Hostname: page-component-586b7cd67f-rcrh6 Total loading time: 0 Render date: 2024-11-22T04:41:46.607Z Has data issue: false hasContentIssue false
  • English
  • Français

Nematodes associated with terrestrial slugs in the Edmonton region of Alberta, Canada

Published online by Cambridge University Press:  13 October 2020

T. Brophy ,
R.J. Mc Donnell ,
D.K. Howe ,
D.R. Denver ,
J.L. Ross  and
L.T. Luong Open the ORCID record for L.T. Luong [Opens in a new window]
T. Brophy
Affiliation:
Department of Biological Sciences, University of Alberta, Edmonton, AB, T6G 2E9, Canada
R.J. Mc Donnell
Affiliation:
Department of Crop and Soil Science, Oregon State University, Corvallis, OR97331
D.K. Howe
Affiliation:
Department of Integrative Biology, Oregon State University, Corvallis, OR97331
D.R. Denver
Affiliation:
Department of Integrative Biology, Oregon State University, Corvallis, OR97331
J.L. Ross
Affiliation:
Department of Conservation Ecology and Entomology, Faculty of AgriSciences, Stellenbosch University, Private Bag X1, Matieland7602, South Africa
L.T. Luong*
Affiliation:
Department of Biological Sciences, University of Alberta, Edmonton, AB, T6G 2E9, Canada
*
Author for correspondence: L.T. Luong, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

A survey of nematodes associated with terrestrial slugs was conducted in residential gardens, nurseries, greenhouses and agricultural sites located in and around Edmonton, Alberta, Canada. A total of 2406 slugs were collected from 82 sites. Slugs were decapitated and cadavers were incubated for two weeks, with emerging nematodes removed and processed for identification. Nematodes were identified using molecular sequence data for the 18S ribosomal DNA. Nematodes were recovered from 20 of the 82 sites surveyed, with 24.4% of the slugs infected with nematodes. A total of seven nematodes were identified to species level, including Caenorhabditis elegans, Panagrolaimus papillosus, Pellioditis typica, Pelodera pseudoteres, Rhabditella axei, Rhabditoides inermiformis and Phasmarhabditis californica. An additional four specimens were identified to genus level, including Oscheius sp. (9), Pristionchus sp., Rhabditis sp. and Rhabditophanes sp. (1). The two most common nematode species were C. elegans and P. pseudoteres. The facultative parasite, P. californica, was recovered from a single Arion rufus specimen, collected from a seasonal nursery. To our knowledge, this study represents the first survey of slug-associated nematodes in Canada.

Keywords

Biological controlDeroceras reticulatumgastropodMolluscaparasitismPhasmarhabditisslug pests
Type
Research Paper
Information
Journal of Helminthology , Volume 94 , 2020 , e200
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

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.)

Footnotes

*

Current address: Crop Health and Protection (CHAP), National Agri-Food Innovation Campus, Sand Hutton, York, YO411LZ, UK.

References

Bailey, SER (2002) Molluscicidal baits for control of terrestrial gastropods. pp. 33–54 in Barker, GM (Ed) Molluscs as crop pests. Wallingford, CABI Publishing.CrossRefGoogle Scholar
Barker, GM (2002) Molluscs as crop pests. p. 558. Wallingford, CABI Publishing.CrossRefGoogle Scholar
Benson, DA, Cavanaugh, M, Clark, K, Karsch-Mizrachi, I, Lipman, DJ, Ostell, J and Sayers, EW (2013) GenBank. Nucleic Acids Research 41(database issue): D36–D42.CrossRefGoogle ScholarPubMed
Blaxter, ML, De Ley, P, Garey, JR, et al. (1998) A molecular evolutionary framework for the phylum Nematoda. Nature 392(6671), 71–75.CrossRefGoogle ScholarPubMed
Brophy, T, Howe, DK, Denver, DR and Luong, LT (2020) First report of a gastropod parasitic nematode Phasmarhabditis californica (Nematoda: Rhabditidae) in Alberta, Canada. The Journal of Nematology 52, 1–3..CrossRefGoogle Scholar
Carnaghi, M, Rae, R, Tandingan De Ley, I, et al. (2017) Nematode associates and susceptibility of a protected slug Geomalacus maculosus to four biocontrol nematodes. Biocontrol Science and Technology 27, 294–299.CrossRefGoogle Scholar
Castle, GD, Mills, GA, Gravell, A, Jones, L, Townsend, I, Cameron, DG and Fones, GR (2017) Review of the molluscicide metaldehyde in the environment. Environmental Science: Water Research & Technology 3, 3415–3428.Google Scholar
DeAngelis, JD (1993) Slugs. Oregon State University Extension Bulletin FS 277. Corvallis, Oregon, Oregon State University.Google Scholar
Fletcher, MR, Hunter, K and Barnet, EA (1994) Pesticide poisoning of animals. p. 52. London, MAFF Publications.Google Scholar
Folmer, O, Black, M, Hoeh, WR, Lutz, R and Vrijenhoek, RC (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit 1 from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Forsyth, RG (2004) Land snails of British Columbia, Royal B.C. Museum handbook. p. 188. Victoria, Royal British Columbia Museum.Google Scholar
Godan, D (1983) Pest slugs and snails. Berlin, Springer-Verlag.CrossRefGoogle Scholar
Grewal, PS, Grewal, SK, Tan, L and Adams, BJ (2003) Parasitism of molluscs by nematodes: types of associations and evolutionary trends. Journal of Nematology 35, 146–156.Google ScholarPubMed
Grimm, FW, Forsyth, RG, Schueler, FW and Karstad, A (2009) Identifying land snails and slugs in Canada. 1st edn. p. 168. Ottawa, Canadian Food Inspection Agency.Google Scholar
Hall, TA (1999) BioEdit: a user-friendly biological sequence alignment [ed.], and analysis program for Windows 95/98/ NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hata, T, Hara, AH and Hu, BKS (1997) Molluscicides and mechanical barriers against slugs, Vaginula plebeia Fischer and Veronicella cubensis Pfeiffer (Stylommatophora: Veronicellidae). Crop Protection 16, 501–506.CrossRefGoogle Scholar
Hawkins, JW, Lankester, MW, Lautenschlager, RA and Bell, FW (1997) Effects of alternative conifer release treatments on terrestrial gastropods in northwestern Ontario. Forestry Chronicle 73, 91–98.CrossRefGoogle Scholar
Henderson, I and Triebskorn, R (2002) Chemical control of terrestrial gastropods. pp. 1–32 in Barker, GM (Ed) Molluscs as crop pests. Wallington, CABI Publishing.Google Scholar
Kiontke, K and Sudhaus, W (2006) Ecology of Caenorhabditis species. In WormBook: the online review of C. elegans biology [Internet]. Pasadena (CA): WormBook; 2005-2018. Available at https://www.ncbi.nlm.nih.gov/books/NBK19723/, accessed July 2020.CrossRefGoogle Scholar
L'Heureux, E and Angers, B (2018) A discreet invasion: distribution, origins, and expansion of the European slug complex Arion subfuscus s.l. in Quebec. Canadian Journal of Zoology 96, 325–331.CrossRefGoogle Scholar
Mc Donnell, RJ, Paine, TD and Gormally, MJ (2009) Slugs: a guide to the invasive and native fauna of California. Davis, University of California Agricultural and Natural Resources Publications.CrossRefGoogle Scholar
Mc Donnell, RJ, Tandingan De Ley, I and Paine, T (2018a) Susceptibility of neonate Lissachatina fulica (Achatinidae: Mollusca) to a US strain of the nematode Phasmarhabditis hermaphrodita (Rhabditidae: Nematoda). Biocontrol Science and Technology 28, 1091–1095.CrossRefGoogle Scholar
Mc Donnell, RJ, Lutz, MS, Howe, DK and Denver, DR (2018b) First report of the gastropod-killing nematode, Phasmarhabditis hermaphrodita, in Oregon, USA. Journal of Nematology 50, 77–78.CrossRefGoogle Scholar
Morand, S, Wilson, MJ and Glen, DM (2004) Nematodes (Nematoda) parasitic in terrestrial gastropods. pp. 525–557 in Barker, GM (Ed) Natural enemies of terrestrial molluscs. Wallington, CABI Publishing.CrossRefGoogle Scholar
Moss, M and Hermanutz, L (2010) Monitoring the small and slimy – protected areas should be monitoring native and non-native slugs (Mollusca: Gastropoda). Natural Areas Journal 30, 322–327.CrossRefGoogle Scholar
Petersen, C, Hermann, RJ, Barg, MC, Schalkowski, R, Dirksen, P, Barbosa, C and Schulenburg, H (2015) Travelling at a slug's pace: possible invertebrate vectors of Caenorhabditis nematodes. BMC Ecology 15, 19.CrossRefGoogle Scholar
Pieterse, A, Malan, AP and Ross, JL (2017) Nematodes that associate with terrestrial molluscs as definitive hosts, including Phasmarhabditis hermaphrodita (Rhabditida: Rhabditidae) and its development as a biological molluscicide. Journal of Helminthology 91, 517–527.CrossRefGoogle ScholarPubMed
Purves, G and Bannon, JW (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, 215–223.Google Scholar
Rae, R, Verdun, C, Grewal, P, Robertson, JF and Wilson, MJ (2007) Biological control of terrestrial molluscs using Phasmarhabditis hermaphrodita – progress and prospects. Pest Management Science 63, 1153–1164.CrossRefGoogle ScholarPubMed
Ratnasingham, S and Hebert, PD (2007) BOLD: the Barcode of Life Data System (http://www.barcodinglife.org). Molecular Ecology Notes 7, 355–364.CrossRefGoogle ScholarPubMed
Reich, I, Gormally, M, Allcock, AL, Mc Donnell, R, Castillejo, J, Iglesias, J, Quinteiro, J and Smith, CJ (2015) Genetic study reveals close link between Irish and Northern Spanish specimens of the protected Lusitanian slug Geomalacus maculosus. Biological Journal of the Linnean Society 116, 156–168.CrossRefGoogle Scholar
Ross, JL (2019) Riding the slime wave: gathering global data on slug control. Taunton, UK, Nuffield Farming Scholarships Trust Report.Google Scholar
Ross, JL, Ivanova, ES, Severns, PM and Wilson, MJ (2010) The role of parasite release in invasion of the USA by European slugs. Biological Invasions 12, 603–610.CrossRefGoogle Scholar
Ross, JL, Ivanova, ES, Sirgel, WF, Malan, AP and Wilson, MJ (2012) Diversity and distribution of nematodes associated with terrestrial slugs in the Western Cape Province of South Africa. Journal of Helminthology 86, 215–221.CrossRefGoogle Scholar
Ross, JL, Ivanova, ES, Hatteland, BA, Brurberg, MB and Haukeland, S (2016) Survey of nematodes associated with terrestrial slugs in Norway. Journal of Helminthology 90, 583–587.CrossRefGoogle ScholarPubMed
Schulte, F (1989) Description of Rhabditis (Pelodera) pseudoteresn. sp. (Rhabditidae: Nematoda) with a redescription of its sibling R.(P.) teres (Schneider, 1866). Revue de Nématologie 12, 387–394.Google Scholar
Storey, KB, Storey, JM and Churchill, TA (2007) Freezing and anoxia tolerance of slugs: a metabolic perspective. Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 177, 833–840.CrossRefGoogle ScholarPubMed
Tandingan De Ley, IT, McDonnell, RD, Lopez, S, Paine, TD and 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, 1129–1138.CrossRefGoogle Scholar
Tandingan De Ley, I, Holovachov, O, Mc Donnell, RJ, Bert, W, Paine, TD and 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.CrossRefGoogle Scholar
Vlach, J (2016) Slugs and snails in Oregon: a guide to common land molluscs and their relatives. p. 39. Salem, Oregon Department of Agriculture.Google Scholar
Williams, BD, Schrank, B, Huynh, C, Shownkeen, R and Waterston, RH (1992) A genetic mapping system in Caenorhabditis elegans based on polymorphic sequence tagged sites. Genetics 131, 15.Google ScholarPubMed
Wilson, MJ and Grewal, PS (2005) Biology, production and formulation of slug-parasitic nematodes. pp. 421–429 in Grewal, PS, Ehlers, RU and Shapiro-Ilan, DI (Eds) Nematodes as biocontrol agents. Wallingford, CABI Publishing.CrossRefGoogle Scholar
Wilson, MJ, Glen, DM and George, SK (1993) The rhabditid nematode Phasmarhabditis hermaphrodita as a potential biological control agent for slugs. Biocontrol Science and Technology 3, 503–511.CrossRefGoogle Scholar
Wilson, MJ, Wilson, DJ, Aalders, LT and Tourna, M (2016) Testing a new low-labour method for detecting the presence of Phasmarhabditis spp. in slugs in New Zealand. Nematology 18, 925–931.CrossRefGoogle Scholar