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Diversity and distribution of nematodes associated with terrestrial slugs in the Western Cape Province of South Africa

Published online by Cambridge University Press:  01 June 2011

J.L. Ross ,
E.S. Ivanova ,
W.F. Sirgel ,
A.P. Malan  and
M.J. Wilson
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, 119071Moscow, Russia
W.F. Sirgel
Affiliation:
Department of Botany and Zoology, Faculty of Sciences, Stellenbosch University, Private Bag X1, Matieland7602, South Africa
A.P. Malan
Affiliation:
Department of Conservation Ecology and Entomology, Faculty of AgriSciences, Stellenbosch University, Private Bag X1, Matieland7602, South Africa
M.J. Wilson
Affiliation:
Institute of Biological and Environmental Sciences, University of Aberdeen, AB24 3UU, UK
*
*E-mail: jenna.ross@abdn.ac.uk
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Abstract

A survey of nematodes associated with native and introduced species of terrestrial slugs was conducted in the Western Cape Province of South Africa, in order to gather new data regarding diversity and distribution. A total of 521 terrestrial slugs were collected from 35 localities throughout the Western Cape. All slugs were dissected and examined for the presence of internal nematodes. Extracted nematodes were identified using a combination of molecular (18S rRNA gene sequencing) and morphological techniques. Nematodes were found parasitizing slugs at 14 of the 35 sites examined, amounting to 40% of sample sites. Of all slugs, 6% were infected with nematodes. A total of seven species of nematode were identified in the province, including Agfa flexilis, Angiostoma sp., Phasmarhabditis sp. SA1, Phasmarhabditis sp. SA2, Caenorhabditis elegans,Panagrolaimus sp. and Rhabditis sp. Of these species, four were thought to be parasitic to slugs (A. flexilis, Angiostoma sp., Phasmarhabditis sp. SA1 and Phasmarhabditis sp. SA2), as opposed to forming necromenic or phoretic associations. Three new species of slug-parasitic nematode were identified during this study (Angiostoma sp., Phasmarhabditis sp. SA1 and Phasmarhabditis sp. SA2).

Type
Research Papers
Information
Journal of Helminthology , Volume 86 , Issue 2 , June 2012 , pp. 215 - 221
Copyright
Copyright © Cambridge University Press 2011

Introduction

Nematodes associated with terrestrial slugs are understudied in comparison to entomopathogenic nematodes (Wilson & Grewal, Reference Wilson, Grewal, Grewal, Ehlers and Shapiro-Ilan2005). Current understanding of the slug/nematode relationship is based on surveys of Europe (Mengert, Reference Mengert1953; Morand, Reference Morand1988; Laznik et al., Reference Laznik, Ross, Tóth, Lakatos, Vidrih and Trdan2009; Ross et al., Reference Ross, Ivanova, Severns and Wilson2010a, Reference Ross, Ivanova, Spiridonov, Waeyenberge, Moens, Nicol and Wilsonb), North America (Gleich et al., Reference Gleich, Gilbert and Kutscha1977; Ross et al., Reference Ross, Ivanova, Severns and Wilson2010a, Reference Ross, Ivanova, Spiridonov, Waeyenberge, Moens, Nicol and Wilsonb), South-East Asia (Pham Van Luc et al., Reference Pham Van Luc, Spiridonov and Wilson2005) and Australia (Charwat & Davies, Reference Charwat and Davies1999), along with numerous descriptions of individual parasites from around the world (for reviews see Grewal et al., Reference Grewal, Grewal, Tan and Adams2003; Morand et al., Reference Morand, Wilson, Glen and Barker2004; Ross et al., Reference Ross, Ivanova, Severns and Wilson2010a, Reference Ross, Ivanova, Spiridonov, Waeyenberge, Moens, Nicol and Wilsonb). These surveys reveal that there are a total of seven families of nematodes known to be associated with terrestrial slugs: Agfidae, Alloionematidae, Angiostomatidae, Cosmocercidae, Diplogasteridae, Mermithidae and Rhabditidae. This low number of nematode taxa is considered to be an underestimation of the real taxonomic diversity of nematodes associated with terrestrial slugs. A greater understanding could be achieved by surveying countries such as South Africa, where there is a unique climate and habitat diversity (Coe & Skinner, Reference Coe and Skinner1993; Stattersfield et al., 1998).

South Africa is located on the southern tip of Africa, between the Atlantic and Indian oceans. This location provides a range of climates, from subtropical in the east to semiarid in the west (Hatting et al., Reference Hatting, Stock and Hazir2009). In the Western Cape Province (WCP), the climatic range is favourable for European slugs, which has resulted in the widespread distribution of these invasive species (Herbert & Kilburn, Reference Herbert and Kilburn2004). The introduction of these slugs is believed to be due to the migration of European settlers during the eighteenth and early nineteenth century (Smith, Reference Smith1992). The success of these pests is not completely understood, but the lack of associated nematodes has been implicated as an important factor in the invasion of European slugs into North America (Ross et al., Reference Ross, Ivanova, Severns and Wilson2010a). Recent reports by the ARC-Plant Protection Research Institute, state that European slug species have established themselves as major pests in South African agriculture (G. Tribe, pers. comm.). Current methods for controlling slugs rely on chemical molluscicides, such as metaldehyde and carbamate compounds (Hata et al., Reference Hata, Hara and Hu1997). Both metaldehyde and methiocarb are poisonous to a wide range of vertebrates (Homeida & Cooke, Reference Homeida and Cooke1982; Fletcher et al., Reference Fletcher, Hunter and Barnet1994) and studies have shown that methiocarb is toxic to a number of beneficial invertebrates, including earthworms and carabid beetles (Purves & Bannon, Reference Purves and Bannon1992). Therefore it is important that a method of biological control is identified. The most effective commercial method for the biological control of molluscs in Europe is the slug-parasitic nematode Phasmarhabditis hermaphrodita (Rae et al., Reference Rae, Verdun, Grewal, Robertson and Wilson2007). Phasmarhabditis hermaphrodita is currently mass produced by Becker Underwood UK Ltd (Littlehampton, UK) and sold under the trade name of Nemaslug®. To date, this product cannot be sold in South Africa due to current legislation (amendment of Act 18 of 1989 under the Agricultural Pest Act 36 of 1947) which prohibits the introduction of exotic animals. Therefore, only an indigenous nematode isolate may be developed into a new molluscicide product. However, before this can be done, a systematic survey of nematodes associated with terrestrial slugs must be conducted in South Africa. Therefore this paper presents new data on the diversity and distribution of nematodes associated with terrestrial slugs in the WCP of South Africa, where European slug species are known to be widespread and pestiferous.

Materials and methods

Sampling

Slugs were collected from 35 localities in the WCP of South Africa (fig. 1) between 15 May 2009 and 7 September 2009. Sample habitats included public/private gardens, agricultural land, vineyards and private/commercial nurseries. Slugs were identified on the basis of their anatomy (Sirgel, Reference Sirgel1985; Herbert, Reference Herbert2010) and rinsed with 0.9% saline solution to remove surface-dwelling nematodes. Slugs were then dissected and examined for the presence of internal nematodes.

Fig. 1 Map showing the location of sample sites in the Western Cape Province (WCP) of South Africa.

Morphological and molecular identification

Adult nematodes were heat killed and fixed at 60°C in 5% formaldehyde, and were left in the fixative for a minimum of 2 h before being processed into anhydrous glycerol for mounting (Seinhorst, Reference Seinhorst1959). To aid identification, juvenile bacterial-feeding nematodes were cultured on modified kidney media plates (Wilson et al., Reference Wilson, Glen, George and Butler1993), pre-inoculated with bacteria isolated from dead slugs (Wilson et al., Reference Wilson, Glen, George and Pearce1995). Light microscopic studies were done using a Zeiss Jenaval microscope (VEB Carl Zeiss, Jena, DDR).

For molecular identification, individual nematodes were picked directly into 70% ethanol. DNA extraction, polymerase chain reaction (PCR) amplification and sequencing of the 18s rRNA gene followed methods described by Ross et al. (Reference Ross, Ivanova, Spiridonov, Waeyenberge, Moens, Nicol and Wilson2010b). Sequences of slug-parasitic nematodes were deposited in the National Center for Biotechnology Information (NCBI) GenBank and compared with the database (http://www.ncbi.nlm.nih.gov/) using the BLASTN search tool (Altschul et al., Reference Altschul, Gish, Miller, Myers and Lipman1990). The accession numbers, closest matches, identity and coverage of slug-parasitic nematodes were recorded.

Results

A total of 521 terrestrial slugs were collected from 35 sample sites (fig. 1), representing 12 different slug species from seven families (table 1). Of these, 33 slugs were native to South Africa and 488 slugs were European invasive species (table 1). Nematodes were found to parasitize six of the 12 slug species identified, leaving Deroceras panormitanum, Chlamydephorus gibbonsi, Oopelta granulosa, O. polypunctata, Testacella maugei and Laevicaulis alte free from nematode parasites in this survey (table 1).

Table 1 Prevalence and abundance of nematodes associated with terrestrial slugs collected at various localities in the Western Cape Province (WCP) of South Africa.

†, New host association; *, thought to be true parasites rather than necromenic or phoretic association.

Nematodes were found parasitizing slugs at 14 of the 35 sites examined (40%), (fig. 1, table 2). Of all slugs collected, 6% were infected with nematodes. These data are presented in tables 1 and 2, and show that of the 14 positive sites, two sites were found to have Agfa flexilis, one site had Angiostoma sp., two sites had Phasmarhabditis spp., eight sites had Caenorhabditis elegans, three sites had Panagrolaimus sp. and two sites had Rhabditis sp. These species represent four families: Agfidae, Angiostomatidae, Panagrolaimidae and Rhabditidae. Of these species, four are thought to have parasitic relationships with slugs, including A. flexilis, Angiostoma sp., Phasmarhabditis sp. SA1 and Phasmarhabditis sp. SA2 (Agfidae, Angiostomatidae and Rhabditidae) (table 3). The accession numbers, matches, identity and coverage of these slug-parasitic nematodes are recorded in table 3.

Table 2 Sites in the Western Cape Province (WCP) of South Africa with nematodes associated with terrestrial slugs.

†, First record in South Africa.

Table 3 Accession numbers, closest matches, identity and coverage of slug-parasitic nematodes isolated in the Western Cape Province (WCP) of South Africa.

Discussion

This paper presents new data on the diversity and distribution of terrestrial slugs and their associated nematode parasites in the WCP of South Africa. A total of seven species of nematode were identified in the province, including A. flexilis, Angiostoma sp., Phasmarhabditis sp. SA1, Phasmarhabditis sp. SA2, C. elegans, Panagrolaimus sp. and Rhabditis sp. (table 1). Of these seven species, four are thought to have parasitic relationships with slugs (A. flexilis, Angiostoma sp., Phasmarhabditis sp. SA1 and Phasmarhabditis sp. SA2), as opposed to forming necromenic or phoretic associations (tables 1 and 3). These nematodes represent three different families: Agfidae, Angiostomatidae and Rhabditidae.

The family Agfidae are obligate parasites of molluscs that associate with the salivary gland or genital tract (Morand & Hommay, Reference Morand and Hommay1990; Korol & Spiridonov, Reference Korol and Spiridonov1991; Ribas & Casanova, Reference Ribas and Casanova2002). There are only three known species, all of which fall within the genus Agfa (Morand & Hommay, Reference Morand and Hommay1990; Korol & Spiridonov, Reference Korol and Spiridonov1991; Ribas & Casanova, Reference Ribas and Casanova2002).

The Angiostomatidae family has two known genera, Angiostoma and Aulacnema. Molluscan angiostomatids are generally obligate parasites of the intestine (Campana-Rouget & Theodorides, Reference Campana-Rouget and Theodorides1956; Spiridonov, Reference Spiridonov1985; Morand & Spiridonov, Reference Morand and Spiridonov1989; Morand, Reference Morand1992; Pham Van Luc et al., Reference Pham Van Luc, Spiridonov and Wilson2005; Ivanova & Wilson, Reference Ivanova and Wilson2009); however, Angiostoma glandicola has been found to associate with the hepatopancreas (Ivanova & Spiridonov, Reference Ivanova and Spiridonov2010) and Angiostoma aspersae has been isolated from the pallial cavity of slugs (Morand, Reference Morand1986). In addition to being mollusc parasites, angiostomatids have also been described from the intestine and bronchi of amphibian and reptile hosts (Chitwood, Reference Chitwood1933; Bursey & Goldberg, Reference Bursey and Goldberg2000; Bursey & Manire, Reference Bursey and Manire2006; Falcon-Ordaz et al., Reference Falcon-Ordaz, Mendoza-Garfias, Windfield-Perez, Parra-Olea and de Leon2008).

There are several genera within the Rhabditidae family that associate with slugs, including Rhabditis, Caenorhabditis and Phasmarhabditis. However, Phasmarhabditis is the only genus that is considered to be truly parasitic to slugs (Morand et al., Reference Morand, Wilson, Glen and Barker2004). Phasmarhabditis spp. parasitize the mantle cavity of slugs, in close association with the shell. However, unlike the obligate parasites Agfa and Angiostoma, Phasmarhabditis spp. are facultative parasites that are known to live on leaf litter and slug faeces (Tan & Grewal, Reference Tan and Grewal2001; MacMillan et al., Reference MacMillan, Haukeland, Rae, Young, Crawford, Hapca and Wilson2009).

Of the four slug-parasitic nematodes isolated in the WCP, three (Angiostoma sp., Phasmarhabditis sp. SA1 and Phasmarhabditis sp. SA2) have not been described previously. The identification of these undescribed nematodes implies that South Africa is rich in unidentified nematode species. Similar findings have been noted for entomopathogenic nematodes, where several newly described Steinernema and Heterorhabditis species have been identified (Nguyen et al., Reference Nguyen, Malan and Gozel2006; Malan et al., Reference Malan, Nguyen and Addison2006, Reference Malan, Nguyen, De Waal and Tiedt2008; Hatting et al., Reference Hatting, Stock and Hazir2009). Therefore nematode surveys should be conducted throughout the African continent, especially areas with a moist, damp climate, where slugs are known to occur.

A total of 12 terrestrial slug species were identified in the WCP, representing seven families: Agriolimacidae, Arionidae, Chlamydephoridae, Limacidae, Milacidae, Testacellidae and Veronicellidae (table 1). These families have all been identified in previous surveys, but the species C. gibbonsi has not previously been isolated in the WCP (Herbert & Kilburn, Reference Herbert and Kilburn2004). Chlamydephorus gibbonsi is endemic to the Eastern Cape region, ranging from Zululand to East London, with occasional records in Transkei, Pietermaritzburg and the Colenso area (Herbert & Kilburn, Reference Herbert and Kilburn2004). This species occurs in a range of habitats, from indigenous forests to open thornveld (Herbert & Kilburn, Reference Herbert and Kilburn2004). It is possible that C. gibbonsi was introduced into the WCP though the importation of plant material, as a nursery was identified within 1 km of the isolation site.

A total of 521 terrestrial slugs were collected in the WCP, but only 33 slugs were native to South Africa and the remaining 488 slugs were exotic European species (table 1). There are numerous explanations for the success of these European invaders, but Ross et al. (Reference Ross, Ivanova, Severns and Wilson2010a) demonstrated that parasite release played an important role in the invasion of European slugs into North America. They showed that parasite prevalence and species richness was higher in the home range (UK) compared to the invasive range (USA). The results of the present survey are very similar to those of the invasive range (USA) described by Ross et al. (Reference Ross, Ivanova, Severns and Wilson2010a), where nematodes were present at 34% of USA study sites and 5.4% of all slugs examined were associated with nematodes. In South Africa, nematodes were present at 40% of study sites and 6% of slugs were infected. Species richness was also low in South Africa, with only seven species of nematode being identified, four of which were truly parasitic (tables 1 and 3). While the reduced prevalence of nematode parasites may have aided invasion by European slugs into South Africa, it is not possible from our data to be certain that parasite release is the only factor allowing invasion by these exotic slug species. Conversely, we cannot know whether invasion of European species may have been halted by nematode parasites indigenous to South Africa.

This paper presents the first systematic survey of nematodes associated with terrestrial slugs in the WCP of South Africa. This work will not only aid understanding of the slug/nematode association, but will also help with the identification of an indigenous isolate which could be developed as a biological molluscicide in South Africa. Future work should focus on the virulence and biocontrol potential of these nematodes, especially with regards to molluscs that have been identified as pestiferous in the region. However, before this can occur, tests should be conducted on the effects of these nematodes on native non-pestiferous slug species, as many molluscs are included in the Database of Threatened Invertebrates of South Africa (Herbert, Reference Herbert1997).

Acknowledgements

This work was carried out within the University of Aberdeen and the University of Stellenbosch, and was supported financially by Becker Underwood, the Biotechnology and Biological Sciences Research Council (BBSRC) and the British Society for Parasitology. We would like to thank Geoff Tribe, Annelize Lubbe, Scott Gilbert and staff in the Department of Conservation Ecology and Entomology at the University of Stellenbosch for their help with slug collections.

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Figure 0

Fig. 1 Map showing the location of sample sites in the Western Cape Province (WCP) of South Africa.

Figure 1

Table 1 Prevalence and abundance of nematodes associated with terrestrial slugs collected at various localities in the Western Cape Province (WCP) of South Africa.

Figure 2

Table 2 Sites in the Western Cape Province (WCP) of South Africa with nematodes associated with terrestrial slugs.

Figure 3

Table 3 Accession numbers, closest matches, identity and coverage of slug-parasitic nematodes isolated in the Western Cape Province (WCP) of South Africa.