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Nematodes associated with terrestrial gastropod molluscs in Belgium and additional characterisation of Pellioditis californica and P. hermaphrodita

Published online by Cambridge University Press:  21 March 2024

M.A. Cortes ,
W. Bert ,
M. Couvreur ,
D. De Waele  and
P.R. Singh Open the ORCID record for P.R. Singh [Opens in a new window]
M.A. Cortes
Affiliation:
Nematology Research Unit, Department of Biology, Ghent University, K.L. Ledeganckstraat 35, 9000 Ghent, Belgium Department of Veterinary Paraclinical Sciences, College of Veterinary Medicine, Visayas State University, Visca, Baybay City, Leyte, Philippines
W. Bert
Affiliation:
Nematology Research Unit, Department of Biology, Ghent University, K.L. Ledeganckstraat 35, 9000 Ghent, Belgium
M. Couvreur
Affiliation:
Nematology Research Unit, Department of Biology, Ghent University, K.L. Ledeganckstraat 35, 9000 Ghent, Belgium
D. De Waele
Affiliation:
Unit for Environmental Sciences and Management, North-West University, Private Bag X6001, Potchefstroom, South Africa Laboratory of Tropical Crop Improvement, Department of Biosystems, Faculty of Bioscience Engineering, University of Leuven, Willem de Croylaan 42, 3001 Heverlee, Belgium
P.R. Singh*
Affiliation:
Department of Entomology and Nematology, Fort Lauderdale Research and Education Center, Institute of Food and Agricultural Sciences, University of Florida, 3205 College Ave., Davie, FL 33314-7719, USA
*
Corresponding author: P. R. Singh; Email: rolishsingh@gmail.com
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Abstract

A survey for slug- and snail-associated nematodes was conducted in forests, parks, botanical gardens, and nature reserves at 13 localities in Belgium to uncover more diversity of gastropod mollusc-associated nematodes and to characterise Pellioditis populations found in the country. A total of 319 slugs and snails belonging to nine species were examined. Arion vulgaris was the most commonly found mollusc species in this study (eight locations), and 19.4% of the examined mollusc specimens were found infected by nematodes. The highest prevalence of nematodes was observed in Cornu aspersum (60%) followed by A. vulgaris (34.8%), Limax maximus (28.6%), and Cepaea sp. (20%). Eleven nematode species belonging to eight families were isolated and identified from the mollusc hosts including Alloionema appendiculatum, Angiostoma dentiferum, A. gandavense, Angiostrongylus vasorum, Cosmocerca longicauda, Panagrolaimus cf. subelongatus, Pellioditis californica, P. hermaphrodita, Rhabditis sp., Tetrameres cf. fissispina, and Troglostrongylus cf. brevior. Pellioditis was the most commonly found nematode genus (at nine localities) and C. longicauda and P. californica were reported in Belgium for the first time. Co-infections of more than one nematode species were observed in eight (2.5%) molluscs specimens. Most co-infections consisted of two nematode species. In one A. vulgaris specimen, a co-infection of three nematode species (A. vasorum, P. hermaphrodita, and Tetrameres cf. fissispina) was observed. Four ex vivo cultures of P. californica and six ex vivo cultures of P. hermaphrodita were established from single hermaphrodites, and both species were described based on light microscopy, scanning electron microscopy, and morphometric, morphological, and molecular data.

Keywords

Mollusc parasitic-nematodespoint prevalenceslugssnailssurvey

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Type
Research Paper
Information
Journal of Helminthology , Volume 98 , 2024 , e27
Copyright
© The Author(s), 2024. Published by Cambridge University Press

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References

Abd El-Halim, SM, Ali, HH, El-Sayed, AM and Ali, RF (2021) Preliminary study on survey and population dynamic of the terrestrial snail Monacha obstructa (Pfeiffer) (Hygromiidae, Mollusca) at crop fields in Fayoum governorate, Egypt.Pakistan Journal of Biological Sciences 24, 928–938.CrossRefGoogle Scholar
Antzée-Hyllseth, H, Trandem, N, Torp, T and Haukeland, S (2020) Prevalence and parasite load of nematodes and trematodes in an invasive slug and its susceptibility to a slug parasitic nematode compared to native gastropods. Journal of Invertebrate Pathology 173, 107372.CrossRefGoogle Scholar
Barker, GM (2001) The Biology of Terrestrial Molluscs. London, UK: CABI Publishing.CrossRefGoogle Scholar
Barratt, J, Chan, D, Sandaradura, I, Malik, R, Spielman, D, Lee, R, Marriott, D, Harkness, J, Ellis, J and Stark, D (2016) Angiostrongylus cantonensis: A review of its distribution, molecular biology and clinical significance as a human pathogen. Parasitology 143, 1087–118.CrossRefGoogle ScholarPubMed
Bhardwaj, P (2019) Types of sampling in research. Journal of the Practice of Cardiovascular Sciences 5, 157–163.CrossRefGoogle Scholar
Bowles, J, Blair, D and McManus, DP (1992) Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165–173.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. Journal of Nematology 52, 1–3.CrossRefGoogle ScholarPubMed
Carnaghi, M, Rae, R, De Ley, IT, Johnston, E, Kindermann, G, Mc Donnell, R, O’Hanlon, A, Reich, I, Sheahan, J, Williams, CD and Gormally, MJ (2017) Nematode associates and susceptibility of a protected slug (Geomalacus maculosus) to four biocontrol nematodes. Biocontrol Science and Technology 27, 294–299.CrossRefGoogle Scholar
Coupland, JB (1995) Susceptibility of helicid snails to isolates of the nematode Phasmarhabditis hermaphrodita from southern France. Journal of Invertebrate Pathology 66, 207–208.CrossRefGoogle Scholar
De Grisse, AT (1965) Redescription ou modifications de quelques techniques utilisées dans l’étude des nematodes phytoparasitaires. Mededelingen Rijksfaculteit Landbouwwetenschappen Gent 34, 351–359.Google Scholar
Etongwe, CM, Singh, PR, Bert, W and Subbotin, SA (2020) Molecular characterisation of some plant-parasitic nematodes (Nematoda: Tylenchida) from Belgium. Russian Journal of Nematology 28, 1–28.Google Scholar
Genena, MA, Mostafa, FA, Fouly, AH and Yousef, AA (2011) First record for the slug parasitic nematode, Phasmarhabditis hermaphrodita (Schneider) in Egypt. Archives of Phytopathology and Plant Protection 44, 340–345.CrossRefGoogle Scholar
Giannelli, A, Cantacessi, C, Colella, V, Dantas-Torres, F and Otranto, D (2016) Gastropod-borne helminths: a look at the snail-parasite interplay. Trends in Parasitology 32, 255–264.CrossRefGoogle Scholar
Grootaert, P and Maertens, D (1976) Cultivation and life cycle of Mononchus aquaticus. Nematologica 22, 173–181.CrossRefGoogle Scholar
Halwart, M (1994) The golden apple snail Pomacea canaliculata in Asian rice farming systems: Present impact and future threat. International Journal of Pest Management 40, 199–206.CrossRefGoogle Scholar
Hooper, D, Wilson, M, Rowe, J and Glen, D (1999) Some observations on the morphology and protein profiles of the slug-parasitic nematodes Phasmarhabditis hermaphrodita and P. neopapillosa (Nematoda: Rhabditidae). Nematology 1, 173–182.CrossRefGoogle Scholar
Howe, DK, Ha, AD, Colton, A, De Ley, IT, Rae, RG, Ross, J, Wilson, M, Nermuť, J, Zhao, Z, Mc Donnell, RJ and Denver, DR (2020). Phylogenetic evidence for the invasion of a commercialized European Phasmarhabditis hermaphrodita lineage into North America and New Zealand. PLoS One 15, e0237249.CrossRefGoogle ScholarPubMed
Huang, RE, Ye, W, Ren, X and Zhao, Z (2015). Morphological and molecular characterization of Phasmarhabditis huizhouensis sp. nov. (Nematoda: Rhabditidae), a new rhabditid nematode from South China. PLoS One 10, e0144386.CrossRefGoogle ScholarPubMed
Huelsenbeck, JP and Ronquist, F (2001) MRBAYES: Baysian inference of phylogenetic trees. Bioinformatics 17, 754–755.CrossRefGoogle Scholar
Ivanova, ES and Wilson, MJ (2009) Two new species of Angiostoma Dujardin, 1845 (Nematoda: Angiostomatidae) from British terrestrial molluscs. Systematic Parasitology 74:113–124.CrossRefGoogle ScholarPubMed
Ivanova, E, Van Luc, P and Spiridonov, S (2015) Neoalloionema tricaudatum gen. n., sp. n. (Nematoda: Alloionematidae) associated with a cyclophorid snail in Cuc Phuong Natural Park, Vietnam. Nematology 18, 109–120.CrossRefGoogle Scholar
Jolly, S, Poncelet, L, Lempereur, L, Caron, Y, Bayrou, C, Cassart, D, Grimm, F and Losson, B (2014) First report of a fatal autochthonous canine Angiostrongylus vasorum infection in Belgium. Parasitology International 64, 97–99.CrossRefGoogle ScholarPubMed
Joshi, RC (2007) Problems with the management of the golden apple snail Pomacea canaliculata: an important exotic pest of rice in Asia. In Vreysen, MJB, Robinson, AS, and Hendrichs, J (eds), Area-Wide Control of Insect Pests: From Research to Field Implementation. Dordrecht: Springer Netherlands, pp. 257–264.CrossRefGoogle Scholar
Kanzaki, N and Futai, K (2002) A PCR primer set for determination of phylogenetic relationships of Bursaphelenchus species within the xylophilus group. Nematology 4, 35–41.CrossRefGoogle Scholar
Karimi, J, Kharazi-Pakdel, A and Robert, SJ (2003) Report of pathogenic nematode of slugs, Phasmarhabditis hermaphrodita (Nematoda: Rhabditida) in Iran. Journal of Entomological Society of Iran 22, 77–78.Google Scholar
Kerney, M, Cameron, RAD and Riley, G (1979) A Field Guide to the Land Snails of Britain and North-West Europe. London, UK: Collins.Google Scholar
Keyte, M, Grannell, A, Sheehy, L, Shepherd, J and Rae, R (2022) Phasmarhabditis californica in Germany. Nematology 24, 475–480.CrossRefGoogle Scholar
Kumar, P (2020) A review—on molluscs as an agricultural pest and their control. International Journal of Food Science and Agriculture 4, 383–389.CrossRefGoogle Scholar
Lempereur, L, Martinelle, L, Marechal, F, Bayrou, C, Dalemans, AC, Schnyder, M and Losson, B (2016) Prevalence of Angiostrongylus vasorum in southern Belgium, a coprological and serological survey. Parasites & Vectors 9:1–7.CrossRefGoogle ScholarPubMed
Maupas, E (1900). Modes et formes de reproduction des nematodes. Archives de Zoologie Expérimentale et Générale 8-2148-7–104.Google Scholar
Mayer, WE, Herrmann, M and Sommer, RJ (2007) Phylogeny of the nematode genus Pristionchus and implications for biodiversity, biogeography and the evolution of hermaphroditism. BMC Evolutionary Biology 7, 104.CrossRefGoogle ScholarPubMed
Mc Donnell, RJ, Paine, TD and Gormally, MJ (2009) Slugs: A Guide to the Invasive and Native Fauna of California. University of California, Agricultural and Natural Resources Publications.CrossRefGoogle Scholar
Mc Donnell, RJ, Colton, AJ, Howe, DK and Denver, DR (2020) Lethality of four species of Phasmarhabditis (Nematoda: Rhabditidae) to the invasive slug, Deroceras reticulatum (Gastropoda: Agriolimacidae) in laboratory infectivity trials. Biological Control 150, 104349.CrossRefGoogle Scholar
Mc Donnell, RJ, Howe, DK and Denver, DR (2023) First report of the gastropod-killing nematode, Phasmarhabditis californica, in Washington State, U.S.A. Journal of Nematology 55, 1–3.Google ScholarPubMed
Mengert, H (1953) Nematoden und Schnecken. Zeitschrift für Morphologie und Ökologie Tiere 41, 311–349.CrossRefGoogle Scholar
Meyer, WM, Ostertag, R and Cowie, RH (2011) Macro-invertebrates accelerate litter decomposition and nutrient release in a Hawaiian rainforest. Soil Biology and Biochemistry 43, 206–211.CrossRefGoogle Scholar
Morgan, ER, Modry, D, Paredes-Esquivel, C, Foronda, P and Traversa, D (2021) Angiostrongylosis in animals and humans in Europe. Pathogens 10, 1236.CrossRefGoogle ScholarPubMed
Nadler, SA, Carreno, RA, Mejía-Madrid, H, Ullberg, J, Pagan, C, Houston, R and Hugot, JP (2007) Molecular phylogeny of clade III nematodes reveals multiple origins of tissue parasitism. Parasitology 134, 1421–1442.CrossRefGoogle ScholarPubMed
Nermuť, J, Půža, V and Mráček, Z (2010) The first report on the slug parasitic nematode Phasmarhabditis hermaphrodita (Nematoda: Rhabditidae) in the Czech Republic. In 30th International Symposium of the European Society of Nematologists, Vienna, Austria.Google Scholar
Nermuť, J, Půža, V and Mráček, Z (2019) Bionomics of the slug-parasitic nematode Alloionema appendiculatum and its effect on the invasive pest slug Arion vulgaris. Biocontrol 64, 697–707.CrossRefGoogle Scholar
Nguyen, HT, Trinh, QP, Couvreur, M, Singh, PR, Decraemer, W and Bert, W (2019) Molecular and morphological characterisation of a new root-lesion nematode, Pratylenchus horti n. sp.(Tylenchomorpha: Pratylenchidae), from Ghent University Botanical Garden. Nematology 21, 739–752.CrossRefGoogle Scholar
Pandian, D, Najer, T and Modry, D (2023) An overview of Angiostrongylus cantonensis (Nematoda: Angiostrongylidae), an emerging cause of human angiostrongylosis on the Indian subcontinent. Pathogens 12, 852.CrossRefGoogle ScholarPubMed
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
Podgornaya, M, Didenko, N, Vasilchenko, A, Kashchits, J and Mishchenko, I (2020) Control of the number of field slugs Deroceras agreste L. in the plantations of garden strawberry. BIO Web of Conferences 25, https://doi.org/10.1051/bioconf/20202506007.CrossRefGoogle Scholar
Rae, R, Verdun, C, Grewal, PS, 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
Ramos-de-Souza, J, Maldonado, A Jr, Vilela, RV, Andrade-Silva, BE, Barbosa, HS, Gomes, SR and Thiengo, SC (2021) First report of the nematode Cruzia tentaculata using molluscs as natural intermediate hosts, based on morphology and genetic markers. International Journal for Parasitology: Parasites and Wildlife 15, 105–111.Google ScholarPubMed
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
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 ScholarPubMed
Ross, JL, Ivanova, ES, Spiridonov, SE, Waeyenberge, L, Moens, M, Nicol, GW and Wilson, MJ (2010) Molecular phylogeny of slug-parasitic nematodes inferred from 18S rRNA gene sequences. Molecular Phylogenetics and Evolution 55, 738–743.CrossRefGoogle ScholarPubMed
Seinhorst, JW (1959) A rapid method for the transfer of nematodes from fixative to anhydrous glycerine. Nematologica 4, 67–69.CrossRefGoogle Scholar
Sudhaus, W (2018) Various evolutionary avenues of Nematoda to parasitism in Gastropoda. Soil organisms 90, 115–122.Google Scholar
Shakeel, MA and Mowat, DJ (1992) The potential transmission of clover rot, Sclerotinia trifoliorum Erikss., by slugs. Grass and Forage Science 47, 199–202.CrossRefGoogle Scholar
Sheehy, L, Cutler, J, Weedall, GD and Rae, R (2022) Microbiome analysis of malacopathogenic nematodes suggests no evidence of a single bacterial symbiont responsible for gastropod mortality. Frontiers in Immunology 13, 878783.CrossRefGoogle ScholarPubMed
Singh, PR, Couvreur, M, Decraemer, W and Bert, W (2019) Survey of slug-parasitic nematodes in East and West Flanders, Belgium and description of Angiostoma gandavensis n. sp. (Nematoda: Angiostomidae) from arionid slugs. Journal of Helminthology 94, e35.CrossRefGoogle Scholar
Singh, PR, Karssen, G, Couvreur, M and Bert, W (2020) Morphological and molecular characterization of Heterodera dunensis n. sp. (Nematoda: Heteroderidae) from Gran Canaria, Canary Islands. Journal of Nematology 52, 1–14.Google Scholar
Singh, PR, Karssen, G, Couvreur, M, Subbotin, SA and Bert, W (2021) Integrative taxonomy and molecular phylogeny of the plant-parasitic nematode genus Paratylenchus (Nematoda: Paratylenchinae): Linking species with molecular barcodes. Plants 10, 408.CrossRefGoogle ScholarPubMed
Spratt, DM (2015) Species of Angiostrongylus (Nematode: Metastrongyloidea) in wildlife: A review. International Journal of Parasitology: Parasites and Wildlife 4, 178–189.Google ScholarPubMed
Stenberg, J, Melby, KK, Magnusson, C, Nielsen, A, Rydning, J, Wendell, PHM, Alsanius, B, Krokene, P, Thomsen, IM, Wright, SA and Rafoss, T (2021) Risk assessment of the biocontrol product Nemaslug 2.0 with the active organisms Phasmarhabditis californica (strain P19D) and Moraxella osloensis. Scientific Opinion of the Panel on Plant Health of the Norwegian Scientific Committee for Food and Environment.Google 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
Tandingan De Ley, I, Kiontke, K, Bert, W, Sudhaus, W and Fitch, DH (2023) Pellioditis pelhami n. sp. (Nematoda: Rhabditidae) and Pellioditis pellio (Schneider, 1866), earthworm associates from different subclades within Pellioditis (syn. Phasmarhabditis Andrássy, 1976). bioRxiv 2023:2023-06.Google Scholar
Tandingan De Ley, I, 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, Schurkman, J, Wilen, C and Dillman, AR (2020) Mortality of the invasive white garden snail Theba pisana exposed to three US isolates of Phasmarhabditis spp (P. hermaphrodita, P. californica, and P. papillosa). PloS One 15, e0228244.CrossRefGoogle ScholarPubMed
Thomas, AK, Mc Donnell, RJ, Paine, TD and Hardwood, JD (2010) A Field Guide to the Slugs of Kentucky. University of Kentucky College of Agriculture, Agricultural Experiment Station Publication SR-103.Google Scholar
Vrain, TC, Wakarchuk, DA, Levesque, AC and Hamilton, RI (1992) Intraspecific rDNA restriction fragment length polymorphism in the Xiphinema americanum group. Fundamental and Applied Nematology 15, 563–573.Google Scholar
Waki, T (2017) Diversity of terrestrial mollusks and their helminths in artificial environments in Yoyogi Park, Tokyo, Japan. Journal of Asia-Pacific Biodiversity 10, 254–256.CrossRefGoogle Scholar
Wilson, MJ, Burch, G, Tourna, M, Aalders, LT and Barker, GM (2012) The potential of a New Zealand strain of Phasmarhabditis hermaphrodita for biological control of slugs. New Zealand Plant Protection 65, 161–165.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
Zheng, L, Deng, L, Zhong, Y, Wang, Y, Guo, W and Fan, X (2021). Molluscicides against the snail-intermediate host of Schistosoma: a review. Parasitology Research 120, 3355–3393.CrossRefGoogle ScholarPubMed