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New players in the field: Ecology and biocontrol potential of three species of mollusc-parasitic nematodes of the genus Phasmarhabditis

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Abstract

Nematodes of the genus Phasmarhabditis are facultative parasites of molluscs with a world-wide distribution but, so far, only one species P. hermaphrodita has been thoroughly studied and developed as a biocontrol agent. Therefore, in the present study, we studied the ecology and biocontrol potential of three species (P. bohemica, P. bonaquaense and P. apuliae). We demonstrate that nematodes can grow in liquid and solid medium but not all the tested bacteria supported the growth of all nematodes. Pseudomonas sp. did not support the growth of P. bonaquaense and P. apuliae grow only in combination with Flavobacterium sp. Yields of dauer juveniles were higher in monoxenic cultures and in liquid medium. Generally, the most productive species was P. bohemica and the highest quality of dauers was reached in association with Flavobacterium sp. The influence of tested nematodes on feeding activity of Deroceras reticulatum and Cepaea hortensis was weak or none, respectively. But the mortality of D. reticulatum was very high both in polyxenic and monoxenic cultures and reached up to 100% within two weeks after treatment. The highest mortality, in average, was observed in P. bonaquaense or in nematodes associated with Flavobacterium sp. Monoxenized nematodes caused higher mortality than polyxenic cultures. C. hortensis was resistant to these nematodes. Our results provide the basis for further development of these nematodes as novel slug control agents.

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References

  • Andrássy I (1983) A taxonomic review of the suborder Rhabditina (Nematoda: Secernentea). Office de la Recherche Scientifique et Technique Outre-Mer, Paris

    Google Scholar 

  • Buecher EJ, Popiel I (1989) Liquid culture of entomogenous nematode Steinernema feltiae with its bacterial symbiont. J Nematol 21:500–504

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dye DW (1968) A taxonomic study of the genus Erwinia: I. The “amylovora” group. N Z J Sci 11:590–607

  • 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

    Google Scholar 

  • Glen DM, Wilson MJ, Brain P, Stroud G (2000) Feeding activity and survival of slugs, Deroceras reticulatum, exposed to the rhabditid nematode, Phasmarhabditis hermaphrodita: A model of dose response. Biol Control 17:73–81

    Article  Google Scholar 

  • Hooper DJ, Wilson MJ, Rowe JA, Glen DM (1999) Some observations on the morphology and protein profiles of the slug-parasitic nematodes Phasmarhabditis hermaphrodita and P. neopapillosa (Nematoda: Rhabditidae). Nematology 1:173–182

    Article  Google Scholar 

  • Lunau S, Stoessel S, Schmidtpeisker AJ, Ehlers R-U (1993) Establishment of monoxenic inocula for scaling up in vitro cultures of the entomopathogenic nematodes Steinernema spp. and Heterorhabditis spp. Nematologica 39:385–399

    Article  Google Scholar 

  • MacMillan K, Haukeland S, Rae R, Young I, Crawford J, Hapca S, Wilson MJ (2009) Dispersal patterns and behaviour of the nematode Phasmarhabditis hermaphrodita in mineral soils and organic media. Soil Biol Biochem 41:1483–1490

    Article  CAS  Google Scholar 

  • Mc Donnell RJ, Colton AJ, Howe DK, Denver DR (2020) Lethality of four species of Phasmarhabditis (Nematoda: Rhabditidae) to the invasive slug, Deroceras reticulatum (Gastropoda: Agriolimacidae) in laboratory infectivity trials. Biol Control 150:104349

  • Mengert H (1953) Nematoden und schnecken. Zeitschrif Für Morphologie Und Ökologie Tiere 48:311–349

    Article  Google Scholar 

  • Nermuť J, Půža V, Mráček Z (2012) The effect of intraspecific competition on the development and quality of Phasmarhabditis hermaphrodita (Rhabditida: Rhabditidae). Biocontrol Sci Technol 22:1389–1397

  • Nermuť J, Půža V, Mráček Z (2014) 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, Mekete T, Mráček Z (2016a) Phasmarhabditis bonaquaense n. sp (Nematoda: Rhabditidae), a new slug-parasitic nematode from the Czech Republic. Zootaxa 4179:530–546

    Article  Google Scholar 

  • Nermuť J, Půža V, Mráček Z (2016b) Phasmarhabditis apuliae n. sp (Nematoda: Rhabditidae), a new rhabditid nematode from milacid slugs. Nematology 18:1095–1112

    Article  Google Scholar 

  • Nermuť J, Půža V, Mekete T, Mráček Z (2017) Phasmarhabditis bohemica n. sp (Nematoda: Rhabditidae), a slug-parasitic nematode from the Czech Republic. Nematology 19:93–107

    Article  Google Scholar 

  • Nguyen KB, Smart GC (1995) Morphometrics of infective juveniles of Steinernema sp. and Heterorhabditis bacteriophora (Nematoda: Rhabditida). J Nematol 27:206–212

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Pieterse A, Tiedt LR, Malan AP, Ross JL (2017) First record of Phasmarhabditis papillosa (Nematoda: Rhabditidae) in South Africa, and its virulence against the invasive slug, Deroceras panormitanum. Nematology 19:1035–1050

    Article  CAS  Google Scholar 

  • Poinar GO, Hansen EL (1986) Associations between nematodes and bacteria. Heminthological Abstracts 55:61–68

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Rae R, Verdun C, Grewal P, Robertson JF, Wilson MJ (2007) Biological control of terrestrial molluscs using Phasmarhabditis hermaphrodita - progress and prospects. Pest Manag Sci 63:1153–1164

    Article  CAS  Google Scholar 

  • Rae RG, Robertson JF, Wilson MJ (2008) Susceptibility and immune response of Deroceras reticulatum, Milax gagates and Limax pseudoflavus exposed to the slug parasitic nematode Phasmarhabditis hermaphrodita. J Invertebr Pathol 97:61–69

    Article  Google Scholar 

  • Rae RG, Robertson JF, Wilson MJ (2009) Chemoattraction and host preference of the gastropod parasitic nematode Phasmarhabditis hermaphrodita. J Parasitol 95:517–526

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Rae R (2017) The gastropod shell has been co-opted to kill parasitic nematodes. Sci Rep 7:4745

    Article  CAS  Google Scholar 

  • Ross JL, Pieterse A, Malan AP, Ivanova E (2018) Phasmarhabditis safricana n. sp. (Nematoda: Rhabditidae), a parasite of the slug Deroceras reticulatum from South Africa. Zootaxa 4420:391–404

    Article  Google Scholar 

  • Sandström JP, Russell JA, White JP, Moran NA (2001) Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol Ecol 10:217–228

    Article  Google Scholar 

  • Sohlenius B (1968) Influence of microorganisms and temperature upon some rhabditid nematodes. Pedobiologia 8:137–145

    Google Scholar 

  • Speiser B, Zaller JG, Newdecker A (2001) Size-specific susceptibility of the pest slugs Deroceras reticulatum and Arion lusitanicus to the nematode biocontrol agent Phasmarhabditis hermaphrodita. Biocontrol 46:311–320

  • Tan L, Grewal PS (2001) Infection behavior of the rhabditid nematode Phasmarhabditis hermaphrodita to the grey garden slug Deroceras reticulatum. J Parasitol 87:1349–1354

    Article  CAS  Google Scholar 

  • Tan L, Grewal PS (2002) Endotoxin activity of Moraxella osloensis against the grey garden slug, Deroceras reticulatum. Appl Environ Microbiol 68:3943–3947

    Article  CAS  Google Scholar 

  • Tandingan De Ley I, Holovachov O, Mc Donnell RJ, Bert W, Paine TD, De Ley P (2016) Description of Phasmarhabditis californica n. sp. and first report of P. papillosa (Nematoda: Rhabditidae) from invasive slugs in the USA. Nematology 18:175–193

    Article  CAS  Google Scholar 

  • Wang X, Quinn PJ (2010) Endotoxin: lipopolysaccharides of Gram-negative bacteria. In: Wang X, Quinn PJ (eds) Endotoxins: structure, function and recognition. Springer, Dordecht, pp 3–25

    Chapter  Google Scholar 

  • Wilson MJ, Glen DM, George SK (1993) The rhabditid nematode Phasmarhabditis hermaphrodita as a potential biological control agent for slugs. Biocontrol Sci Technol 3:503–511

  • Wilson MJ, Glen DM, George SK, Pearce JD (1995a) Selection of a bacterium for the mass-production of Phasmarhabditis hermaphrodita (Nematoda, Rhabditidae) as a Biol Control agent for slugs. Fundam Appl Nematol 18:419–425

    Google Scholar 

  • 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

    Google Scholar 

  • Wilson MJ, Hughes LA, Hamacher GM, Glen DM (2000) Effects of Phasmarhabditis hermaphrodita on non-target molluscs. Pest Manag Sci 56:711–716

    Article  CAS  Google Scholar 

  • 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

    Chapter  Google Scholar 

Download references

Funding

This study was supported by the Biology Centre CAS, Institute of Entomology (RVO: 60077344).

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JN wrote the manuscript, designed and conducted experiments and participated to the statistical analysis. MH/LFO participated to the experiments and statistical analysis. VP conducted statistical analyses and revised the manuscript. All authors read and approved the manuscript.

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Correspondence to Jiří Nermuť.

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Nermuť, J., Holley, M., Ortmayer, L.F. et al. New players in the field: Ecology and biocontrol potential of three species of mollusc-parasitic nematodes of the genus Phasmarhabditis. BioControl 67, 543–553 (2022). https://doi.org/10.1007/s10526-022-10160-8

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  • DOI: https://doi.org/10.1007/s10526-022-10160-8

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