Elena S. Ivanova

The role of parasite release in invasion of the USA by European slugs

Several species of European slugs are invasive in the USA, threatening native species and damaging agricultural and horticultural crops. One possible explanation for the success of these invaders is parasite release. To test this hypothesis we collected European slugs in part of their native range (United Kingdom) and in the USA and compared prevalence, distribution and species richness of their nematode parasites. All slugs were dissected and examined for the presence of nematodes. In the UK, nematodes were present at 93% of study sites and 16.4% of all slugs examined were associated with nematodes whereas in the USA the respective figures were 34% of sites and 5.4% of slugs. Nematode species richness was greater in the UK with 12 species being found, seven of which were thought to be truly parasitic as opposed to being phoretic or necromenic. Nine species of nematode were found in the USA, four of which were truly parasitic. Four of the ten European slug species examined in the USA, were entirely free of truly parasitic nematodes whereas all were infected by nematodes in some sites in the UK. There was a significant difference in the prevalence of truly parasitic nematodes in five of these species when comparing their home versus invasive range. A significant difference in parasite prevalence was observed when comparing native and introduced slug species in the USA, however, this was not significant in the UK. Our data support a role for parasite release during the invasion of the USA by European slugs.

Molecular phylogeny of slug-parasitic nematodes inferred from 18S rRNA gene sequences

Terrestrial molluscs are diverse and are infected by many nematodes. We propose a phylogeny of slug-parasitic nematodes using 18S rRNA gene sequences from nematodes isolated from slugs collected from six countries. Eight species, representing six families of nematodes were identified and trees inferred placed them within four (I, III, IV and V) out of the five clades of Nematoda, indicating multiple origins of slug parasitism. Five species representing three families formed a monophyletic group in clade V. Although these species are closely related, their morphology has changed greatly, suggesting adaptive radiation to fill different niches within the host.

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

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).

Two new species of Angiostoma Dujardin, 1845 (Nematoda: Angiostomatidae) from British terrestrial molluscs

Two new species of Angiostoma Dujardin, 1845 taken from the intestines of terrestrial molluscs (Gastropoda: Stylommatophora) collected in the UK are described and illustrated. Angiostoma milacis n. sp. is parasitic in milacid and agriolimacid slugs and is closely related to A. asamati Spiridonov, 1985. Angiostoma zonitidis n. sp. was found in a zonitid snail and is most closely related to A. kimmeriense Korol & Spiridonov, 1992 (emend.), a species also from zonitid snails. An amended generic diagnosis is proposed. The distribution of A. limacis and A. milacis sp. n. in hosts is discussed and a key to the species of Angiostoma is presented.

Survey of nematodes associated with terrestrial slugs in Norway.

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.

Angiostoma margaretae n. sp (Nematoda: Angiostomatidae), a parasite of the milacid slug Milax gagates Draparnaud collected near Caledon, South Africa

Angiostoma margaretae n. sp. (Angiostomatidae) is described from the oesophagus of the slug Milax gagates Draparnaud collected near Caledon in the Western Cape Province of South Africa. The new species closely resembles another parasite of a milacid slug, A. milacis Ivanova & Wilson, 2009, with a similar head, stoma and spicule shape, the presence of distally outstretched ovaries, coiled oviducts, the same number of caudal papillae and enlarged rectal glands. However, A. margaretae differs from the latter by having: a shorter, wider tail with a rounded vs pointed tip; the distal parts of both ovaries with a particular hook-like shape due to an expansion closely following the short initial zone; ovoviparous females; and a different arrangement of male papillae. A. margaretae is comparable with A. limacis Dujardin, 1845, A. asamati (Spiridonov, 1985), A. coloaense (Pham Van Luc, Spiridonov & Wilson, 2005) and A. stammeri (Mengert, 1953), which have a similar stoma shape and size, but can be readily differentiated by the presence of distally outstretched vs reflexed ovaries and the presence vs lack of enlarged rectal glands. The new species has a similar arrangement of the ovaries to A.kimmeriense Korol & Spiridonov, 1991 and A. zonitidis Ivanova & Wilson, 2009, but is clearly differentiated by the lack of an off-set lip region and presence of a large bowl-shaped vs tubular stoma and less numerous male caudal papillae (seven pairs vs nine in A.kimmeriense and 10 in A. zonitidis).

Born to be Wild – Don’t Forget the Invertebrates

Parasitology research mostly aims to control parasites of humans and domesticated animals. Recently, many scientists have realized much can be learned by studying wildlife parasites. To this end, Trends in Parasitology published two special issues comprising some of the most interesting, topical science relating to wildlife parasitology [1]. The emphasis of the published articles was almost exclusively on parasites that use vertebrate animal hosts. Here, we argue that progress in parasitology could be accelerated if more parasitologists studied parasites that use invertebrates as definitive hosts.

Neoalloionema tricaudatum gen. n., sp. n. (Nematoda: Alloionematidae) associated with a cyclophorid snail in Cuc Phuong Natural Park, Vietnam

A new nematode genus and species associated with terrestrial gastropods from Vietnam is described and illustrated. Partial SSU and ITS rDNA sequences were obtained and subjected to phylogenetic analysis. Both morphologically and molecularly, Neoalloionema tricaudatum gen. n., sp. n. is closest to Alloionema appendiculatum , another gastropod associate. It is differentiated from A. appendiculatum by the presence of an outstretched vs reflexed testis and the absence of denticles in the stoma, by the parasitic juveniles inhabiting the pallial cavity vs the foot of the host and having six vs two lips and large sucker-like phasmids vs pore-like. The most peculiar feature of N. tricaudatum gen. n., sp. n. is the presence of paired, solid appendages located at the mid-tail region of juveniles from the pallial cavity of the host. The nature of the association between N. tricaudatum gen. n., sp. n. and its gastropod host is discussed.

A new genus and two new nematode species (Drilonematoidea: Ungellidae: Synoecneminae) parasitic in two morphs of Drawida ghilarovi Gates, endemic earthworm from the Russian Far East.

Drasico n. g. is erected to accommodate two new species of nematode, Drasico nemoralis n. sp. and D. paludigenus n. sp., recovered from coelomic cavities of Drawida ghilarovi Gates, endemic earthworms of the Russian Far East. The new genus is characterised by the following unique for the Synoecneminae characters: apical portion of the head attenuated, cephalic hooks displaced to the base of attenuated portion, amphids displaced posterior to cephalic hooks, excretory duct short and weak, males possessing several genital papilliform sensilla. The new species are differentiated by the size, number and disposition of the male genital sensilla (larger and more numerous in D. nemoralis n. sp.); the body shape of females (with thinner neck and wider mid-body in D. paludigenus n. sp.) and the ovarian tube arranged in transversal folds in D. paludigenus (vs longitudinal folds in D. nemoralis n. sp.). Nucleotide sequences of D2–D3 expansion segment of 28S rDNA for the two new species differed at 13 positions. Phylogenetic analysis revealed close relationships of Drasico n. g. with species of Siconema Timm, 1966. The host species was represented by two morphs (blue-grey forest and tar-black meadow-swamp morph) with intraspecific divergence of 16–17% for cytochrome c oxidase subunit 1 (COI) gene, and each host morph was found infected by a different nematode species. A co-infection with the plectid nematode Creagrocercus drawidae Ivanova & Spiridonov, 2011 was recorded together with D. nemoralis n. sp. in the blue-grey forest morph.

Angiostoma norvegicum n. sp. (Nematoda: Angiostomatidae) a parasite of arionid slugs in Norway

Angiostoma norvegicum n. sp. (Angiostomatidae) is described from the oesophagus, crop and the buccal mass of five species of slugs of the family Arionidae, Arion vulgaris (Moquin-Tandon), Arion ater (L.), Arion fasciatus (Nilsson), Arion fuscus (Müller) and Arion rufus/Arion ater hybrid), collected throughout Norway. Angiostoma norvegicum n. sp. was found parasitising arionids at seven of the 30 sample sites examined (23.3%), and 9.9% of all Arion spp. were infected with this nematode. The new species is characterised by its large size (4.0–8.6 mm long) and in having: lateral alae; 6 + 6 papillae at the cephalic end; a large circular mouth aperture; a spacious stoma; a pharyngeal basal bulb without valvular apparatus; an excretory pore near the base of bulb; a distal part of posterior ovary always outstretched; an anterior ovary distally nearly always outstretched; a vulva situated anterior to mid-body; long, nearly straight spicules and a small gubernaculum; three circumcloacal papillae and caudal genital papillae (GP) arranged in a pattern 1+2/3+3 with GP 5 and GP 8 opened on dorsal side of narrow bursa not reaching tail tip; short conical tails in both sexes with tips supplied by 4 short, unequal denticles. Morphologically, A. norvegicum n. sp. is similar to Angiostoma limacis Dujardin, 1845, which diagnostic characteristics are given based on examination of specimens from Norway and the UK. Conversely, the phylogenetic analyses based on D2D3 large subunit (LSU) rRNA gene sequences performed in the present study did not support the morphological affinity of these two species. Phylogenetic analyses demonstrated that although Angiostoma spp. cluster together, A. norvegicum n. sp. forms a tight monophyletic clade with the milacid nematode parasites Angiostoma margaretae Ross, Malan & Ivanova, 2011 and Angiostoma milacis Ivanova & Wilson, 2009.