, Volume 64, Issue 6, pp 697–707 | Cite as

Bionomics of the slug-parasitic nematode Alloionema appendiculatum and its effect on the invasive pest slug Arion vulgaris

  • Jiří NermuťEmail author
  • Vladimír Půža
  • Zdeněk Mráček


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.


Arion vulgaris Alloionema appendiculatum Acinetobacter Pseudomonas Neisseria 



This research was supported by National Agency for Agricultural Research (NAZV) Project No. QK1910270.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abu Hatab M, Gaugler R (2001) Diet composition and lipids of in vitro-produced Heterorhabditis bacteriophora. Biol Control 20:1–7CrossRefGoogle Scholar
  2. 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 54:209–214CrossRefGoogle Scholar
  3. Charwat SM, Davies KA (1999) Laboratory screening of nematodes isolated from South Australia for potential as biocontrol agents of helicid snails. J Invertebr Pathol 74:55–61CrossRefGoogle Scholar
  4. Chitwood BG, McIntosh A (1934) A new variety of Alloionema (Nematoda: Diplogasteridae), with a note on genus. Proc Helmithol Soc Washington 1:37–38Google Scholar
  5. Čurčič BPM, Sudhaus W, Dimitrijevič RN, Makarov SE, Tomič VT (2008) Rhabditophanes schneideri (Rhabditida) phoretic on a cave pseudoscorpion. J Invertebr Pathol 99:254–256CrossRefGoogle Scholar
  6. 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 65–78CrossRefGoogle Scholar
  7. Friedman MJ (1990) Commercial production and development. In: Gaugler K, Kaya HK (eds) Entomopathogenic nematodes in biological control. CRC Press, Boca Raton, pp 153–172Google Scholar
  8. Hapca SM, Budha P, Crawford JW, Young IM (2007) Movement of the nematode, Phasmarhabditis hermaphrodita in a structurally heterogeneous environment. Nematology 9:731–738CrossRefGoogle Scholar
  9. 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 93:877–898CrossRefGoogle Scholar
  10. Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, New York, pp 115–176Google Scholar
  11. 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 95:43–49Google Scholar
  12. Mengert H (1953) Nematoden und Schnecken. Z Morphol Okol Tiere 48:311–349CrossRefGoogle Scholar
  13. 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 525–557CrossRefGoogle Scholar
  14. 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 61:201–206CrossRefGoogle Scholar
  15. 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 125–126Google Scholar
  16. 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 24:1026–1038CrossRefGoogle Scholar
  17. Nermuť J, Půža V, Mráček Z (2015) Re-description of slug parasitic nematode Alloionema appendiculatum (Rhabditida: Alloionematidae). Nematology 17:897–910CrossRefGoogle Scholar
  18. Newell PF (1966) The analysis of the nocturnal behaviour of slugs on the surface of the soil. Med Biol Illustration 16:146–159Google Scholar
  19. Patel MN, Stolinski M, Wright DJ (1997) Neutral lipids and the assessment of infectivity in entomopathogenic nematodes: observations on four Steinernema species. Parasitology 114:489–496CrossRefGoogle Scholar
  20. Quitt E (1971) Klimatické oblasti Československa (Climatic regions of Czechoslovakia). Academia, Studia Geographica 16, GÚ ČSAV, BrnoGoogle Scholar
  21. Rae RG, Robertson JF, Wilson MJ (2006) The chemotactic response of Phasmarhabditis hermaphrodita (Nematoda: Rhabditida) to cues of Deroceras reticulatum (Mollusca: Gastropoda). Nematology 8:197–200CrossRefGoogle Scholar
  22. Rae RG, Robertson JF, Wilson MJ (2009) Chemoattraction and host preference of the gastropod parasitic nematode Phasmarhabditis hermaphrodita. J Parasitol 95:517–526CrossRefGoogle Scholar
  23. 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 104:222–226CrossRefGoogle Scholar
  24. Wilson MJ (2012) Pathogens and parasites of Terrestrial Molluscs. In: Lacey LA (ed) Manual of Techniques in Invertebrate Pathology. Academic Press, London, pp 427–439CrossRefGoogle Scholar
  25. 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 421–429CrossRefGoogle Scholar
  26. 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 18:419–425Google Scholar
  27. 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 18:159–166Google Scholar
  28. Yang H, Jian H, Zhang S, Zhang G (1997) Quality of the entomopathogenic nematode Steinernema carpocapsae produced on different media. Biol Control 10:193–198CrossRefGoogle Scholar

Copyright information

© International Organization for Biological Control (IOBC) 2019

Authors and Affiliations

  • Jiří Nermuť
    • 1
    Email author
  • Vladimír Půža
    • 1
  • Zdeněk Mráček
    • 1
  1. 1.Biology Centre CAS, Institute of EntomologyLaboratory of Entomopathogenic NematodesČeské BudějoviceCzech Republic

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