In the period from August to October 2018, 140 specimens of the Spanish slug, Arion vulgaris, were collected from Podbrezje, Slovenia. Slugs were dissected and examined for the presence of parasitic nematodes within the cadavers. Identification of the nematodes was conducted using morphological and molecular techniques and confirmed the presence of Phasmarhabditis papillosa. This is the first record of P. papillosa from the mollusc host, A. vulgaris. Laboratory experiments aimed at testing the efficacy of P. papillosa against A. vulgaris were conducted using nematodes grown in vivo. Nematodes were applied at concentration rates of 50, 100 and 200 nematodes slug−1, respectively. Three weeks following treatment, the mortality of slugs was confirmed in all treatments (50 nematodes slug−1, 37.4 ± 2.7%; 100 nematodes slug−1, 48.4 ± 2.7%; 200 nematodes slug−1, 50.6 ± 2.7%). However, the pathogenesis of P. papillosa was observed first in the treatments with the lowest nematode dose at 4 days after treatments, while a decrease in the feeding behaviour of slugs was noted first in the treatments with the highest nematode dose. Future opportunities for the potential use of P. papillosa as a biological control agent against slugs are discussed. This is the first report of P. papillosa from Slovenia, and of its virulence against A. vulgaris.
Purchase
Buy instant access (PDF download and unlimited online access):
Institutional Login
Log in with Open Athens, Shibboleth, or your institutional credentials
Personal login
Log in with your brill.com account
Andrássy, I. (1983). A taxonomic review of the suborder Rhabditina (Nematoda: Secernentia). Paris, France, ORSTOM.
Anonymous (2018). Restrictions on the use of metaldehyde to protect wildlife. London, Crown copyright. Available from: https://www.gov.uk/government/news/restrictions-on-the-use-of-metaldehyde-to-protect-wildlife (accessed 21 December 2018).
Bailey, S.E.R. (2002). Molluscicidal baits for control of terrestrial gastropods. In: Barker, G.M. (Ed.). Molluscs as crop pests. Wallingford, UK, CABI Publishing, pp. 33-54. DOI: 10.1079/9780851993201.0033
Barker, G.M. (2001). The biology of terrestrial molluscs. Wallingford, UK, CAB International. DOI: 10.1079/9780851993188.0000
Barker, G.M. (2002). Molluscs as crop pests. Wallingford, UK, CAB International. DOI: 10.1079/9780851993201.0000
Buhl, K., Bond, C. & Stone, D. (2013). Iron phosphate general fact sheet. Corvallis. OR, USA, National Pesticide Information Center, Oregon State University Extension Services. Available from: http://npic.orst.edu/factsheets/ironphosphategen.html (Accessed 08 January 2019).
Castle, G.D., Mills, G.A., Gravell, A., Jones, L., Townsend, I., Cameron, D.G. & Fones, G.R. (2017). Review of the molluscicide metaldehyde in the environment. Environmental Science: Water Research & Technology 3, 415-428. DOI: 10.1039/C7EW00039A
Choi, Y.H., Bohana, D.A., Potting, R.P.J., Semenov, M.A. & Glen, D.M. (2006). Individual based model of slug population and spatial dynamics. Ecological Modelling 190, 336-350. DOI: 10.1016/j.ecolmodel.2005.04.019
Dörler, D., Scheucher, A. & Zaller, J.G. (2019). Efficacy of chemical and biological slug control measures in response to watering and earthworms. Scientific Reports 9, 1-8. DOI: 10.1038/s41598-019-39585-5
Douglas, M.R. & Tooker, J.F. (2012). Slug (Mollusca: Agriolimacidae, Arionidae) ecology and management in no-till field crops, with an emphasis on the mid-Atlantic region. Journal of Integrated Pest Management 3, 1-9. DOI: 10.1603/IPM11023
Ehlers, R.-U. (1998). Entomopathogenic nematodes – save biocontrol agents for sustainable systems. Phytoprotection 79, 94-102. DOI: 10.7202/706164ar
Evans, N.J. (1986). An investigation on the status of the terrestrial slugs Arion ater ater (L.) and Arion ater rufus (L.) (Mollusca, Gastropoda, Pulmonata) in Britain. Zoological Scripta 15, 313-322. DOI: 10.1111/j.1463-6409.1986.tb00232.x
Frank, T. (1998). Slug damage and numbers of the slug pests, Arion lusitanicus and Deroceras reticulatum, in oilseed rape grown beside sown wildflower strips. Agricultural Ecosystems & Environment 67, 67-78. DOI: 10.1016/S0167-8809(97)00108-4
Glare, T., Caradus, J., Gelernter, W., Jackson, T., Keyhani, N., Köhl, J., Marrone, P., Morin, L. & Stewart, A. (2012). Have biopesticides come of age? Trends in Biotechnology 30, 250-258. DOI: 10.1016/j.tibtech.2012.01.003
Glen, D.M. & Moens, R. (2002). Agriolimacidae, Arionidae and Milacidae as pests in west European cereals. In: Barker, G.M. (Ed.). Molluscs as crop pests. Wallingford, UK, CAB International, pp. 271-300. DOI: 10.1079/9780851993201.0425
Grimm, B. & Schaumberger, K. (2002). Daily activity of the pest slug Arion lusitanicus under laboratory conditions. Annals of Applied Biology 141, 35-44. DOI: 10.1111/j.1744-7348.2002.tb00193.x
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
Ivanova, E.S. & Spiridonov, S.E. (2010). Angiostoma glandicola sp. n. (Nematoda: Angiostomatidae): a parasite in the land snail Megaustenia sp. from the Cat Tien Forest, Vietnam. Journal of Helminthology 84, 297-304. DOI: 10.1017/S0022149X09990678
Kanzaki, N. & Futai, K. (2002). A PCR primer set for determination of phylogenetic relationships of Bursaphelenchus species within the xylophilus group. Nematology 4, 35-41. DOI: 10.1163/156854102760082186
Koppenhöfer, A.M. & Kaya, H.K. (1995). Density-dependent effects on Steinernema glaseri (Nematoda: Steinernematidae) within an insect host. Journal of Parasitology 81, 797-799. DOI: 10.2307/3283982
Kozłowski, J. (2007). The distribution, biology, population dynamics and harmfulness of Arion lusitanicus Mabille, 1868 (Gastropoda: Pulmonata: Arionidae) in Poland. Journal of Plant Protection Research 47(3), 219-230.
Kruitbos, L.M., Heritage, S., Hapca, S. & Wilson, M.J. (2009). Influence of substrate on the body-waving behaviour of nematodes. Nematology 11, 917-925. DOI: 10.1163/156854109X443433
Langan, A.M. & Shaw, E.M. (2006). Responses of the earthworm Lumbricus terrestris (L.) to iron phosphate and metaldehyde slug pellet formulations. Applied Soil Ecology 34, 184-189. DOI: 10.1016/j.apsoil.2006.02.003
Laznik, Ž. & Trdan, S. (2016). Is a combination of different natural substances suitable for slug (Arion spp.) control? Spanish Journal of Agricultural Research 14, 1-7. DOI: 10.5424/sjar/2016143-9053
Laznik, Ž., Tóth, T., Lakatos, T., Vidrih, M. & Trdan, S. (2009). First record of Steinernema feltiae (Filipjev) (Rhabditida: Steinernematidae) in Slovenia. Helminthologia 46, 135-138. DOI: 10.2478/s11687-009-0026-7
Laznik, Ž., Križaj, D. & Trdan, S. (2011). The effectiveness of electrified fencing using copper electrodes for slug (Arion spp.) control with direct electric current and voltage. Spanish Journal of Agricultural Research 9, 894-900. DOI: 10.5424/sjar/20110903-412-10
MacMillan, K., Haukeland, S., Rae, R., Young, I., Crawford, J., Hapca, S. & Wilson, M.J. (2009). Dispersal patterns and behaviour of the nematode Phasmarhabditis hermaphrodita in mineral soils and organic media. Soil Biology and Biochemistry 41, 1483-1490. DOI: 10.1016/j.soilbio.2009.04.007
Majić, I., Sarajlić, A., Lakatos, T., Tóth, T., Raspudić, E., Puškadija, Z., Kanižai Šarić, G. & Laznik, Ž. (2019). Virulence of new strain of Heterorhabditis bacteriophora from Croatia against Lasioptera rubi. Plant Protection Science 55, 134-141. DOI: 10.17221/119/2018-PPS
Mengert, H. (1953). Nematoden und Schnecken. Zeitschrift für Morphologie und Ökologie der Tiere 4, 311-349.
Morand, S., Wilson, M.J. & Glen, D.M. (2004). Nematodes (Nematoda) parasitic in terrestrial gastropods. In: Barker, G.M. (Ed.). Natural enemies of terrestrial molluscs. Wallingford, UK, CAB International, pp. 525-557. DOI: 10.1079/9780851993195.0525
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, 1413-1429. DOI: 10.1645/GE-522R.1
Nermut’, J., Půža, V. & Mráček, Z. (2012). The effect of intraspecific competition on the development and quality of Phasmarhabditis hermaphrodita (Rhabditida: Rhabditidae). Biocontrol Science and Technology 22, 1389-1397. DOI: 10.1080/09583157.2012.730604
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, 1026-1038. DOI: 10.1080/09583157.2014.915926
Nguyen, K.B. (2007). Methodology, morphology and identification. In: Nguyen, K.B. & Hunt, D.J. (Eds). Hunt, D.J. & Perry, R.N.). Entomopathogenic nematodes: systematics phylogeny and bacterial symbionts. Nematology Monographs and Perspectives 5 (Series editors: Leiden, The Netherlands, Brill, pp. 59-120. DOI: 10.1163/ej.9789004152939.i-816.25
Nicolopoulou-Stamati, P., Maipas, S., Kotampasi, C., Stamatis, P. & Hens, L. (2016). Chemical pesticides and human health: the urgent need for a new concept in agriculture. Frontiers in Public Health 4, 148. DOI: 10.3389/fpubh.2016.00148
Pfenninger, M., Weigand, A., Bálint, M. & Klussmann-Kolb, A. (2014). Misperceived invasion: the Lusitanian slug (Arion lusitanicus auct. non-Mabille or Arion vulgaris Moquin-Tandon 1855) is native to central Europe. Evolutionary Applications 7, 702-713. DOI: 10.1111/eva.12177
Pieterse, A., Tiedt, L.R., Malan, A.P. & Ross, J.L. (2017). First record of Phasmarhabditis papillosa (Nematoda: Rhabditidae) in South Africa, and its virulence against the invasive slug, Deroceras panormitanum. Nematology 19, 1035-1050. DOI: 10.1163/15685411-00003105
Purvis, G. & Bannon, J.W. (1992). Non-target effects of repeated methiocarb slug pellets application on carabid beetle (Coleoptera, Carabidae) activity in winter-sown cereals. Annals of Applied Biology 121, 215-223. DOI: 10.1111/j.1744-7348.1992.tb03453.x
Půža, V. & Mráček, Z. (2005). Seasonal dynamics of entomopathogenic nematodes of the genera Steinernema and Heterorhabditis as a response to abiotic factors and abundance of insect hosts. Journal of Invertebrate Pathology 89, 116-122. DOI: 10.1016/j.jip.2005.04.001
Rae, R., 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, 1153-1164. DOI: 10.1002/ps.1424
Rae, R.G., Robertson, J.F. & Wilson, M.J. (2008). Susceptibility and immune response of Deroceras reticulatum, Milax gagates and Limax pseudoflavus exposed to the slug parasitic nematode Phasmarhabditis hermaphrodita. Journal of Invertebrate Pathology 97, 61-69. DOI: 10.1016/j.jip.2007.07.004
Ross, J.L. (2019). Riding the slime wave: gathering global data on slug control. Taunton, UK, Nuffield Farming Scholarships Trust Report.
Ross, J.L., Ivanova, E.S., Spiridonov, S.E., Waeyenberge, L., Moens, M., Nicol, G.W. & Wilson, M.J. (2010). Molecular phylogeny of slug-parasitic nematodes inferred from 18S rRNA gene sequences. Molecular Phylogenetics and Evolution 55, 738-743. DOI: 10.1016/j.ympev.2010.01.026
Ross, J.L., Ivanova, E.S., Hatteland, B.A., Brurberg, M.B. & Haukeland, S. (2015). Survey of nematodes associated with terrestrial slugs in Norway. Journal of Helminthology 115, 1-5. DOI: 10.1017/S0022149X15000784
Rowson, B., Anderson, R., Turner, J. & Symondson, B. (2014). The slugs of Britain and Ireland: Undetected and undescribed species increase a well-studied, economically important fauna by more than 20%. PLoS ONE 9, e91907. DOI: 10.1371/journal.pone.0091907
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, 1335-1343. DOI: 10.1007/s11368-010-0246-y
Schneider, A. (1866). Monografie der Nematoden. Berlin, Germany, Duck und Verlag von Georg Reimer.
Schneider, A. (1871). Nachtrag – Eine Beobachtung aus dem Gebiete der Zoologie. Botanische Zeitung 29, column 109.
Schüder, I., Port, G. & Bennison, J. (2003). Barriers, repellents and antifeedants for slug and snail control. Crop Protection 22, 1033-1038. DOI: 10.1016/s0261-2194(03)00120-0
Slotsbo, S., Damgaard, C., Hansen, L.M. & Holmstrup, M. (2013). The influence of temperature on life history traits in the Iberian slug, Arion lusitanicus. Annual Applied Biology 162, 80-88. DOI: 10.1111/aab.12003
Speiser, B., Zaller, J.G. & Neudecker, 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. DOI: 10.1023/A:1011469730322
Tan, L. & Grewal, P.S. (2001). Pathogenicity of Moraxella osloensis, a bacterium associated with the nematode Phasmarhabditis hermaphrodita, to the slug Deroceras reticulatum. Applied and Environmental Microbiology 67, 5010-5016. DOI: 10.1128/AEM.67.11.5010-5016.2001
Tandingan De Ley, I., Holovachov, O., Mc Donnell, 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, 175-193. DOI: 10.1163/15685411-00002952
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, 563-573.
Welter-Schultes, F. (2012). European non-marine molluscs a guide for species identification. Göttingen, Germany, Planet Poster Editions.
Wilson, M.J. & Rae, R. (2015). Phasmarhabditis hermaphrodita as a control agent for slugs. In: Campos-Herrera, R. (Ed.). Nematode pathogenesis of insects and other pests. Cham, Switzerland, Springer International Publishing, pp. 509-521. DOI: 10.1007/978-3-319-18266-7_21
Wilson, M.J., Glen, D.M., George, S.K. & Butler, R.C. (1993). The rhabditid nematode Phasmarhabditis hermaphrodita, as a potential biocontrol agent for slugs. Biocontrol Science and Technology 3, 503-511. DOI: 10.1080/09583159309355306
Wilson, M.J., Hughes, L.A., Jefferies, D. & Glen, D.M. (1999). Slugs (Deroceras reticulatum and Arion ater agg.) avoid soil treated with the rhabditid nematode Phasmarhabditis hermaphrodita. Biological Control 16, 170-176. DOI: 10.1006/bcon.1999.0757
Wynne, R., Morris, A. & Rae, R. (2016). Behavioural avoidance by slugs and snails of the parasitic nematode Phasmarhabditis hermaphrodita. Biocontrol Science and Technology 26, 1129-1138. DOI: 10.1080/09583157.2016.1185513
Zemanova, M.A., Knop, E. & Heckel, G. (2016). Phylogeographic past and invasive presence of Arion pest slugs in Europe. Molecular Ecology 25, 5747-5764. DOI: 10.1111/mec.13860
All Time | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 625 | 172 | 13 |
Full Text Views | 46 | 9 | 0 |
PDF Views & Downloads | 71 | 8 | 0 |
In the period from August to October 2018, 140 specimens of the Spanish slug, Arion vulgaris, were collected from Podbrezje, Slovenia. Slugs were dissected and examined for the presence of parasitic nematodes within the cadavers. Identification of the nematodes was conducted using morphological and molecular techniques and confirmed the presence of Phasmarhabditis papillosa. This is the first record of P. papillosa from the mollusc host, A. vulgaris. Laboratory experiments aimed at testing the efficacy of P. papillosa against A. vulgaris were conducted using nematodes grown in vivo. Nematodes were applied at concentration rates of 50, 100 and 200 nematodes slug−1, respectively. Three weeks following treatment, the mortality of slugs was confirmed in all treatments (50 nematodes slug−1, 37.4 ± 2.7%; 100 nematodes slug−1, 48.4 ± 2.7%; 200 nematodes slug−1, 50.6 ± 2.7%). However, the pathogenesis of P. papillosa was observed first in the treatments with the lowest nematode dose at 4 days after treatments, while a decrease in the feeding behaviour of slugs was noted first in the treatments with the highest nematode dose. Future opportunities for the potential use of P. papillosa as a biological control agent against slugs are discussed. This is the first report of P. papillosa from Slovenia, and of its virulence against A. vulgaris.
All Time | Past Year | Past 30 Days | |
---|---|---|---|
Abstract Views | 625 | 172 | 13 |
Full Text Views | 46 | 9 | 0 |
PDF Views & Downloads | 71 | 8 | 0 |