Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-29T08:51:10.610Z Has data issue: false hasContentIssue false

Nematodes that associate with terrestrial molluscs as definitive hosts, including Phasmarhabditis hermaphrodita (Rhabditida: Rhabditidae) and its development as a biological molluscicide

Published online by Cambridge University Press:  31 August 2016

A. Pieterse
Affiliation:
Department of Conservation Ecology and Entomology, Faculty of AgriSciences, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa
A.P. Malan
Affiliation:
Department of Conservation Ecology and Entomology, Faculty of AgriSciences, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa
J.L. Ross*
Affiliation:
Department of Conservation Ecology and Entomology, Faculty of AgriSciences, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa Institute of Biological and Environmental Sciences, University of Aberdeen, AB24 3UU, UK
*

Abstract

Terrestrial molluscs (Mollusca: Gastropoda) are important economic pests worldwide, causing extensive damage to a variety of crop types, and posing a health risk to both humans and wildlife. Current knowledge indicates that there are eight nematode families that associate with molluscs as definitive hosts, including Agfidae, Alaninematidae, Alloionematidae, Angiostomatidae, Cosmocercidae, Diplogastridae, Mermithidae and Rhabditidae. To date, Phasmarhabditis hermaphrodita (Schneider, 1859) Andrássy, 1983 (Rhabditida: Rhabditidae) is the only nematode that has been developed as a biological molluscicide. The nematode, which was commercially released in 1994 by MicroBio Ltd, Littlehampton, UK (formally Becker Underwood, now BASF) under the tradename Nemaslug®, is now sold in 15 different European countries. This paper reviews nematodes isolated from molluscs, with specially detailed information on the life cycle, host range, commercialization, natural distribution, mass production and field application of P. hermaphrodita.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Andrássy, I. (1976) Evolution as a basis for the systematization of nematodes. London, Pitman Publishing.Google Scholar
Andrássy, I. (1983) A taxonomic review of the sub-order Rhabditina (Nematoda: Secernentae). Paris, Office de la Recherche Scientifique et Technique, Outre-Mer. Available at http://horizon.documentation.ird.fr/exl-doc/pleins_textes/divers11-03/04391.pdf (accessed 10 January 2016).Google Scholar
Azzam, K.M. (2003) Description of the nematode Phasmarhabditis tawfiki n. sp. isolated from Egyptian terrestrial snails and slugs. Journal of the Egyptian German Society of Zoology 42, 7987.Google Scholar
Bailey, S.E.R. (2002) Molluscicidal baits for control of terrestrial gastropods. pp. 3354 in Barker, G.M. (Ed.) Molluscs as crop pests. Wallingford, CABI Publishing.Google Scholar
Baker, G.H. (2002) Helicidae and Hygromiidae as pests in cereal crops and pastures in southern Australia. pp. 193216 in Barker, G.M. (Ed.) Molluscs as crop pests. Wallingford, CABI Publishing.Google Scholar
Barker, G.M. (Ed.) (2001) The biology of terrestrial molluscs. Wallingford, CABI Publishing.CrossRefGoogle Scholar
Barker, G.M. (Ed.) (2002) Molluscs as crop pests. Wallingford, CABI Publishing.CrossRefGoogle Scholar
Blaxter, M.L., Deley, P., Garey, J.R., Liu, L.X., Scheldemann, P., Vierstraete, A., Vanfleteren, J.R., Mackey, L.Y., Dorris, M., Frisse, L.M., Vida, J.T. & Kelley Thomas, W. (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392, 7175.CrossRefGoogle ScholarPubMed
Brown, A.P., Barker, A., Hopkins, A. & Nelson, D. (2011) Application of Phasmarhabditis hermaphrodita (Nemaslug) to commercial broad acre crops. IOBC/WPRS Bulletin 64, 99104.Google Scholar
Campos-Herrera, R. (2015) Nematode pathogenesis of insects and other pests: Ecology and applied technologies for sustainable plant and crop protection. Zürich, Springer International Publishing Switzerland.Google Scholar
Charwat, S.M. & Davies, K.A. (1999) Laboratory screening of nematodes isolated from South Australia for potential as biocontrol agents of helicid snails. Journal of Invertebrate Pathology 74, 5561.Google Scholar
Coupland, J.B. (1995) Susceptibility of helicid snails to isolates of the nematode Phasmarhabditis hermaphrodita from Southern France. Journal of Invertebrate Pathology 66, 207208.CrossRefGoogle Scholar
Ester, A. & Wilson, M.J. (2005) Application of slug parasitic nematodes. pp. 421429 in Grewal, P.S., Ehlers, R.-U. & Shapiro-Ilan, D.I. (Eds) Nematodes as biocontrol agents. Wallingford, CABI Publishing.Google Scholar
Ester, A., Huiting, H.F., Molendijk, L.P.G. & Vlaswinkel, M.E.T. (2003a) The rhabditid nematode Phasmarhabditis hermaphrodita (Schneider) as a potential biological control agent to control field slugs Deroceras reticulatum (Muller) in Brussels sprouts. pp. 313318 in Dussart, G.B.J. (Ed.) Slugs and snails: Agricultural, veterinary and environmental perspectives. Monograph no. 80. Alton, British Crop Protection Council.Google Scholar
Ester, A., Van Rozen, K. & Molendijk, L.P.G. (2003b) Field experiments using the rhabditid nematode Phasmarhabditis hermaphrodita or salt as control measures against slugs in green asparagus. Crop Protection 22, 689695.Google Scholar
Ester, A., Van Rozen, K. & Hazendonk, A. (2003c) Efficacy of pesticides to control Lehmannia valentiana (Ferussac) in orchids (Cymbidium) in greenhouse experiments. pp. 8994 in Dussart, G.B.J. (Ed.) Slugs and snails: Agricultural, veterinary and environmental perspectives. Monograph no. 80. Alton, British Crop Protection Council.Google Scholar
Falcón-Ordaz, J., Mendoza-Garfias, B., Windfield-Perez, J.C., Parra-Olea, G. & Perez-Ponce de Leon, G. (2008) Angiostoma lamotheargumedoi n. sp. (Nematoda: Angiostomatidae) from the intestine of Pseudoeurycea mixteca (Caudata: Plethodontidae) in central Mexico. Revista Mexicana de Biodiversidad 79, 107112.Google Scholar
Fletcher, M.R., Hunter, K. & Barnet, E.A. (1994) Pesticide poisoning of animals 1993. London, MAFF Publications.Google Scholar
France, A. & Gerding, M. (2000) Discovery of Phasmarhabditis hermaphrodita in Chile and its pathological differences with the U.K. isolate in slug control. Journal of Nematology 32, 430.Google Scholar
Genena, M.A.M., Mostafa, F.A.M., Fouly, A.H. & Yousef, A.A. (2011) First record for the slug parasitic nematode, Phasmarhabditis hermaphrodita (Schneider) in Egypt. Archives of Phytopathology and Plant Protection 44, 340345.Google Scholar
Glen, D.M. (2000) The effects of cultural measures on cereal pests and their role in integrated pest management. Integrated Pest Management Reviews 5, 2540.Google Scholar
Glen, D.M., Wiltshire, C.W., Hughes, L., Ester, A., Van Rozen, K., Castillejo, J., Iglesias, J., Speiser, B., Coupland, J. & Gwynn, R. (2000) The use of slug-parasitic nematodes and other techniques for control of slug and snail damage in horticultural crops. BCPC: Brighton Conference pests and diseases. pp. 345350. Croydon, British Crop Protection Council.Google Scholar
Grewal, P.S., Grewal, S.K., Taylor, R.A.J. & Hammond, R.B. (2001) Application of molluscicidal nematodes to slug shelters: a novel approach to economic biological control of slugs. Biological Control 22, 7280.Google Scholar
Grewal, P.S., Grewal, S.K., Tan, L. & Adams, B.J. (2003a) Parasitism of molluscs by nematodes: types of associations and evolutionary trends. Journal of Nematology 35, 146156.Google Scholar
Grewal, S.K., Grewal, P.S. & Hammond, R.B. (2003b) Susceptibility of North American native and non-native slugs (Mollusca: Gastropoda) to Phasmarhabditis hermaphrodita (Nematoda: Rhabditidae). Biocontrol Science and Technology 13, 119125.Google Scholar
Grubisic, D., Ostrec, L.J. & Dusak, I. (2003) Biological control of slugs in vegetable crops in Croatia. pp. 115120 in Dussart, G.B.J. (Ed.) Slugs and snails: agricultural, veterinary and environmental perspectives. Monograph no. 80. Alton, British Crop Protection Council.Google Scholar
Haber, M., Schungel, M., Putz, A., Muller, S., Hasert, B. & Schulenburg, H. (2005) Evolutionary history of Caenorhabditis elegans inferred from microsatellites: evidence for spatial and temporal genetic differentiation and the occurrence of outbreeding. Molecular Biology and Evolution 22, 160173.Google Scholar
Hammond, R.B. & Byers, R.A. (2002) Agriolimacidaae and Arionidae as pests in conservation-tillage soybean and maize cropping in North America. pp. 301335 in Barker, G.M. (Ed.) Molluscs as crop pests. Wallingford, CABI Publishing.CrossRefGoogle Scholar
Huang, R.E., Ye, W., Ren, X. & Zhao, Z. (2015) Morphological and molecular characterization of Phasmarhabditis huizhouensis sp. nov. (Nematoda: Rhabditidae), a new rhabditid nematode from South China. PLoS One 10, e0144386. doi:10.1371/journal.pone.0144386.Google Scholar
Iglesias, J., Castillejo, J. & Castro, R. (2003) The effect of repeated applications of the molluscicide metaldehyde and the biocontrol nematode Phasmarhabditis hermaphrodita on molluscs, earthworms, nematodes, acarids and collembolans: a two-year study in North West Spain. Pest Management Science 59, 12171224.CrossRefGoogle ScholarPubMed
Ivanova, E.S., Spiridonov, S.E., Clark, W.C., Tourna, M., Wilson, M.J. & Barker, G.M. (2013) Description and systemic affinity of Alaninema ngata n. sp. (Alaninematidae: Panagrolaimorpha) parasitizing leaf-veined slugs (Athoracophoridae: Pulmonata) in New Zealand. Nematology 15, 859870.Google Scholar
Ivanova, E., Pham Van Luc, & Spiridonov, S. (2016) Neoalloionema tricaudatum gen. n., sp. n. (Nematoda: Alloionematidae) associated with a cyclophorid snail in Cuc Phuong Natural Park, Vietnam. Nematology 18, 109120.Google Scholar
Jones, D. (2014) EU votes to ban methiocarb slug pellets. Farmers Weekly 161, 93. Available at http://www.fwi.co.uk/arable/eu-votes-to-ban-methiocarb-slug-pellets.htm (accessed 17 January 2016).Google Scholar
Joyce, S.A., Reid, A., Driver, F. & Curran, J. (1994) Application of polymerase chain reaction (PCR) methods to identification of entomopathogenic nematodes. pp. 178187 in Burnell, A.M., Ehlers, R.U. & Masson, J.P. (Eds) Biotechnology: Genetics of entomopathogenic nematode bacteria complexes. Luxembourg, DG XII, European Commission.Google Scholar
Kanzaki, N. & Futai, K. (2002) A PCR primer set for determination of phylogenetic relationships of Bursaphelenchus species within the xylophilus group. Nematology 4, 3541.Google Scholar
Karimi, J., Kharazi-Pakadel, A. & Robert, S.J. (2003) Report of pathogenic nematodes of slugs, Phasmarhabditis hermaphrodita (Nematoda:Rhabditida) in Iran. Journal of Entomological Society of Iran 22, 7778.Google Scholar
Laznik, Z., Ross, J.L., Tóth, T., Lakatos, T., Vidrih, M. & Trdan, S. (2009) First record of the nematode Alloionema appendiculatum Schneider (Rhabditida: Alloionematidae) in Arionidae slugs in Slovenia. Russian Journal of Nematology 17, 137139.Google Scholar
Maupas, E. (1900) Modes et formes de reproduction des nématodes. Archives de Zoologie Expérimentale et Générale 8, 464642.Google Scholar
Mengert, H. (1953) Nematoden und Schneken. Zeitschrift fuer Morphologie und Oekologie der Tiere 41, 311349.Google Scholar
Morand, S., Wilson, M.J. & Glen, D.M. (2004) Nematodes (Nematoda) parasitic in terrestrial gastropods. pp. 525557 in Barker, G.M. (Ed.) Natural enemies of terrestrial molluscs. Wallingford, CABI Publishing.Google Scholar
Nadler, S.A. & Hudspeth, D.S.S. (1998) Ribosomal DNA and phylogeny of the Ascaridoidea (Nemata: Secernentea): implications for morphological evolution and classification. Molecular Phylogenetics and Evolution 10, 221236.Google Scholar
Nadler, S.A., D'Amelio, S., Dailey, M.D., Paggi, L., Siu, S. & Sakanari, J.A. (2005) Molecular phylogenetics and diagnosis of Anisakis, Pseudoterranova, and Contracaecum from Northern Pacific marine mammals. Journal of Parasitology 91, 14131429.Google Scholar
Nermut’, J., Půža, V. & Mráček, Z. (2014) The effect of different growing substrates on the development and quality of Phasmarhabditis hermaphrodita (Nematoda: Rhabditidae). Biocontrol Science and Technology 24, 10261038.Google Scholar
Nermut’, J., Půža, V. & Mráček, Z. (2015) Re-description of the slug-parasitic nematode Alloionema appendiculatum Schneider, 1859 (Rhabditida: Alloionematidae). Nematology 17, 897910.Google Scholar
Nguyen, K.B. (2007) Methodology, morphology and identification. pp. 59120 in Nguyen, B.B. & Hunt, D. (Eds) Entomopathogenic nematodes: Systematics phylogeny and bacterial symbionts. Leiden, Brill.Google Scholar
Nunn, G.B. (1992) Nematode molecular evolution . Doctoral dissertation, University of Nottingham, Nottingham, UK.Google Scholar
O'Brien, M., Spillane, C., Meade, C. & Mullins, E. (2008) An insight into the impact of arable farming on Irish biodiversity: a scarcity of studies hinders a rigorous assessment. Biology and Environment, Proceedings of the Royal Irish Academy 108, 97108.Google Scholar
Petersen, C., Hermann, R.J., Barg, M.C., Schalkowski, R., Dirksen, P., Barbosa, C. & Schulenburg, H. (2015) Travelling at a slug's pace: possible invertebrate vectors of Caenorhabditis nematodes. BMC Ecology 15, 19. doi:10.1186/s12898-015-0050-z CrossRefGoogle Scholar
Poinar, G.O. (1983) The natural history of nematodes. Princeton, New Jersey, Prentice Hall.Google Scholar
Purvis, G. & Bannon, J.W. (1992) Non-target effects of repeated methiocarb slug pellets application on carabid beetle (Coleoptera, Carbidae) activity in winter-sown cereals. Annals of Applied Biology 121, 215223.Google Scholar
Rae, R.G., Robertson, J. & Wilson, M.J. (2005) Susceptibility of indigenous U.K. earthworms and an invasive pest flatworm to the slug parasitic nematode Phasmarhabditis hermaphrodita . Biocontrol Science and Technology 15, 623626.CrossRefGoogle Scholar
Rae, R.G., Verdun, C., Grewal, P.S., Robertson, J.F. & Wilson, M.J. (2007) Biological control of terrestrial molluscs using Phasmarhabditis hermaphrodita – progress and prospects. Pest Management Science 63, 11531164.Google Scholar
Rae, R.G., Robertson, J.F. & Wilson, M.J. (2009) Chemoattraction and host preference of the gastropod parasitic nematode Phasmarhabditis hermaphrodita . Journal of Parasitology 95, 517526.Google Scholar
Ross, J.L., Ivanova, E.S., Severns, P.M. & Wilson, M.J. (2010a) The role of parasite release in invasion of the USA by European slugs. Biological Invasions 12, 603610.Google Scholar
Ross, J.L., Ivanova, E.S., Spiridonov, S.E., Waeyenberge, L., Moens, M., Nicol, G.W. & Wilson, M.J. (2010b) Molecular phylogeny of slug-parasitic nematodes inferred from 18S rRNA gene sequences. Molecular Phylogenetics and Evolution 55, 738743.Google Scholar
Ross, J.L., Ivanova, E.S., Sirgel, W.F., Malan, A.P. & Wilson, M.J. (2012) Diversity and distribution of nematodes associated with terrestrial slugs in the Western Cape Province of South Africa. Journal of Helminthology 86, 215221.Google Scholar
Ross, J.L., Ivanova, E.S., Hatteland, B.A., Brurberg, M.B. & Haukeland, S. (2016a) Survey of nematodes associated with terrestrial slugs in Norway. Journal of Helminthology 90, 582587.Google Scholar
Ross, J.L., Ivanova, E.S. & Haukeland, S. (2016b) Angiostoma norvegicum n. sp. (Nematoda: Angiostomatidae) a parasite of arionid slugs in Norway. Systematic Parasitology, in press.Google Scholar
Rueda, A., Caballero, R., Kaminsky, R. & Andrews, K.L. (2002) Vaginulidae in Central America, with emphasis on the bean slug Sarasinula plebeia (Fischer). pp. 115144 in Barker, G.M. (Ed.) Molluscs as crop pests. Wallingford, CABI Publishing.Google Scholar
Sakovich, N.J. (2002) Integrated management of Cantareus asperses (Müller) (Helicidae) as a pest of citrus in California. pp. 353336 in Barker, G.M. (Ed.) Molluscs as crop pests. Wallingford, CABI Publishing.Google Scholar
Sanderson, G. & Sirgel, W. (2002) Helicidae as pests in Australian and South African grapevines. pp. 255270 in Barker, G.M. (Ed.) Molluscs as crop pests. Wallingford, CABI Publishing.Google Scholar
Santos, M.J.G., Ferreira, N.G.C., Soares, A.M.V.M. & Loureiro, S. (2010) Toxic effects of molluscicidal baits to the terrestrial isopod Porcellionides pruinosus (Brandt, 1833). Journal of Soils and Sediments 10, 13351343.Google Scholar
Schneider, A. (1859) Über eine Nematodenlarvae und gewisse Verschiedenheiten in den Geschlechtsorganen der Nematoden. Zeitschrift für wissenschaftliche Zoologie 10, 176178.Google Scholar
Schreurs, J. (1963) Investigations on the biology, ecology and control of the giant African snail in west New Guinea. Manokwari, Manokwari Agricultural Research Station.Google Scholar
Schüder, I., Port, G. & Bennison, J. (2003) Barriers, repellents and antifeedants for slug and snail control. Crop Protection 22, 10331038.Google Scholar
South, A. (1992) Terrestrial slugs: biology, ecology and control. London, Chapman & Hall.Google Scholar
Speiser, B., Zaller, J.G. & Newdecker, A. (2001) Size-specific susceptibility of the pest slugs Deroceras reticulatum and Arion lusitanicus to the nematode biocontrol agent Phasmarhabditis hermaphrodita . BioControl 46, 311320.Google Scholar
Sudhaus, W. (1976) Vergleichende untersuchungen zur phylogenie, systematik, Ökologie, biologie und ethologie der Rhabditidae (Nematoda). Zoologica 43, 1229.Google Scholar
Sudhaus, W. (2011) Phylogenetic systematisation and catalogue of paraphyletic ‘Rhabditidae’ (Secernentea, Nematoda). Journal of Nematode Morphology and Systematics 14, 113178.Google Scholar
Sudhaus, W. & Fitch, D. (2001) Comparative studies on the phylogeny and systematics of the Rhabditidae (Nematoda). Journal of Nematology 33, 170.Google Scholar
Tan, L. & Grewal, P.S. (2001) Infection behaviour of the rhabditid nematode Phasmarhabditis hermaphrodita to the grey garden slug Deroceras reticulatum . Journal of Parasitology 87, 13491354.Google Scholar
Tandingan De Ley, I., Mundo-Ocampo, M., Yoder, M. & De Ley, P. (2007) Nematodes from vernal pools in the Santa Rosa Plateau Ecological Reserve, California I. Hirschmanniella santarosae sp. n. (Nematoda: Pratylenchidae), a cryptic sibling species of H. pomponiensis Abdel-Rahman & Maggenti, 1987. Nematology 9, 405429.Google Scholar
Tandingan De Ley, I.T., McDonnell, R.D., Lopez, S., Paine, T.D. & De Ley, P. (2014) Phasmarhabditis hermaphrodita (Nematoda: Rhabditidae), a potential biocontrol agent isolated for the first time from invasive slugs in North America. Nematology 16, 11291138.Google Scholar
Tandingan De Ley, I.T., Holovachov, O., McDonnell, R.J., Bert, W., Paine, T.D. & 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, 175193.Google Scholar
Thomas, W.K., Vida, J.T., Frisse, L.M., Mundo-Ocampo, M. & Baldwin, J.G. (1997) DNA sequences from formalin-fixed nematodes: integrating molecular and morphological approaches to taxonomy. Journal of Nematology 29, 250254.Google Scholar
Vanderburgh, D.J. & Anderson, R.C. (1987) The relationship between nematodes of the genus Cosmocercoides Wilkie, 1930 (Nematoda: Cosomcercoidea) in toads (Bufo americanus) and slugs (Deroceras laeve). Canadian Journal of Zoology 65, 16501661.Google Scholar
Vandergast, A.G. & Roderick, G.K. (2003) Mermithid parasitism of Hawaiian Tetragnatha spiders in a fragmented landscape. Journal of Invertebrate Pathology 84, 128136.Google Scholar
Vrain, T., Wakarchuk, D.A., Levesque, A.C. & Hamilton, R.I. (1992) Intraspecific rDNA restriction fragment length polymorphism in the Xiphinema americanum group. Fundamental and Applied Nematology 15, 563573.Google Scholar
Whitaker, G. & Rae, R. (2015) The gastropod parasitic nematode Phasmarhabditis hermaphrodita does not affect non-target freshwater snails Lymnaea stagnalis, Bithynia tentaculata and Planorbarius corneus . Nematology 17, 679683.Google Scholar
Williams, A.J. & Rae, R. (2015) Susceptibility of the Giant African snail (Achatina fulica) exposed to the gastropod parasitic nematode Phasmarhabditis hermaphrodita . Journal of Invertebrate Pathology 127, 122126.Google Scholar
Willis, J.C., Bohan, D.A., Choi, Y.H., Conrad, K.F. & Semenov, M.A. (2006) Use of an individual-based model to forecast the effect of climate change on the dynamic, abundance and geographical range of the pest slug Deroceras reticulatum in the UK. Global Change Biology 12, 16431657.Google Scholar
Wilson, M.J. & Barker, G.M. (2011) Slugs as pasture pests. Proceedings of the New Zealand Grassland Association 72, 241246.Google Scholar
Wilson, M.J., Glen, D.M. & George, S.K. (1993) The rhabditid nematode Phasmarhabditis hermaphrodita as a potential biological control agent for slugs. Biocontrol Science and Technology 3, 503511.Google Scholar
Wilson, M.J., Glen, D.M., George, S.K., Pearce, J.D. & Wiltshire, C.W. (1994) Biological control of slugs in winter wheat using the rhabditid nematode Phasmarhabditis hermaphrodita . Annals of Applied Biology 125, 377390.CrossRefGoogle Scholar
Wilson, M.J., Glen, D.M., Pearce, J.D. & Rodgers, P.B. (1995) Monoxenic culture of the slug parasite Phasmarhabditis hermaphrodita (Nematoda: Rhabditidae) with different bacteria in liquid and solid phase. Fundamental & Applied Nematology 18, 159166.Google Scholar
Wilson, M.J., Burch, G., Tourna, M., Aalders, L.T. & Barker, G.M. (2012) The potential of a New Zealand strain of Phasmarhabditis hermaphrodita for biological control of slugs. New Zealand Plant Protection 65, 161165.CrossRefGoogle Scholar
Wilson, W. & Rae, R. (2015) Phasmarhabditis hermaphrodita as a control agent for slugs. pp. 509522 in Campos-Herrera, R. (Ed.) Nematode pathogenesis of insects and other pests – ecology and applied technologies for sustainable plant and crop protection. Dordrecht, Springer Netherlands.Google Scholar
Zaborski, E.R., Gittenger, L.A.S. & Roberts, S.J. (2001) A possible Phasmarhabditis spp. (Nematoda: Rhabditidae) isolated from Lumbricus terrestris (Oligochaeta: Lumbricidae). Journal of Invertebrate Pathology 77, 282287.Google Scholar