Dispersion of nematodes (Rhabditida) in the guts of slugs and snails
DOI:
https://doi.org/10.25674/4jp6-0v30Keywords:
rhabditids, accidental phoresis, endophoresis | necromeny, dispersal, PhasmarhabditisAbstract
A survey was carried out to find non-parasitic nematodes associated with slugs and snails in order to elucidate the initial phase of endophoresis and necromeny in gastropods. 78 % of the specimens of the 12 terrestrial gastropod species surveyed carried nematodes. A total of 23 nematode species were detected alive and propagable in gastropod faeces, with 16 different species found in Arion rufus alone. Most were saprobiontic rhabditids, with species of Caenorhabditis, Oscheius and Panagrolaimus appearing with some regularity. The nematodes were accidentally ingested with food and survived the passage through the digestive tract, allowing them to be transported to suitable microhabitats such as decaying fruits or fungi. The intestines of snails and slugs taken from hibernation or aestivation were free of nematodes. Seven gastropod species were experimentally infected with eight rhabditid species, all of which were able to persist uninjured in the intestines of the gastropods for two to five days before being excreted with the faeces. A list of nematode species accidentally associated with gastropods is compiled from the literature for comparison. The role of gastropods in spreading nematodes and other small animals (a few observations on rotifers and mites are mentioned) deserves more attention.
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References
Arias, R. O. & H. H. Crowell (1963): A contribution to the biology of the gray garden slug. – Bulletin of the Southern California Academy of Sciences 62: 83 – 97.
Andrássy, I. (2007): Free-living nematodes of Hungary (Nematoda errantia), II. Pedozoologica Hungarica, No. 4. Hungarian Natural History Museum, Budapest: 496 pp.
Azzam, K. M. (2006): Survey of terrestrial gastropods, their host plants and parasitic nematodes as biocontrol agents. – Journal of the Egyptian German Society of Zoology 49D: 49 – 61.
Azzam, K. M. & M. H. Belal (2006): Survey on the nematodes isolated from aquatic snails and their potential as bio-control agents of snails. – Bulletin of the Faculty of Agriculture, Cairo University 57: 185 – 198.
Bretschneider, M. (2007): Untersuchungen zur Phoresie von Nematoden durch terrestrische Gastropoden. – Diploma thesis, FU Berlin.
Charwat, S. M. & K. A. Davies (1999): Laboratory screening of nematodes isolated from South Australia for potential as biocontrol agents of helicid snails. – Journal of Invertebrate Pathology 74: 55 – 61.
Chitwood, B. G. & M. B. Chitwood (1932): Pathoaphelenchus parietinus (= Aphelenchus ormerodis) in the intestine of Philomycus dorsalis. – Journal of Parasitology 19: 91.
Chitwood, B. G. & M. B. Chitwood (1934): Daubaylia potomaca n. sp., a nematode parasite of snails, with a note on other nemas associated with molluscs. – Proceedings of the Helminthological Society of Washington 1: 8 – 9.
Chitwood, B. G. & M. B. Chitwood (1937): Snails as hosts and carriers of nematodes and Nematomorpha. – The Nautilus 50: 130 – 135.
Cobb, N. A. (1888): Beiträge zur Anatomie und Ontogenie der Nematoden. Fischer, Jena: 36 pp.
Cook, R., B. J. Thomas & K. A. Mizen (1989): Dissemination of white clover mosaic virus and stem nematode, Ditylenchus dipsaci, by the slug Deroceras reticulatum. Slugs and snails of the world. British Crop protection Council. Monograph 41: 107 – 112.
De Ley, I. T., R. D. McDonnell, S. Lopez, T. D. Paine & P. De Ley (2014): Phasmarhabditis hermaphrodita (Nematoda: Rhabditidae), a potential biocontrol agent isolated for the first time from invasive slugs in North America. – Nematology 16: 1129 – 1138.
De Ley, I. T., R. D. McDonnell, T. D. Paine & P. De Ley (2017): Phasmarhabditis: The slug and snail parasitic nematodes in North America. In: Abd-Elgawad, M. M. M., T. H. Askary & J. Coupland (eds): Biocontrol Agents: Entomopathogenic and Slug Parasitic Nematodes. CABI, Wallingford, UK, Boston, USA: 560 – 578.
Félix, M.-A. & F. Duveau (2012): Population dynamics and habitat sharing of natural populations of Caenorhabditis elegans and C. briggsae. – BMC Biology 10: 59.
Fox, I. & I. García-Moll (1962): Echiniscus molluscorum, new tardigrade from the feces of the land snail, Bulimulus exilis (Gmelin) in Puerto Rico (Tardigrada: Scutechiniscidae). – Journal of Parasitology 48: 177 – 181.
Gleich, J. G., F. F. Gilbert & N. P. Kutscha (1977): Nematodes in terrestrial gastropods from central Maine. – Journal of Wildlife Diseases 13: 43 – 46.
Godan, D. (1983): Pest Slugs and Snails. Biology and Control. Springer, Berlin, Heidelberg, New York: 445 pp.
Huang, R.-E., W. Ye, X. Ren & Z. Zhao (2015): Morphological and molecular characterization of Phasmarhabditis huizhouensis sp. nov. (Nematoda: Rhabditidae), a new rhabditid nematode from South China. PLoS One 10: e0144386.
Kiontke, K. & W. Sudhaus (2006): Ecology of Caenorhabditis species. In: The C. elegans research community (ed.): WormBook.
Körner, H. (1954): Die Nematodenfauna des vergehenden Holzes und ihre Beziehungen zu den Insekten. – Zoologische Jahrbücher (Systematik) 82: 245 – 353.
Marcus, E. & E. Marcus (1963): On Brazilian supralittoral and brackish water snails. – Boletim do Instituto Oceanográfico 13: 41 – 52.
Maupas, É. (1899): La mue et l’enkystement chez les nématodes. – Archive Zoologique expérimentelle et générale 7: 563 – 628.
Maupas, É. (1916): Nouveaux Rhabditis d’Algérie. – Comptes Rendus de la Société Biologique (Paris) 79: 607 – 613.
Maupas, É. (1919): Essais d’hybridation chez des nématodes. – Bulletin Biologique de la France et de la Belgique 52: 466 – 498.
Mengert, H. (1953): Nematoden und Schnecken. – Zeitschrift für Morphologie und Ökologie der Tiere 41: 311–349.
Nermut', J., V. Půža & Z. Mráček (2016): Phasmarhabditis apuliae n. sp. (Nematoda: Rhabditidae), a new rhabditid nematode from milacid slugs. – Nematology 18: 1095 – 1112.
Odaibo, A. B., A. J. Dehinbo, L. K. Olofintoye & O. A. Falode (2000): Occurrence and distribution of Rhabditis axei (Rhabditida; Rhabditidae) in African giant snails in southwestern Nigeria. – Helminthologia 37: 233 – 235.
Olofintoye, L. K. & O. F. Olorunniyi (2016): Intensity of Rhabditis axei at different parts of gastrointestinal tracts of Archachatina marginata ovum and Achatina achatina. – Journal of Bio Innovation 5: 182 – 185.
Örley, L. (1886): Die Rhabditiden und ihre medicinische Bedeutung. Friedländer, Berlin: 84 pp.
Petersen, C., R. J. Hermann, M.-C. Barg, R. Schalkowski, P. Dirksen, C. Barbosa & H. Schulenburg (2015): Travelling at a slug’s pace: possible invertebrate vectors of Caenorhabditis nematodes. – BMC Ecology 15: 19.
Pieterse, A. (2016): Investigating the potential of indigenous nematode isolates to control invasive molluscs in canola. – Thesis, Stellenbosch University: 120 pp.
Pieterse, A., A. P. Malan, L. M. Kruitbos, W. Sirgel & J. L. Ross (2017a): Nematodes associated with terrestrial slugs from canola fields and ornamental nurseries in South Africa. – Zootaxa 4312: 194 – 200.
Pieterse, A., A. P. Malan & J. L. Ross (2017b): Nematodes that associate with terrestrial molluscs as definitive hosts, including Phasmarhabditis hermaphrodita (Rhabditida: Rhabditidae) and its development as a biological molluscicide. – Journal of Helminthology 91: 517 – 527.
Ratanarat-Brockelman, C. & G. J. Jackson (1974): Rhabditis maupasi: occurrence in food snails and cultivation. – Experimental Parasitology 36: 114 – 122.
Reiter, M. (1928): Zur Systematik und Ökologie der zweigeschlechtlichen Rhabditiden. – Arbeiten aus dem Zoologischen Institut der Universität Innsbruck 3: 3 – 94.
Ross, J. L., E. S. Ivanova, P. M. Severns & M. J. Wilson (2010): The role of parasite release in invasion of the USA by European slugs. – Biological Invasions 12: 603 – 610.
Ross, J. L., E. S. Ivanova, W. F. Sirgel, A. P. Malan & M. J. Wilson (2012): Diversity and distribution of nematodes associated with terrestrial slugs in the Western Cape Province of South Africa. – Journal of Helminthology 86: 215 – 221.
Ross, J. L., E. S. Ivanova, S. Spiridonov, G. Nicol & M. J. Wilson (2009): Phylogeny of nematodes associated with terrestrial slugs inferred from 18S rRNA sequences. – Insect Pathogens and Insect Parasitic Nematodes IOBC/wprs Bulletin 45: 473 – 475.
Schneider, A. (1866): Monographie der Nematoden. Reimer, Berlin: 357 pp.
Shinohara, T. (1960): [Studies on Rhabditis (Nematoda, Rhabditidae).] – Journal of the Kurume Medical Association 23: 2777 – 2819 (In Japanese).
Sudhaus, W. (1976): Vergleichende Untersuchungen zur Phylogenie, Systematik, Ökologie, Biologie und Ethologie der Rhabditidae (Nematoda). – Zoologica 43: 1 – 229.
Sudhaus, W. (2010): Preadaptive plateau in Rhabditida (Nematoda) allowed the repeated evolution of zooparasites, with an outlook on evolution of life cycles within Spiroascarida. – Palaeodiversity 3, Supplement: 117–130.
Sudhaus, W. (2011): Phylogenetic systematisation and catalogue of paraphyletic ’Rhabditidae’ (Secernentea, Nematoda). – Journal of Nematode Morphology and Systematics 14: 113 – 178.
Sudhaus, W. & K. Kiontke (1996): Phylogeny of Rhabditis subgenus Caenorhabditis (Rhabditidae, Nematoda). – Journal of Zoological Systematics and Evolutionary Research 34: 217 – 233.
Türke, M., M. Lange & N. Eisenhauer (2018): Gut shuttle service: endozoochory of dispersal-limited soil fauna by gastropods. – Oecologia 186: 655 – 664.
Wang. A., G. Ash, M. Hodda & F. G. Jahromi (2015): Molecular phylogeny inferred from 18S rRNA gene sequences of nematodes associated with Cernuella virgata, a pest snail in Australia. – Journal of Phylogenetics & Evolutionary Biology 3: 148.
Wouts, W. M., Z. Mráček, S. Gerdin & R. A. Bedding (1982): Neoaplectana Steiner, 1929 a junior synonym of Steinernema Travassos, 1927 (Nematoda; Rhabditida). Systematic Parasitology 4: 147 – 154.
Yokoo, T. & K. Okabe (1968): Two new species of genus Rhabditis (Nematoda: Rhabditidae) found in the intermediate host of Schistosoma japonica, Oncomelania hupensis nosophora and Oncomelania hupensis formosana. – Agricultural Bulletin of Saga University 25: 69 – 78.
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