Abstract
Alloionema appendiculatum Schneider, 1859 (Rhabditida: Alloionematidae) is a common parasite of terrestrial molluscs capable of causing high snail mortality in heliculture. It has also been described as a parasite of the invasive slug Arion vulgaris Moquin-Tandon, 1855 (Pulmonata: Arionidae), a serious pest in central Europe. Nontheless, our knowledge about the ecology of this nematode is poor. Our study aims to provide new information about some as yet unknown aspects of the biology of this species, mainly its prevalence, attraction to slug associated cues, development, progeny production, and influence on the mortality and feeding activity of its host. The results of our study provide new information about the saprobic life cycle and natural prevalence of the species, but also show that, in standard conditions, A. appendiculatum has a very weak influence on the mortality and feeding activity of A. vulgaris. We concede that the effect of A. appendiculatum on the slug host can be strongly influenced by bacterial associates, even though the role of bacteria in nematode development is questionable and needs further research. Based on our results, A. appendiculatum does not seem to be a suitable agent for the biocontrol of A. vulgaris.
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References
Abu Hatab M, Gaugler R (2001) Diet composition and lipids of in vitro-produced Heterorhabditis bacteriophora. Biol Control 20:1–7
Cabaret J, Morand S, Aubert C, Yvore P (1988) Snail farming—a survey of breeding management, hygiene and parasitism of the garden snail, Helix aspersa Müller. J Molluscan Stud 54:209–214
Charwat SM, Davies KA (1999) Laboratory screening of nematodes isolated from South Australia for potential as biocontrol agents of helicid snails. J Invertebr Pathol 74:55–61
Chitwood BG, McIntosh A (1934) A new variety of Alloionema (Nematoda: Diplogasteridae), with a note on genus. Proc Helmithol Soc Washington 1:37–38
Čurčič BPM, Sudhaus W, Dimitrijevič RN, Makarov SE, Tomič VT (2008) Rhabditophanes schneideri (Rhabditida) phoretic on a cave pseudoscorpion. J Invertebr Pathol 99:254–256
Ehlers R-U, Shapiro-Ilan DI (2005) Mass production. In: Grewal PS, Ehlers R-U, Shapiro-Ilan DI (eds) Nematodes as biocontrol agents. CABI Publishing, Wallingford, pp 65–78
Friedman MJ (1990) Commercial production and development. In: Gaugler K, Kaya HK (eds) Entomopathogenic nematodes in biological control. CRC Press, Boca Raton, pp 153–172
Hapca SM, Budha P, Crawford JW, Young IM (2007) Movement of the nematode, Phasmarhabditis hermaphrodita in a structurally heterogeneous environment. Nematology 9:731–738
Holovachov O, Boström S, Tangingan De Ley I, Mc Donnell RJ, Alvarado S, Paine TD, De Ley P (2016) Alloionema similis n. sp., a genetically divergent sibling species of A. appendiculatum Schneider, 1859 (Rhabditida: Alloionematidae) from invasive slug in California, USA. Syst Parasitol 93:877–898
Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–176
Laznik Z, Ross JL, Trdan S (2010) Massive occurrence and identification of the nematode Alloionema appendiculatum Schneider (Rhabditida: Alloionematidae) found in Arionidae slugs in Slovenia. Acta Agric Slovenica 95:43–49
Mengert H (1953) Nematoden und Schnecken. Z Morphol Okol Tiere 48:311–349
Morand S, Wilson MJ, Glen DM (2004) Nematodes (Nematoda) parasitic in terrestrial gastropods. In: Barker GM (ed) Natural enemies of terrestrial molluscs. CABI Publishing, Wallingford, pp 525–557
Nermuť J, Půža V, Mráček Z (2012) The response of Phasmarhabditis hermaphrodita (Nematoda: Rhabditidae) and Steinernema feltiae (Nematoda: Steinernematidae) to different host-associated cues. Biol Control 61:201–206
Nermuť J, Půža V, Mráček Z (2014a) Some observations on morphology and ecology of mollusc-parasitic nematode Alloionema appendiculatum. In: 47th annual meeting of SIP, program and abstracts, 3-7 August 2014, Mainz, pp 125–126
Nermuť J, Půža V, Mráček Z (2014b) The effect of different growing substrates on the development and quality of Phasmarhabditis hermaphrodita (Nematoda: Rhabditidae). Biocontrol Sci Technol 24:1026–1038
Nermuť J, Půža V, Mráček Z (2015) Re-description of slug parasitic nematode Alloionema appendiculatum (Rhabditida: Alloionematidae). Nematology 17:897–910
Newell PF (1966) The analysis of the nocturnal behaviour of slugs on the surface of the soil. Med Biol Illustration 16:146–159
Patel MN, Stolinski M, Wright DJ (1997) Neutral lipids and the assessment of infectivity in entomopathogenic nematodes: observations on four Steinernema species. Parasitology 114:489–496
Quitt E (1971) Klimatické oblasti Československa (Climatic regions of Czechoslovakia). Academia, Studia Geographica 16, GÚ ČSAV, Brno
Rae RG, Robertson JF, Wilson MJ (2006) The chemotactic response of Phasmarhabditis hermaphrodita (Nematoda: Rhabditida) to cues of Deroceras reticulatum (Mollusca: Gastropoda). Nematology 8:197–200
Rae RG, Robertson JF, Wilson MJ (2009) Chemoattraction and host preference of the gastropod parasitic nematode Phasmarhabditis hermaphrodita. J Parasitol 95:517–526
Rae RG, Tourna M, Wilson MJ (2010) The slug parasitic nematode Phasmarhabditis hermaphrodita associates with complex and variable bacterial assemblages that do not affect its virulence. J Invertebr Pathol 104:222–226
Wilson MJ (2012) Pathogens and parasites of Terrestrial Molluscs. In: Lacey LA (ed) Manual of Techniques in Invertebrate Pathology. Academic Press, London, pp 427–439
Wilson MJ, Grewal PS (2005) Biology, production and formulation of slug-parasitic nematodes. In: Grewal PS, Ehlers R-U, Shapiro-Ilan DI (eds) Nematodes as biocontrol agents. CABI Publishing, Wallingford, pp 421–429
Wilson MJ, Glen DM, George SK, Pearce JD (1995a) Selection of a bacterium for the mass-production of Phasmarhabditis hermaphrodita (Nematoda, Rhabditidae) as a biocontrol agent for slugs. Fundam Appl Nematol 18:419–425
Wilson MJ, Glen DM, Pearce JD, Rodgers PB (1995b) Monoxenic culture of the slug parasite Phasmarhabditis Hermaphrodita (Nematoda, Rhabditidae) with different bacteria in liquid and solid-phase. Fundam Appl Nematol 18:159–166
Yang H, Jian H, Zhang S, Zhang G (1997) Quality of the entomopathogenic nematode Steinernema carpocapsae produced on different media. Biol Control 10:193–198
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This research was supported by National Agency for Agricultural Research (NAZV) Project No. QK1910270.
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Nermuť, J., Půža, V. & Mráček, Z. Bionomics of the slug-parasitic nematode Alloionema appendiculatum and its effect on the invasive pest slug Arion vulgaris. BioControl 64, 697–707 (2019). https://doi.org/10.1007/s10526-019-09967-9
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DOI: https://doi.org/10.1007/s10526-019-09967-9