Abstract
The present study deals with morphological differences between two closely related parasitic nematode species (Anguillicola crassus Kuwahara et al., 1974 and Anguillicola novaezelandiae Moravec & Taraschewski, 1988) in two different experimentally infected eel species (Anguilla anguilla Linnaeus, 1758 and Anguilla japonica Temminck & Schlegel, 1847). Furthermore, it considers the question whether size differences between those two species are ontogenetically determined or host species-dependent. In order to analyse these questions, experimental infections with the four possible host-parasite systems have been performed, followed by precise morphometric measurements related to body size and head structures of all resulting nematodes 120 days post infection. Body size measurements (length and width) of A. crassus generally exceeded those of A. novaezelandiae, while both Anguillicola species turned out to be smaller in Japanese eels than in European eels. Comparative measurements of neck width, maximum oesophagus width, and posterior head end width were found to be highly significant with regard to the different host-parasite systems. Shape and width of neck have been identified as reliable discriminating factors for species distinction. Generally, the relation of anterior head end width and neck width proved to be distinctly species-specific and can thus serve as a decisive and easily measureable distinguishing feature.
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Abdelmonem AA, Metwally MM, Hussein HS, Elsheikha HM (2010) Gross and microscopic pathological changes associated with parasitic infection in European eel (Anguilla anguilla, Linnaeus 1758). Parasitol Res 106:463–469
Blanc G, Bonneau S, Biaganti S, Petter AJ (1992) Description of the larval stages of Anguillicola crassus (Nematoda, Dracunculoidea) using light and scanning electron microscopy. Aquat Living Resour 5:307–318
Brunanska M, Fagerholm HP, Moravec F (2007) Structure of the pharynx in the adult nematode Anguillicoloides crassus (Nematoda: Rhabditida). J Parasitol 93(5):1017–1028
Brunanska M, Fagerholm HP, Moravec F, Vasilkova Z (2010) Ultrastructure of the buccal capsule in the adult female Anguillicoloides crassus (Nematoda: Anguillicolidae). Helminthologia 47(3):170–178
Dangel KC, Sures B (2013) Natural Anguillicola novaezelandiae infection—is there seasonality in New Zealand? Parasitol Res 112:1623–1630
Dangel KC, Keppel M, Sures B (2013) Can differences in life cycle explain differences in invasiveness?—a study on Anguillicola novaezelandiae in the European eel. Parasitology 140:1831–1836
Dangel KC, Keppel M, Le TTY, Grabner D, Sures B (2015) Competing invaders: performance of two Anguillicola species in Lake Bracciano. Int J Parasitol: Parasites Wildl 4:119–124
Fazio G, Sasal P, Da Silva C, Fumet B, Boissier J, Lecomte-Finiger R, Moné H (2008) Regulation of Anguillicola crassus (Nematoda) infrapopulations in their definitive host, the European eel, Anguilla anguilla. Parasitology 135:1707–1716
Grabner DS, Dangel KC, Sures B (2012) Merging species? Evidence for hybridization between the eel parasites Anguillicola crassus and A. novaezelandiae (Nematoda, Anguillicoloidea). Parasite Vector 5:244
Keppel M, Dangel KC, Sures B (2014) Comparison of infection success, development and swim bladder pathogenicity of two congeneric Anguillicola species in experimentally infected Anguilla anguilla and A. japonica. Parasitol Res 113:3727–3735
Knopf K, Lucius R (2008) Vaccination of eels (Anguilla japonica and Anguilla anguilla) against Anguillicola crassus with irradiated L3. Parasitology 135:633–640
Kuwahara A, Niimi A, Itagaki H (1974) Studies on a nematode parasitic in the air bladder of the eel. I. Description of Anguillicola crassa n. sp. (Philometridea, Anguillicolidae). Jpn J Parasitol 23:275–279
Laetsch DR, Heitlinger EG, Taraschewski H, Nadler SA, Blaxter ML (2012) The phylogenetics of Anguillicolidae (Nematoda: Anguillicolidea), swimbladder parasites of eels. BMC Evol Biol 12:60
Lefebvre F, Schuster T, Münderle M, Hine M, Poulin R (2004) Anguillicolosis in the short-finned eel Anguilla australis: epidemiology and pathogenicity. N Z J Mar Fresh 38:577–583
Loukili A, Belghyti D (2007) The dynamics of the nematode Anguillicola crassus, Kuvahara 1974 in eel Anguilla anguilla (L. 1758) in the Sebou estuary (Morocco). Parasitol Res 100:683–686
Maamouri F, Gargouri L, Ould Daddah M, Bouix G (1999) Occurrence of Anguillicola crassus (Nematoda, Anguillicolidae) in the Ichkeul lake (Northern Tunisia). Bull Eur Assoc Fish Pathol 19:17–19
Moravec F (1994) Parasitic nematodes of freshwater fishes of Europe. Academia, Prague
Moravec F (2006) Dracunculoid and anguillicoloid nematodes parasitic in vertebrates. Academia, Prague
Moravec F, Rohde K (1992) Three species of nematodes of the superfamily Dracunculoidea from Australian fishes. Acta Soc Zool Bohemoslov 56:187–195
Moravec F, Taraschewski H (1988) Revision of the genus Anguillicola Yamaguti, 1935 (Nematoda: Anguillicolidae) of the swimbladder of eels, including descriptions of two new species, A. novaezelandiae sp. n. and A. papernai sp. n. Folia Parasitol 35:125–146
Moravec F, Di Cave D, Orecchia P, Paggi L (1994a) Experimental observations on the development of Anguillicola crassus in its definitive host, Anguilla anguilla. Folia Parasitol 41(2):138–148
Moravec F, Di Cave D, Orecchia P, Paggi L (1994b) Present occurrence of Anguillicola novaezelandiae (Nematoda, Dracunculoidea) in Europe and its development in the intermediate host. Folia Parasitol 41:203–208
Münderle M (2005) Ökologische, morphometrische und genetische Untersuchungen an Populationen des invasiven Schwimmblasen-Nematoden Anguillicola crassus aus Europa und Taiwan. Dissertation, Karlsruhe Institute of Technology
Münderle M, Taraschewski H, Klar B, Chang CW, Shiao JC, Shen KN, He JT, Lin SH, Tzeng WN (2006) Occurrence of Anguillicola crassus (Nematoda: Dracunculoidea) in Japanese eels Anguilla japonica from a river and an aquaculture unit in SW Taiwan. Dis Aquat Org 71:101–108
Neumann W (1985) Schwimmblasenparasit Anguillicola bei Aalen. Fischer und Teichwirt 11:322
Nielsen ME (1999) An enhanced humoral immune response against the swimbladder nematode, Anguillicola crassus, in the Japanese eel, Anguilla japonica, compared with the European eel, A. anguilla. J Helminthol 73:227–232
Paggi L, Orecchia P, Minervini R, Mattiucci S (1982) Appearance of Anguillicola australiensis Johnston and Mawson, 1940 (Dracuncoloidea: Anguillicolidae) in Anguilla anguilla of Lake Bracciano. Parassitologia 24:139–144
Rolbiecki L (2008) New data on the biology of the introduced exotic nematode Anguillicola crassus Kuwahara, Niimi et Itagaki, 1974 in the eel Anguilla anguilla in Lake Wdzydze (Polish waters). Oceanol Hydrobiol Stud 37(3):37–48
Sorci G, Skarstein F, Morand S, Hugot JP (2003) Correlated evolution between host immunity and parasite life histories in primates and oxyurid parasites. Proc R Soc Lond B Biol 270:2481–2484
Taraschewski H, Moravec F, Lamah T, Anders K (1987) Distribution and morphology of two helminths recently introduced into European eel populations: Anguillicola crassus (Nemaotoda, Dracunculoidea) and Paratenuisentis ambiguus (Acanthocephala, Tenuisentidae). Dis Aquat Org 3:167–176
van Banning P, Haenen OLM (1990) Effects of the swimbladder nematode Anguillicola crassus in wild and farmed eel, Anguilla anguilla. In: Perkins FO, Cheng TC (eds) Pathology in Marine Science. Academic Press, San Diego, pp 317–330
Weclawski U, Heitlinger EG, Baust T, Klar B, Petney T, Han YS, Taraschewski H (2014) Rapid evolution of Anguillicola crassus in Europe: species diagnostic traits are plastic and evolutionarily labile. Front Zool 11:74
Wilkes CP, Thompson FJ, Gardner MP, Paterson S, Viney ME (2004) The effect of the host immune response on the parasitic nematode Strongyloides ratti. Parasitology 128:661–669
Acknowledgments
This study was funded by Deutsche Forschungsgemeinschaft (DFG) (grant number SU217/12-1).
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The authors declare that they have no competing interests.
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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
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Keppel, M., Dangel, K.C. & Sures, B. Size does matter—a closer look on Anguillicola morphology. Parasitol Res 114, 3479–3486 (2015). https://doi.org/10.1007/s00436-015-4576-y
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DOI: https://doi.org/10.1007/s00436-015-4576-y