Diversity of terrestrial mollusks and their helminths in artificial environments in Yoyogi Park, Tokyo, Japan lable at ScienceDirect Journal of Asia Pacific Biodiversity xxx (2017) 1e3 Contents lists[.]
Journal of Asia-Pacific Biodiversity xxx (2017) 1e3 H O S T E D BY Contents lists available at ScienceDirect Journal of Asia-Pacific Biodiversity journal homepage: http://www.elsevier.com/locate/japb Short communication Diversity of terrestrial mollusks and their helminths in artificial environments in Yoyogi Park, Tokyo, Japan Tsukasa Waki* Meguro Parasitological Museum, Meguro-ku, Tokyo 153-0064, Japan a r t i c l e i n f o a b s t r a c t Article history: Received 24 August 2016 Received in revised form December 2016 Accepted 23 December 2016 Available online xxx The author sampled terrestrial mollusks in Yoyogi Park, which is a typical urban park in Tokyo, Japan In total, 177 individuals were sampled, representing 19 species from 12 families Thirteen species were native to the area and six were introduced species which probably spread with plants and soil along human trade routes From the sampled mollusks, immature stages of the trematode family Brachylaimidae and parasitic nematodes Angiostoma sp., Phasmarhabditis sp and Mermithidae were collected The three nematodes were reported for the first time among terrestrial mollusks in Japan Copyright Ó 2017, National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA) Production and hosting by Elsevier This is an open access article under the CC BY-NC-ND license (http:// creativecommons.org/licenses/by-nc-nd/4.0/) Keywords: artificial environment helminth mollusk fauna terrestrial mollusks Introduction Terrestrial mollusks occur worldwide, and it is estimated that more than 35,000 species occur in various environments (Barker 2001) Even in artificial environments such as parks, farmlands, and public gardens, many terrestrial mollusks, including introduced species, have been reported (Hollingsworth et al 2003; Horsák et al 2004; Kawase et al 2013) In such areas we can observe introduced and native species sharing the same environment, indicating that interspecific relationships can be found between them Despite its ecological importance, few studies have reported the distribution of terrestrial mollusks in artificial environments Additionally, information on the distribution of helminths is important in order to understand the ecology of their hosts However, no study has revealed the helminth fauna in terrestrial mollusks in the Northeast Asia region, although the information is available in Europe, America, and Africa (Ivanova et al 2013; Ross et al 2010a, 2010b) Yoyogi Park, encompassing ca 540,000 m2, is a typical urban park in Tokyo, Japan (Figure 1) Most of the park is open space where many flower beds and trees have been planted Additionally, this park is adjacent to a small forest at Meiji-jingu (730,000 m2) In * Corresponding author Tel.: ỵ81 (0)3 3716 7144; fax: ỵ81 (0)3 3716 2322 E-mail address: tsukasaw@kiseichu.org Peer review under responsibility of National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA) this study, a mollusk survey was carried out to clarify the terrestrial mollusk fauna in the park Additionally, the discovery of the helminths inhabiting those mollusks is reported, including the nematodes Angiostoma, Phasmarhabditis, and Mermithidae, the first record of these nematodes from mollusks in Japan Materials and methods Terrestrial mollusks were sampled on May and 4, 2016 Large mollusks were sampled by hand To collect micromollusks with shell sizes less than w5 mm, litter and soil were collected and sieved through a mm mesh The filtrate sample was examined carefully to isolate the micromollusks The mollusks obtained were identified by the morphology of the shells and their reproductive systems (Herbert 1997) The soft tissues were dissected and rinsed with 0.4% saline solution to isolate helminths The helminths obtained were fixed and preserved in 70% ethanol and observed under the microscope for morphological identification Results In total, 177 terrestrial mollusks were obtained, representing 19 species from 12 families (Table 1) Thirteen species were native to the sampled area, and five species were introduced from Europe or America Another species, Gastrocopta armigerella, is native to http://dx.doi.org/10.1016/j.japb.2016.12.002 pISSN2287-884X eISSN2287-9544/Copyright Ó 2017, National Science Museum of Korea (NSMK) and Korea National Arboretum (KNA) Production and hosting by Elsevier This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/) Please cite this article in press as: Waki T, Diversity of terrestrial mollusks and their helminths in artificial environments in Yoyogi Park, Tokyo, Japan, Journal of Asia-Pacific Biodiversity (2017), http://dx.doi.org/10.1016/j.japb.2016.12.002 T Waki / Journal of Asia-Pacific Biodiversity xxx (2017) 1e3 Figure Survey site of the terrestrial mollusks in the present study Table Terrestrial mollusks, and helminths obtained from the mollusks, in Yoyogi Park, Japan Mollusk species Clade Caenogastropoda Family Diplommatinidae Palaina pusilla Clade Stylommatophora Family Chondrinidae Gastrocopta armigerella Family Valloniidae Vallonia costata Family Clausiliidae Euphaedusa tau Stereophaedusa japonica Family Subulinidae Allopeas pyrgula Allopeas clavulinum Paropeas achatinaceum Family Punctidae Punctidae species Family Helicarionidae Urazirochlamys doenitzii Parakaliella harimensis Helicarionidae species* Family Zonitidae Zonitoides arboreus Hawaiia minuscula Family Limacidae Lehmannia sppy Family Agriolimacidae Derocerus larvae Family Philomycidae Meghimatium bilineatum Family Bradybaenidae Acusta despecta sieboldian Aegista goniosoma Bradybaena similaris Native or introduced Number collected Helminth taxonomy Helminth family/species Number of infected hosts Native 22 d d d Introduced 22 d d d Introduced 20 d d d Native Native d d d d d d Native Native Introduced 25 d d Trematode Nematode d d Brachylaimidae Angiostoma sp d d 1 Native 17 d d d Native Native Native d d Nematode d d Mermithidae d d Introduced Introduced 53 d Nematode d Phasmarhabditis sp d Introduced 28 d d d d d d Introduced Native Nematode Phasmarhabditis sp Native Native Native 4 d d d d d d d d d *Juveniles of Helicarionidae species y Lehmannia valentiana and Lehmannia nyctelia Japan, but was probably introduced from outside the park since this snail is native to coastal forests Anatomic observation of reproductive systems revealed the coexistence of Lehmannia valentiana and Lehmannia nyctelia in Yoyogi Park; however, their juveniles, having no reproductive systems, could not be identified Because of this, the two slug species were regarded as ‘Lehmannia spp.’ in this paper (Table 1) Three Helicarionidae juveniles were obtained but could not be identified because of their lack of reproductive systems Punctum sp could not be identified because of insufficient taxonomic studies of this genus in Japan Metacercariae of the trematode family Brachylaimidae and larvae of nematodes of the family Melmithidae, Phasmarhabditis sp and Angiostoma sp were found from Paropeas achatinaceum, Helicarionidae species, Hawaiia minuscula and Meghimatium bilineatum (Table 1) The helminths were impossible to identify because few morphological characters existed due to their immaturity Discussion The present study reveals that the mollusk fauna in Yoyogi Park is a combination of native and introduced mollusks The Please cite this article in press as: Waki T, Diversity of terrestrial mollusks and their helminths in artificial environments in Yoyogi Park, Tokyo, Japan, Journal of Asia-Pacific Biodiversity (2017), http://dx.doi.org/10.1016/j.japb.2016.12.002 T Waki / Journal of Asia-Pacific Biodiversity xxx (2017) 1e3 introduced species may be transported by the transplantation of plants and soil, because terrestrial mollusks can be easily spread with plants and soil along human trade routes (National Institute for Environmental Studies 2016) Introduced terrestrial mollusks sometimes cause serious damage to native mollusks and ornamental plants (Griffiths et al 1993; Hollingsworth et al 2003), but such damage has not been reported in Yoyogi Park at the present time Terrestrial mollusks which prefer human-modified habitats, such as L valentiana, Acusta despecta sieboldiana, and Zonitoides arboreus (Ueshima et al 2001), were commonly found in the park, although some species which prefer natural environments, such as Palaina pusilla and M bilineatum, were also sampled, suggesting that the mollusk fauna was strongly influenced by the forest of Meiji-jingu which is adjacent to Yoyogi Park In this study, four helminth species were found from this small area, suggesting that the helminth fauna is diverse in the Northeast Asia region Further studies are needed to clarify the diversity of terrestrial-mollusk helminths in this region This study reported the occurrence of Melmithidae species, Phasmarhabditis sp., and Angiostoma sp in terrestrial mollusks for the first time in Tokyo, Japan, although all individuals were at the larval stage In general, Melmithidae larvae infect insects or terrestrial mollusks, and subsequently hatch out from the host to move into soil or water to grow into the adult stage (Nickle 1972; Vandergast and Roderick, 2003) Because of this, it is natural in Melmithidae that only a larval-stage nematode would be sampled from the host snail As for Angiostoma sp and Phasmarhabditis sp., their adults have been found in terrestrial mollusks in previous studies (Huang et al 2015; Morand 1992; Morand and Barker 1995; Rae et al 2007), suggesting that occurrences of larvae and adults are seasonal in the sampling area Additionally, in the United Kingdom, the nematode Phasmarhabditis hermaphrodita is used as a biotic pesticide to remove slugs (Ester and Van 2003) because the infection was lethal to the host slugs (Rae et al 2007) The Phasmarhabditis nematodes inhabiting this park may be also utilized as a biotic pesticide This study indicated that P achatinaceum was infected with metacercaria from Brachylaimidae species, the final host being birds or mammals (Alicata 1940; Sato et al 1999) From the area surrounding the park, many birds, rats, and mice have been reported (Kato et al 1994; Katoh and Kamiyama 2014), suggesting that these animals prey on host snails and act as final hosts of the Brachylaimidae Conflicts of interest There are no conflicts of interest to declare Acknowledgments I am grateful to Ron G Noseworthy for revising the manuscript References Alicata JE 1940 The life cycle of Postharmostomum gallinum, the cecal fluke of poultry The Journal of Parasitology 26:135e143 Barker GM 2001 The biology of terrestrial molluscs United Kingdom: CABI Griffiths O, Cook A, Wells SM 1993 The diet of the introduced carnivorous snail Euglandina rosea in Mauritius and its implications for threatened island gastropod faunas Journal of Zoology 229:79e89 Ester A, Van RK 2003 Effect of NemaslugÒ, salt or carvone on the slug damage in green asparagus Asparagus Research Newsletter 19:10e22 Herbert DG 1997 The terrestrial slugs of KwaZulu-Natal: diversity, biogeography and conservation (Mollusca: Pulmonata) Annals-Natal Museum 38:197e239 Hollingsworth RG, Follett PA, Armstrong JW 2003 Effects of irradiation on the reproductive ability of Zonitoides arboreus, a snail pest of orchid roots Annals of Applied Biology 143:395e399 Horsák M, Dvorák L, Juri cková L 2004 Greenhouse gastropods of the Czech Republic: current stage of research Malakológiai Tájékoztató 22:141e147 Huang RE, Ye W, Ren X, et al 2015 Morphological and molecular characterization of Phasmarhabditis huizhouensis sp nov (Nematoda: Rhabditidae), a new rhabditid nematode from South China PloS one 10:e0144386 Ivanova ES, Marianna S, Panayotova P, et al 2013 Observations on the nematode fauna of terrestrial molluscs of the Sofia area (Bulgaria) and the Crimea peninsula (Ukraine) Russian Journal of Nematology 21:41e49 Kato Y, Kohno K, Toukubo Y, et al 1994 Listeria spp carrier rats trapped at restaurants and food shops in buildings in central Tokyo Journal of the Japan Veterinary Medical Association 47:349e352 Kawase M, Nishio K, Ichihara S, et al 2013 Land mollusks in Nagoya city, Aichi prefecture, central Japan Bulletin of Segi Gakuen University 7:12e17 Katoh K, Kamiyama T 2014 Relationship between species composition of birds crossing over boundaries of patchy woodlands and surrounding landcover Journal of the Japanese Institute of Landscape Architecture 77:613e618 Morand S 1992 Angiostoma spiridonovi n sp (Nematoda: Angiostomatidae) from Limax flavus (Gastropoda: Limacidae) Journal of the Helminthological Society of Washington 59:212e217 Morand S, Barker GM 1995 Angiostoma schizoglossae n sp (Nematoda: Angiostomatidae) from the New Zealand endemic slug Schizoglossa novoseelandica (Gastropoda: Rhytididae) The Journal of Parasitology 81:94e98 National Institute for Environmental Studies 2016 Available at: https://www.nies.go jp/biodiversity/invasive/DB/detail/70390.html [Date accessed: August 2016] Nickle WR 1972 A contribution to our knowledge of the Mermithidae (Nematoda) Journal of Nematology (2):113 Rae R, Verdun C, Grewal PS, et al 2007 Biological control of terrestrial molluscs using Phasmarhabditis hermaphroditadprogress and prospects Pest Management Science 63:1153e1164 Ross JL, Ivanova ES, Severns PM, et al 2010a The role of parasite release in invasion of the USA by European slugs Biological Invasions 12:603e610 Ross JL, Ivanova ES, Spiridonov SE, et al 2010b Molecular phylogeny of slugparasitic nematodes inferred from 18S rRNA gene sequences Molecular Phylogenetics and Evolution 55:738e743 Sato H, Ihama Y, Inaba T, et al.1999 Helminth fauna of carnivores distributed in northwestern Tohoku, Japan, with special reference to Mesocestoides paucitesticulus and Brachylaima tokudai Journal of Veterinary Medical Science 61:1339e1342 Ueshima R, Saito H, Hasegawa K 2001 Land and freshwater molluscs of the Shirogane Forest in Institute for Nature Study, National Science Museum Miscellaneous Reports of the National Park for Nature Study 33:167e172 Vandergast AG, Roderick GK 2003 Mermithid parasitism of Hawaiian Tetragnatha spiders in a fragmented landscape Journal of Invertebrate Pathology 84: 128e136 Please cite this article in press as: Waki T, Diversity of terrestrial mollusks and their helminths in artificial environments in Yoyogi Park, Tokyo, Japan, Journal of Asia-Pacific Biodiversity (2017), http://dx.doi.org/10.1016/j.japb.2016.12.002 ... fauna in Yoyogi Park is a combination of native and introduced mollusks The Please cite this article in press as: Waki T, Diversity of terrestrial mollusks and their helminths in artificial environments. .. cite this article in press as: Waki T, Diversity of terrestrial mollusks and their helminths in artificial environments in Yoyogi Park, Tokyo, Japan, Journal of Asia-Pacific Biodiversity (2017),... Journal of Asia-Pacific Biodiversity xxx (2017) 1e3 Figure Survey site of the terrestrial mollusks in the present study Table Terrestrial mollusks, and helminths obtained from the mollusks, in Yoyogi