences. The obtained COI sequence of the specimen in Region X showed 99-100% similarity with the voucher specimens from Mexico (KX959495, KX959496, KX959497, KX959498, and KX495499); while that of the specimen from Region XI is 100% identical to specimens collected from Japan (MW507142), Canada (MT680918 and MT941436), UK (KF894311), and Vietnam (MT941435 and MT941436). Moreover, D. laeve from Region X and Region XI shared 98% similarity with each other. Preliminary surveys show that slug occurrence is prevalent mainly in highland regions of the southern Philippines where specialty crops/high value crops like vegetables and ornamentals are cultivated. Further surveys are essential to confirm any damage that they may cause, their distribution, associated parasites, and pest status in the Philippines.
The life history traits of the invasive slug, Deroceras laeve, occurring in the Darjeeling Himalayas, India, were estimated
under laboratory conditions using the hatchlings from eggs of field-collected D. laeve. The growth pattern of D. laeve
was found to be logarithmic, rapidly increased initially, and reached a stable condition till death. The maximum life span
of D. laeve was 138±3.48 days, with slightly higher mortality during the juvenile period, which decreased gradually at
older ages. The pre-reproductive period of 37±2.7 days, reproductive period of 100.8±5.2 days, and 5.4±1.72 days
post-reproductive period of D. laeve were observed. D. laeve attained sexual maturity during 38±2.7 days, and the agespecific fecundity increased with increasing age. The hatchability of the eggs was observed to be >75% following the
incubation period of 14.25±0.49 days. The net reproductive value (R0), generation time (Tc), and finite rate of increase
(λ) were 40.01, 12.48 weeks, and 1.455, respectively. Apparently, the earlier sexual maturity, high net reproductive rate,
and shorter generation time of D. laeve are indicative of its invasive nature as well as prospective range expansion in
similar geographic locations.
During citizen-science expeditions to the Ulu Temburong National Park, Brunei, several individuals were collected of a semi-slug species of the genus Microparmarion that, based on morphology and in-the-field DNA-barcoding, was found to be an undescribed species.
In this paper, we describe Microparmarion sallehi Wu, Ezzwan & Hamdani, n. sp., after field centre supervisor Md Salleh Abdullah Bat. We provide details on the external and internal reproductive morphology, the shell and the ecology of the type locality, as well as a diagnosis comparing it with related species. DNA barcodes were generated for five individuals and used for a phylogenetic reconstruction. Microparmarion sallehi sp. n. and M. exquadratus Schilthuizen et al., 2019 so far are the only Bornean species of the genus that live in lowland forest; other species are found in montane forests.
We redescribe and figure Valiguna flava, an almost unknown Southeast-Asian land slug. Detailed morphology, radula, jaw and living specimens of Valiguna flava were studied for the first time, based on material recently collected in Borneo and on the holotype. Vl. flava is also compared with Valiguna siamensis, the only other species of the genus, which is for the first time recorded in China.
This paper gives an overview of a number of ecological, demographic, and behavioural characteristics of a group of closely related species (here referred to as O. (P.) concinnum) of the diplommatinid snail subgenus Plectostoma. Some of the members of this species complex are endemic to limestone outcrops in the Kinabatangan. This information will be an essential basis for further studies of their evolution and conservation. Our data show that Plectostoma populations are very dense and very large, with tens of millions of adults on less than a square kilometre being no exception. Adults make up the largest part of the population, and also are overrepresented among the dead shells on the forest floor. This indicates that most individuals survive to adulthood and/or adult lifespan is long compared to the time spent as juveniles. At least one-third of adults die due to predation, and probably more, since some predators do not leave marks on the shell. Mating behaviour appears to involve a " shell-mounting " phase, followed by " face-to-face " copulation. Males are characterised by a bright red shell apex, but otherwise no
The Bornean land snails of the families Pupillidae, Clausiliidae, Hydrocenidae, and Helicinidae are reviewed based on collections from 38 localities in Sarawak and Sabah and on previous records from the island. The following species are recorded: PUPILLIDAE—Pupisoma orcula (Benson), Costigo puluiusculum (Issel) new combination, Costigo moleculina Benthem-Jutting, Nesopupa moreleti (Brown), N. malayana Issel; Boysidia (Dasypupa) salpinx new subgenus and species, B. (D.) paini new species. The following Malayan species are referred to the subgenus Dasypupa: B. (D.) terae (Tomlin), B. (D.) megaphona (Benthem-Jutting), B. (D.) elephas (Benthem-Jutting), and B. (D.) perigyra (Benthem-Jutting). CLAUSILIIDAE: Phaedusa borneensis (Pfr.), P. filicostata stenotrema new species. HYDROCENIDAE : Georissa bangueyensis Smith, G . borneensis Smith, G. everetti Smith, G. gomantonensis Smith, G. hosei Godwin-Austen, G. kobelti Gredler, G. niahensis Godwin-Austen, G. saulae (Benthem-Jutting) new combination, G. scalinella (Benthem-Jutting) new combination, G. similis Smith, G. williamsi Godwin-Austen, G. hadra new species, G. pyrrhoderma new species, and G. xesta new species. Names placed in synonymy include G. flavescens Smith (= G. gomantonensis) and G. hungerfordi Godwin-Austen (= G. williamsi). No HELICINIDAE were collected. Species previously recorded from the island are listed.
