Various evolutionary avenues of Nematoda to parasitism in Gastropoda

Authors

  • Walter Sudhaus Institut für Biologie/Zoologie der Freien Universität, Königin-Luise-Str. 1-3, 14195 Berlin, Germany

DOI:

https://doi.org/10.25674/1yds-c108

Keywords:

necromeny, parasitoidism, larval parasitism, paratenic host, host switch

Abstract

The various associations between nematodes and gastropods, which range from random transportation to endophoresis, necromeny, larval parasitism and an entire parasitic or parasitoidic life-style with and without intermediate or paratenic hosts, are discussed in an evolutionary context. Ten to eleven lineages have accomplished the transition to a life at the expense of gastropods, three via a detour of parasitism in vertebrates (Metastrongyloidea, Nemhelix and within Cosmocercoides). In the lineage to Agfa the sequence endophoretic, necromenic, parasitic in the intestine to parasitic in salivary glands of gastropods is reconstructed.

Downloads

Download data is not yet available.

References

Anantaraman, S. (1964): A juvenile Echinocephalus uncinatus (Molin, 1858) in the marine gastropod, Hemifusus pugilinus (Born), with notes on the genus Echinocephalus (Nematoda : Gnathostomidae). – Annals and Magazine of Natural History 7: 101 – 105.

Anderson, R. C. (2000): Nematode parasites of vertebrates: Their development and transmission. 2nd ed., CAB International, Wallingford, U.K. & New York, USA: 650 pp.

Anderson, R. C. & C. M. Bartlett (1993): Daubaylia pearsoni n. sp. (Nematoda: Daubayliidae) in Glyptophysa gibbosa (Planorbidae) in Australia. – Journal of Parasitlogy 79: 671 – 673.

Azzam, K. M. (2003): Description of the nematode Phasmarhabditis tawfiki n. sp. isolated from Egyptian terrestrial snails and slugs. – Journal of the Egyptian German Society of Zoology 42D: 79 – 87.

Azzam, K. M. (2006): Survey of terrestrial gastropods, their host plants and parasitic nematodes as biocontrol agents. – Journal of the Egyptian German Society of Zoology 49D: 49 – 61.

Azzam, K. M. & M. H. Belal (2006): Survey on the nematodes isolated from aquatic snails and their potential as bio-control agents of snails. – Bulletin of the Faculty of Agriculture, Cairo University 57: 185 – 198.

Baker, M. R. (1978): Transmission of Cosmocercoides dukae (Nematoda: Cosmocercoidea) to amphibians. – Journal of Parasitlogy 64: 765 – 766.

Ballantyne, R. J. (1991): Life history and development of Pneumonema tiliquae (Nematoda: Rhabdiasidae). – International Journal for Parasitology 21: 521 – 533.

Bartlett, C. M. & R. C. Anderson (1985): Larval nematodes (Ascaridida and Spirurida) in the aquatic snail, Lymnaea stagnalis. Journal of Invertebrate Pathology 46: 153 – 159.

Baruš, V. (1964): Freshwater snails as reservoir hosts of invasive larvae of the nematode Syngamus (S.) trachea (Montagu 1811). – Proceedings of the Symposium “Parasitic worms and aquatic conditions”, Prague: 83 – 89.

Berry, G. N. & L. R. G. Cannon (1981): The life history of Sulcascaris sulcata (Nematoda: Ascaridoidea), a parasite of marine molluscs and turtles. – International Journal for Parasitology 11: 43 – 54.

Camino, N. B. & S. E. Gonzàlez (2011): Daubaylia n. sp. (Nematoda, Daubayliidae), a parasite of the snail Helix aspersa (Müller) (Mollusca, Pulmonata, Helicidae) from Argentina. – Studi Trentini di Scienze Naturali 88: 29 – 32.

Carreno, R. A. & S. A. Nadler (2003): Phylogenetic analysis of the Metastrongyloidea (Nematoda: Stongylida) inferred from ribosomal RNA gene sequences. – Journal of Parasitology 89: 965 – 973.

Charwat, S. M. & K. A. Davies (1999): Laboratory screening of nematodes isolated from South Australia for potential as biocontrol agents of helicid snails. – Journal of Invertebrate Pathology 74: 55 – 61.

Cheng, T. C. (1978): Larval nematodes parasitic in shellfish. – Marine Fisheries Review 40: 39 – 42.

Chitwood, B. G. & M. B. Chitwood (1934): Daubaylia potomaca n . sp., a nematode parasite of snails, with a note on other nemas associated with molluscs. – Proceedings of the Helminthological Society of Washington 1: 8 – 9.

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

Dougherty, E. C. (1951): Evolution of zoöparasitic groups in the phylum Nematoda, with special reference to host-distribution. – Journal of Parasitology 37: 353–378.

Dundee, D. S. (1977): Mermithids in introduced molluscs. – Journal of Parasitology 63: 590.

Grewal, P. S., S. K. Grewal, L. Tan & B. J. Adams (2003): Parasitism of molluscs by nematodes: types of associations and evolutionary trends. – Journal of Nematology 35: 146 – 156.

Hagmeier, A. (1912): Beiträge zur Kenntnis der Mermithiden. – Zoologische Jahrbücher (Systematik) 32: 1 – 92.

Holovachov, O., S. Boström, N. Reid, A. Warén & C. Schander (2011): Endeolophos skeneae sp. nov. (Chromadoridae) – a free-living marine nematode epibiotically associated with deep-sea gastropod Skenea profunda (Skeneidae). – Journal of the Marine Biological Association of the United Kingdom 91: 387 – 394.

Holovachov, O., L. Camp & S. A. Nadler (2015): Sensitivity of ribosomal RNA character sampling in the phylogeny of Rhabditida. – Journal of Nematology 47: 337 – 355.

Huang, R.-E., W. Ye, X. Ren & Z. Zhao (2015): Morphological and molecular characterization of Phasmarhabditis huizhouensis sp. nov. (Nematoda: Rhabditidae), a new rhabditid nematode from South China. PLoS One 10: e0144386.

Ivanova, E. S., M. S. Panayotova-Pencheva & S. E. Spiridonov (2013a): 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.

Ivanova, E. S., S. E. Spiridonov, W. C. Clark, M. Tourna, M. Wilson & G. M. Barker (2013b): Description and systematic affinity of Alaninema ngata n. sp. (Alaninematidae: Panagrolaimorpha) parasitising leaf-veined slugs (Athoracophoridae: Pulmonata) in New Zealand. – Nematology 15: 859 – 870.

Juhász, A. (2014): Detection of Hexamermis albicans nematode in Succinea putris ambersnail in Hungary. V4 Parasitological Meeting, Stará Lesná, Slovakia, Abstracts: 22 – 23.

Kaiser, H. (1977): Untersuchungen zur Morphologie, Biometrie, Biologie und Systematik von Mermithiden. Ein Beitrag zum Problem der Trennung morphologisch schwer unterscheidbarer Arten. – Zoologische Jahrbücher (Systematik) 104: 20 – 71.

Langford, G. J. & J. Janovy (2009): Comparative life cycles and life histories of North American Rhabdias spp. (Nematoda: Rhabdiasidae): Lungworms from snakes and anurans. – Journal of Parasitology 95: 1145 – 1155.

Mengert, H. (1953): Nematoden und Schnecken. – Zeitschrift für Morphologie und Ökologie der Tiere 41: 311 – 349.

Mienis, H. K. (1986): First record of the parasitic nematode, Hexamermis albicans, from a slug in Israel. – Zoology in the Middle East 1: 156.

Miljutin, D. M. (2014): Order Marimermithida Rubtzov 1980, emend. Tchesunov 1995. In: Schmidt-Rhaesa, A. (ed.): Nematoda. Handbook of Zoology. De Gruyter, Berlin, Boston: 345 – 350.

Millemann, R. E. (1963): Studies on the taxonomy and life history of echinocephalid worms (Nematoda: Spiruroidea) with a complete description of Echinocephalus pseudouncinatus Millemann, 1951. – Journal of Parasitology 49: 754 – 764.

Morand, S. & G. M. Barker (1995): Hugotdiplogaster neozelandia n. gen., n. sp. (Nematoda: Diplogasteridae), a parasite of the New Zealand endemic slug, Athoracophorus bitentaculatus (Quoy & Gaimard, 1832) (Gastropoda: Athoracophoridae). – New Zealand Journal of Zoology 22: 109 – 113.

Morand, S., M. J. Wilson & D. M. Glen (2004): Nematodes (Nematoda) parasitic in terrestrial gastropods. In: Barker, G. M. (ed.): Natural Enemies of Terrestrial Molluscs. – CABI Publishing, Wallingford, UK, Cambridge, MA: 525 – 557.

Moravec, F. (1996): Aquatic invertebrates (snails) as new paratenic hosts of Anguillicola crassus (Nematoda: Dracunculoidea) and the role of paratenic hosts in the life cycle of this parasite. – Diseases of Aquatic Organisms 27: 237 – 239.

Morley, N. J. (2010): Aquatic molluscs as auxiliary hosts for terrestrial nematode parasites: implications for pathogen transmission in a changing climate. – Parasitology 137: 1041 – 1056.

Nermut’, J. & V. Půža (2017): Slug parasitic nematodes: biology, parasitism, production and application. – In: Abd-Elgawad, M. M. M., T. H. Askary & J. Coupland (eds): Biocontrol Agents: Entomopathogenic and Slug Parasitic Nematodes. CABI, Wallingford, UK, Boston, USA: 533 – 547.

Petersen, C., R. J. Hermann, M.-C. Barg, R. Schalkowski, P. Dirksen, C. Barbosa & H. Schulenburg (2015): Travelling at a slug’s pace: possible invertebrate vectors of Caenorhabditis nematodes. – BMC Ecology 15: 19.

Pieterse, A. (2016): Investigating the potential of indigenous nematode isolates to control invasive molluscs in canola. – Thesis, Stellenbosch University: 120 pp.

Pieterse, A., A. P. Malan, L. M. Kruitbos, W. Sirgel & J. L. Ross (2017): Nematodes associated with terrestrial slugs from canola fields and ornamental nurseries in South Africa. – Zootaxa 4312: 194 – 200.

Poinar, G. O. (1984): Daubaylia olsoni sp. n. (Daubayliidae: Rhabditida) from the leech, Diana anoculata, in California. – Proceedings of the Helminthological Society of Washington 51: 217 – 220.

Poinar, G. O. (2011): The evolutionary history of nematodes – as revealed in stone, amber and mummies. Brill, Leiden, Boston: 429 pp.

Poinar, G. O. (2015): The geological record of parasitic nematode evolution. – Advances in Parasitology 90: 53 – 92.

Ross, J. L., E. S. Ivanova, B. A. Hatteland, M. B. Brurberg & S. Haukeland (2016): Survey of nematodes associated with terrestrial slugs in Norway. – Journal of Helminthology 90: 583 – 587.

Ross, J. L., E. S. Ivanova, P. M. Severns & M. J. Wilson (2010a): The role of parasite release in invasion of the USA by European slugs. – Biological Invasions 12: 603 – 610.

Ross, J. L., E. S. Ivanova, W. F. Sirgel, A. P. Malan & M. J. Wilson (2012): Diversity and distribution of nematodes associated with terrestrial slugs in the Western Cape Province of South Africa. – Journal of Helminthology 86: 215 – 221.

Ross, J. L., E. S. Ivanova, S. Spiridonov, G. Nicol & M. J. Wilson (2009): Phylogeny of nematodes associated with terrestrial slugs inferred from 18S rRNA sequences. – Insect Pathogens and Insect Parasitic Nematodes IOBC/wprs Bulletin 45: 473 – 475.

Ross, J. L., E. S. Ivanova, S. E. Spiridonov, L. Waeyenberge, M. Moens, G. W. Nicol & M. J. Wilson (2010b): Molecular phylogeny of slug-parasitic nematodes inferred from 18S rRNA gene sequences. – Molecular Phylogenetics and Evolution 55: 738 – 743.

Sudhaus, W. (2010): Preadaptive plateau in Rhabditida (Nematoda) allowed the repeated evolution of zooparasites, with an outlook on evolution of life cycles within Spiroascarida. – Palaeodiversity 3: Supplement: 117–130.

Sudhaus, W. (2018): Dispersion of nematodes (Rhabditida) in the guts of slugs and snails. – Soil Organisms 90 (3): 101– 114.

Tan, L. & P. S. Grewal (2001): Infection behavior of the rhabditid nematode Phasmarhabditis hermaphrodita to the grey garden slug Deroceras reticulatum. – Journal of Parasitology 87: 1349 – 1354.

Thiengo, S. C. (1995): Presence of mermithid larvae (Nematoda, Mermithidae) in Limax flavus and Sarasinula marginata (Mollusca, Gastropoda) in Brazil. – Memórias do Instituto Oswaldo Cruz 90: 347.

Vanderburgh, D. J. & R. C. Anderson (1987): The relationship between nematodes of the genus Cosmocercoides Wilkie, 1930 (Nematoda: Cosmocercoidea) in toads (Bufo americanus) and slugs (Deroceras laeve) . – Canadian Journal of Zoology 65: 1650 – 1661.

Zaborski, E. R., L. A. Gittenger & S. J. Roberts (2001): A possible Phasmarhabditis sp. (Nematoda: Rhabditidae) isolated from Lumbricus terrestris (Oligochaeta: Lumbricidae). – Journal of Invertebrate Pathology 77: 284 – 287.

Downloads

Published

2018-12-01

Issue

Section

ARTICLES

How to Cite

Sudhaus, W. (2018). Various evolutionary avenues of Nematoda to parasitism in Gastropoda. Soil Organisms, 90(3), 115–122. https://doi.org/10.25674/1yds-c108