Skip to main content Skip to main navigation menu Skip to site footer
Responsive image
Issue: Vol. 4312 No. 1: 28 Aug. 2017
Type: Correspondence
Published: 2017-08-28
DOI: 10.11646/zootaxa.4312.1.12
Page range: 194–200
Abstract views: 90
PDF downloaded: 5

Nematodes associated with terrestrial slugs from canola fields and ornamental nurseries in South Africa

Department of Conservation Ecology and Entomology, Faculty of Agrisciences, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa
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
Department of Botany and Zoology, Stellenbosch University, Private Bag XI, Matieland 7602, South Africa
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
Nematoda Agfa Angiostoma Molluscs Nematodes Parasites Phasmarhabditis

Abstract

A survey of nematodes that use terrestrial slugs as definitive hosts, was conducted in canola fields and ornamental nurseries located in the Western Cape province of South Africa. A total of 3290 slugs were collected from 22 different sites. On the identification of the slugs, they were vivisected and examined for internal nematodes. After identifying the nematodes found, on the basis of their morphological characteristics, their identity was confirmed using molecular sequence data for the internal transcribed spacer (ITS-1, 5.8S, ITS-2), D2-D3 expansion segments of the large subunit (LSU or 28S) and small subunit (SSU or 18S) ribosomal DNA. Of the 22 sites investigated, 13 had nematodes present, with 8 % of the slugs being found to be infected with nematodes. Seven nematode species were confirmed, including Agfa flexilis, Angiostoma margaretae, Angiostoma sp. (SA1), Caenorhabditis elegans, mermithid sp. (SA1), Phasmarhabditis sp. (SA3) and Phasmarhabditis sp. (SA4). In addition, several Angiostoma spp. were also isolated, but could only be identified to genus level due to limited material. Of the seven confirmed species, four were previously undescribed. This is the first record of A. margaretae associating with Deroceras panormitanum, Deroceras reticulatum, Lehmannia valentiana and Oopelta polypunctata. Also, this is the first time that a mermithid has been found associating with molluscs in South Africa.

 

References

  1. 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.
    https://doi.org/10.1016/s0022-2836(05)80360-2

    Bursey, C.R. & Goldberg, S.R. (2000) Angiostoma onychodactyla sp. n. (Nematoda: Angiostomatidae) and other intestinal helminths of the Japanese clawed salamander, Onychodactylus japonicus (Caudata: Hynobiidae) from Japan. Comparative Parasitology, 67, 60–65.

    Bursey, C.R. & Manire, C.A. (2006) Angiostoma carettae n. sp. (Nematoda: Angiostomatidae) from the loggerhead sea turtle Caretta caretta (Testudines: Cheloniidae), Florida, USA. Comparative Parasitology, 73, 253–256.
    https://doi.org/10.1654/4200.1

    Chitwood, B.G. (1933) On some nematodes of the superfamily Rhabditoidea and their status as parasites of reptiles and amphibians. Journal of the Washington Academy of Sciences, 23, 508–520.

    Chitwood, B.G. & Chitwood, M.B. (1937) Snails as host carriers of nematodes and Nematomorpha. The Nautilus, 50, 130–135.

    Cowie, R.H., Hayes, K.A., Tran, C.T. & Meyer III, W.M. (2008) The horticultural industry as a vector of alien snails and slugs: widespread invasions in Hawaii. International Journal of Pest Management, 54 (4), 267–276.
    https://doi.org/10.1080/09670870802403986

    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.

    Grewal, S.K., Grewal, P.S. & Hammond, R.B. (2003) Susceptibility of North American native and non-native slugs (Mollusca: Gastropoda) to Phasmarhabditis hermaphrodita (Nematoda: Rhabditidae). Biocontrol Science and Technology, 13, 119–125.
    https://doi.org/10.1080/0958315021000054449

    Hatting, J., Stock, P. & Hazir, S. (2009) Diversity and distribution of entomopathogenic nematodes (Steinernematidae, Heterorhabditidae) in South Africa. Journal of Invertebrate Pathology, 102, 120–128.
    https://doi.org/10.1016/j.jip.2009.07.003

    Iglesias, J. & Speiser, B. (2001) Consumption rate and susceptibility to parasitic nematodes and chemical molluscicides of the pest slugs Arion hortensis s. s. and A. distinctus. Journal of Pest Science, 74, 159–166.
    https://doi.org/10.1046/j.1439-0280.2001.01037.x

    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.
    https://doi.org/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.
    https://doi.org/10.1163/156854102760082186

    Kiontke, K. & Sudhaus, W. (2006) Ecology of Caenorhabditis species. Available from: http://www.wormbook.org (accessed 15 February 2017)
    https://doi.org/10.1895/wormbook.1.37.1

    Malan, A.P., Nguyen, K.B. & Addison, M.F. (2006) Entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) from the southwestern parts of South Africa. African Plant Protection, 12, 65–69.

    Malan, A.P., Knoetze, R. & Moore, S.D. (2011) Isolation and identification of entomopathogenic nematodes from citrus orchards and their biocontrol potential against false codling moth. Journal of Invertebrate Pathology, 108, 115–125.
    https://doi.org/10.1016/j.jip.2011.07.006

    Mienis, H.K. (1986) First record of the parasitic nematode, Hexamermis albicans, from a slug in Israel. Zoology in the Middle East, 1, 156.
    https://doi.org/10.1080/09397140.1986.10637545

    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. CABI Publishing, Wallingford, pp. 525–557.
    https://doi.org/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 Anasakis, Pseudoterranova, and Contracaecum from Northern Pacific marine mammals. Journal of Parasitology, 91, 1413–1429,

    Nguyen, K.B., Shapiro-Ilan, D.I., Stuart, R.J., McCoy, C.W., James, R.R. & Adams, B.J. (2004) Heterorhabditis mexicana n. sp. (Rhabditida: Heterorhabditidae) from Tamaulipas, Mexico, and morphological studies of the bursa of Heterorhabditis spp. Nematology, 6, 231–244.
    https://doi.org/10.1163/1568541041218031

    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.
    https://doi.org/10.1186/s12898-015-0050-z

    Pieterse, A., Malan, A.P. & Ross, J.L. (2016) Nematodes that associate with terrestrial molluscs as definitive hosts, including Phasmarhabditis hermaphrodita (Rhabditida: Rhabditidae) and its development as a biological molluscicide. Journal of Helminthology, 9, 517-527.
    https://doi.org/10.1017/S0022149X16000572

    Poinar, G.O. Jr. (1976) Presence of Mermithidae (Nematoda) in invertebrate paratenic hosts. Journal of Parasitology, 62, 843–844.
    https://doi.org/10.2307/3278981

    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.

    https://doi.org/10.1016/j.jip.2007.07.004

    Ross, J.L., Ivanova, E.S., Spiridinov, S.E., Waeyenberge, L., Mens, 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.
    https://doi.org/10.1016/j.ympev.2010.01.026

    Ross, J.L., Malan, A.P. & Ivanova, E.S. (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.
    https://doi.org/10.1007/s11230-011-9294-y

    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.
    https://doi.org/10.1017/s0022149x11000277

    Ross, J.L., Ivanova, E.S., Hatteland, B.A., Brurberg, M.B. & Haukeland, S. (2016) Survey of nematodes associated with terrestrial slugs in Norway. Journal of Helminthology, 90, 582–587.
    https://doi.org/10.1017/S0022149X15000784

    Ross, J.L., Ivanova, E.S. & Haukeland, S. (2017) Angiostoma norvegicum n. sp. (Nematoda: Angiostomatidae) a parasite of arionid slugs in Norway. Systematic Parasitology, 94 (1), 51–63.

    https://doi.org/10.1007/s11230-016-9674-4

    Seinhorst, J.W. (1959) A rapid method for the transfer of nematodes from fixative to anhydrous glycerine. Nematologica, 4, 67–69.
    https://doi.org/10.1163/187529259x00381

    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.
    https://doi.org/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 (11), 5010–5016.
    https://doi.org/10.1128/aem.67.11.5010-5016.2001

    Théodoridès, J. (1957) Sur un nématode nouveau parasite d’un mollusque gastéropode d’Indonésie Alaninema venmansi n. g. n. sp. (Nematoda, Drilonematidae). Annales de Parasitologie, 32, 267–270.

    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.

    Wilson, M.J., Glen, D.M. & George, S.K. (1993a) The rhabditid nematode Phasmarhabditis hermaphrodita as a potential biological control agent for slugs. Biocontrol Science and Technology, 3, 503–511.
    https://doi.org/10.1080/09583159309355306

    Wilson, M.J., Glen, D.M., George, S.K. & Butler, R.C. (1993b) Mass cultivation and storage of the rhabditid nematode Phasmarhabditis hermaphrodita, a biocontrol agent of slugs. Biocontrol Science and Technology, 3, 513–521.
    https://doi.org/10.1080/09583159309355307