Hostname: page-component-848d4c4894-pjpqr Total loading time: 0 Render date: 2024-06-22T06:41:23.240Z Has data issue: false hasContentIssue false
  • English
  • Français

Survey of nematodes associated with terrestrial slugs in Norway

Published online by Cambridge University Press:  28 September 2015

J.L. Ross ,
E.S. Ivanova ,
B.A. Hatteland ,
M.B. Brurberg  and
S. Haukeland
J.L. Ross*
Affiliation:
Institute of Biological and Environmental Sciences, University of Aberdeen, AB24 3UU, UK
E.S. Ivanova
Affiliation:
Centre of Parasitology, A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Science, Leninskii Prospect 33, 119071, Moscow, Russia
B.A. Hatteland
Affiliation:
Department of Biology, University of Bergen, PO Box 7800, 5020Bergen, Norway Norwegian Institute of Bioeconomy Research (NIBIO), Plant Health and Biotechnology, NIBIO Ullensvang, 5781Lofthus, Norway
M.B. Brurberg
Affiliation:
Norwegian Institute of Bioeconomy Research (NIBIO), Pb 115, NO-1431Ås, Norway
S. Haukeland
Affiliation:
Norwegian Institute of Bioeconomy Research (NIBIO), Pb 115, NO-1431Ås, Norway
*
*E-mail: jenna.ross@abdn.ac.uk
Get access Rights & Permissions [Opens in a new window]

Abstract

A survey of nematodes associated with terrestrial slugs was conducted for the first time in Norway. A total of 611 terrestrial slugs were collected from 32 sample sites. Slugs were identified by means of morphological examination, dissection of genitalia and molecular analysis using mitochondrial DNA. Twelve slug species were identified, representing four different slug families. Internal nematodes were identified by means of morphological analysis and the sequencing of the 18S rRNA gene. Of the sample sites studied, 62.5% were found to be positive for nematode parasites, with 18.7% of all slugs discovered being infected. Five nematode species were identified in this study: Alloionema appendiculatum, Agfa flexilis, Angiostoma limacis, Angiostoma sp. and Phasmarhabditis hermaphrodita. Of these species, only one nematode was previously undescribed (Angiostoma sp.). This is the first record of the presence of A. appendiculatum, A. flexilis and A. limacis in Norway.

Type
Research Papers
Information
Journal of Helminthology , Volume 90 , Issue 5 , September 2016 , pp. 583 - 587
Copyright
Copyright © Cambridge University Press 2015 

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

Altschul, S.F., Gish, W., Miller, W., Myers, E.X. & Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology 215, 403–410.Google Scholar
Andersen, A., Haukeland, S., Hatteland, B.A. & Westrum, K. (2012) Brunskogsnegl i landbruket. Gartneryrket 2, 36–38 (in Norwegian).Google Scholar
Cabaret, J. & Morand, S. (1990) Single and dual infection of the land snail Helix aspersa with Muellerius capillaris and Alloionema appendiculatum (Nematoda). Journal of Parasitology 76, 579–580.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, 55–61.CrossRefGoogle ScholarPubMed
Colautti, R.I., Grigorovich, I.A. & MacIsaac, H.J. (2006) Propagule pressure: a null model for biological invasions. Biological Invasions 8, 1023–1037.Google Scholar
Falcon-Ordaz, J., Mendoza-Garfias, B., Windfield-Perez, J.C., Parra-Olea, G. & De Leon, G.P.P. (2008) Angiostoma lamotheargumedoi n. sp. (Nematoda: Angiostomatidae) from the intestine of Pseudoeurycea mixteca (Caudata: Plethodontidae) in central Mexico. Revista Mexicana de Biodiversidad 79, 107–112.Google Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Gleich, J.G., Gilbert, F.F. & Kutscha, N.P. (1977) Nematodes in terrestrial gastropods from central Maine. Journal of Wildlife Diseases 13, 43–46.CrossRefGoogle ScholarPubMed
Grewal, P.S., Grewal, S.K., Tan, L. & Adams, B.J. (2003) Parasitism of molluscs by nematodes: types of associations and evolutionary trends. Journal of Nematology 33, 146–156.Google Scholar
Grimm, B. (2002) Effect of the nematode Phasmarhabditis hermaphrodita on young stages of the pest slug Arion lusitanicus . Journal of Molluscan Studies 68, 25–28.CrossRefGoogle Scholar
Hatteland, B.A., Solhøy, T., Schander, C., Skage, M., Von Proschwitz, T. & Noble, L. (2015) Introgression and differentiation of the invasive slug Arion vulgaris from native A. ater . Malacologia 58, 303–321.CrossRefGoogle Scholar
Hofsvang, T., Haukeland, S. & Andersen, A. (2008) Snegler som skadedyr på planter. Bioforsk Tema 24, 1–12 (in Norwegian).Google Scholar
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.Google Scholar
Ivanova, E.S., Panayotova-Pencheva, M.S. & Spiridonov, S.E. (2013) Observations on the nematode fauna of terrestrial molluscs of the Sofia area (Bulgaria) and the Crimea peninsula (Ukraine). Russian Journal of Nematology 21, 41–49.Google Scholar
Kiontke, K., Barriere, A., Kolotuev, I., Podbilewicz, B., Sommer, R., Fitch, D.H. & Felix, M.A. (2007) Trends, stasis, and drift in the evolution of nematode vulva development. Current Biology 17, 1925–1937.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, 137–139.Google Scholar
MacMillan, K., Blok, V., Young, I., Crawford, J. & Wilson, M.J. (2006) Quantification of the slug parasitic nematode Phasmarhabditis hermaphrodita from soil samples using real time qPCR. International Journal for Parasitology 36, 1453–1461.Google Scholar
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 & Biochemistry 41, 1483–1490.Google Scholar
Mengert, H. (1953) Nematoden und Schneken. Zeitschrift für Morphologie und Öekologie Tiere 41, 311–349.Google Scholar
Morand, S. (1988) Contribution à l'étude d'un système hôtes-parasites: Nématodes associés à quelques Mollusques terrestres. Thèse, Université Rennes I.Google Scholar
Morand, S., Wilson, M.J. & Glen, D.M. (2004) Nematodes (Nematoda) parasitic in terrestrial gastropods. pp. 525–557 in Barker, G.M. (Ed.) Natural enemies of terrestrial molluscs. Wallingford, CABI.Google Scholar
Poulin, R. (2011) The many roads to parasitism: a tale of convergence. Advances in Parasitology 74, 1–40.Google Scholar
Rae, R., Verdun, C., Grewal, P., Robertson, J.F. & Wilson, M.J. (2007) Biological control of terrestrial molluscs using Phasmarhabditis hermaphrodita – progress and prospects. Pest Management Science 63, 1153–1164.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, 603–610.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, 738–743.CrossRefGoogle ScholarPubMed
Ross, J.L., Ivanova, E.S. & Malan, A.P. (2011) Angiostoma margaretae n. sp. (Nematoda: Angiostomatidae) a parasite of the milacid slug Milax gagates Draparnaud collected near Caledon, South Africa. Systematic Parasitology 79, 71–76.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, 215–221.Google Scholar
Schuurmans-Stekhoven, L.H. (1950) Alloionema appendiculatum . Acta Zoológica Lilloana 9, 481–485.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, 311–320.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, 1349–1354.Google Scholar
Torchin, M.E., Lafferty, K.D. & Kuris, A.M. (2001) Release from parasites as natural enemies: increased performance of a globally introduced marine crab. Biological Invasions 3, 333–345.Google Scholar
Von Proschwitz, T. & Winge, K. (1994) Iberiaskogsnegl- en art på spredning i Norge. Fauna 47, 195–203 (in Norwegian).Google Scholar