Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-13T04:19:57.339Z Has data issue: false hasContentIssue false

New perspectives on Nephridiacanthus major (Acanthocephala: Oligacanthorhynchidae) collected from hedgehogs in Iran

Published online by Cambridge University Press:  02 March 2020

O.M. Amin*
Affiliation:
Institute of Parasitic Diseases, 11445 E Via Linda 2-419, Scottsdale, Arizona85259, USA
M. Sharifdini
Affiliation:
Cellular and Molecular Research Center, Guilan University of Medical Sciences, Rasht, Iran Department of Medical Parasitology and Mycology, School of Medicine, Guilan University of Medical Sciences, Rasht, Iran
R.A. Heckmann
Affiliation:
Department of Biology, Brigham Young University, 1114 MLBM, Provo, Utah84602, USA
M. Zarean
Affiliation:
Department of Parasitology and Mycology, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
*
Author for correspondence: O.M. Amin, E-mail: omaramin@aol.com

Abstract

We describe morphological features not previously reported for this old acanthocephalan Nephridiacanthus major (Bremser, 1811 in Westrumb, 1821) Golvan, 1962 first described over 200 years ago. Our specimens were collected from long-eared hedgehog Hemiechinus auritus (Gmelin, 1770) (Erinaceidae) in Iran. We compare the morphometrics of our material with others previously reported from the same host in Iran, Russia, central Asia and Europe. Our specimens had markedly smaller proboscides, proboscis hooks and lemnisci than those reported from Russia and central Asia, but comparable measurements of other structures with specimens previously described from other collections. We document our new observations with scanning electron microscopy features not previously demonstrable by other observers and provide a chemical analysis of proboscis hooks using energy-dispersive X-ray analysis for the first time. The molecular profile of this acanthocephalan, based on 18S rDNA and cox1 genes, was generated for the first time. The phylogenetic analysis showed that N. major is placed in a clade of the family Oligacanthorhynchidae, well separated from the families Moniliformidae and Gigantorhynchidae.

Type
Research Paper
Copyright
Copyright © The Author(s) 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amin, OM and Dailey, MD (1998) Description of Mediorhynchus papillosus (Acanthocephala: Gigantorhynchidae) from a Colorado, U.S.A., population, with a discussion of morphology and geographical variability. Journal of the Helminthological Society of Washington 65, 189200.Google Scholar
Amin, OM and Heckmann, RA (2017) Neoandracantha peruensis n. gen. n. sp. (Acanthocephala: Polymorphidae) described from cystacanths infecting the ghost crab Ocypode gaudichaudi on the Peruvian coast. Parasite 24, 115.CrossRefGoogle Scholar
Amin, OM, Heckmann, RA and Zargar, UR (2017) Description of a new quadrigyrid acanthocephalan from Kashmir, with notes on metal analysis and histology, and a key to species of the subgenus Acanthosentis from the Indian subcontinent. Journal of Parasitology 103, 458470.CrossRefGoogle Scholar
Amin, OM, Heckmann, RA and Ha, NV (2018) Descriptions of Acanthocephalus parallelcementglandatus (Echinorhynchidae) and Neoechinorhynchus (N.) pennahia (Neoechinorhynchidae) (Acanthocephala) from amphibians and fish in Central and Pacific coast of Vietnam, with notes on N. (N.) longnucleatus. Acta Parasitologica 63, 572585.CrossRefGoogle Scholar
Amin, OM, Heckmann, RA, Radwan, NA, et al. (2009) Redescription of Rhadinorhynchus ornatus (Acanthocephala: Rhadinorhynchidae) from skipjack tuna, Katsuwonus pelamis, collected in the Pacific Ocean off South America, with special reference to new morphological features. Journal of Parasitology 95, 656664.CrossRefGoogle ScholarPubMed
Amin, OM, Heckmann, RA, Halajian, A, et al. (2011) The morphology of an unique population of Corynosoma strumosum (Acanthocephala, Polymorphidae) from the Caspian seal, Pusa caspica, in the land-locked Caspian Sea using SEM, with special notes on histopathology. Acta Parasitologica 56, 438445.CrossRefGoogle Scholar
Amin, OM, Evans, P, Heckmann, RA, et al. (2013) The description of Mediorhynchus africanus n. sp. (Acanthocephala: Gigantorhynchidae) from galliform birds in Africa. Parasitology Research 112, 28972906.CrossRefGoogle ScholarPubMed
Amin, OM, Heckmann, RA, Osama, M, et al. (2016) Morphological and molecular descriptions of Moniliformis saudi sp. n. (Acanthocephala: Moniliformidae) from the desert hedgehog, Paraechinus aethiopicus (Ehrenberg) in Saudi Arabia, with a key to species and notes on histopathology. Folia Parasitologica 63, 014.CrossRefGoogle Scholar
Amin, OM, Heckmann, RA, Sharifdini, M, et al. (2019) Moniliformis cryptosaudi n. s (Acanthocephala: Moniliformidae) from the long-eared hedgehog Hemiechinus auratus (Gmelin) (Erinaceidae) in Iraq; a case of incipient cryptic speciation related to M. Saudi in Saudi Arabia. Acta Parasitologica 64, 195204.CrossRefGoogle Scholar
Bremser, JG (1811) Notitia collectionis insignis vermium intestinalium et exhortatio ad commercium litterarium, quo illa perficiatur, et scientiæ atque amatoribus reddatur communiter proficua. Naturæ scrutatoribus generatim, specialiter autem Enthelmintholigis dictata ad Administratione Registrare Cæsaræ Musei Historiæ Naturalis Viennensis, In: Cæsarea Musei Historiae Naturalis Vindobonensis, Vienna: 31 pp, (Nachricht von einer Beträchtlichen Sammlung thierischer Eingeweidewürmer, und Einladung zu einer literarischen Verbindung, um dieselve su vervolkommen, und sie für die Wissenschaft und die Liebhaber allgemein nützliche zu machen. An Naturforscher überhapt und an Enthelminthologen insbesondere bon der k. k. Naturalien kabinets-Direktion in Wien.Google Scholar
Byram, JE and Fisher, FM Jr (1973) The absorptive surface of Moniliformis dubius (Acanthocephala). 1. Fine structure. Tissue and Cell 5, 553579.CrossRefGoogle Scholar
Falla, AC, Brieva, C and Bloor, P (2015) Mitochondrial DNA diversity in the acanthocephalan Prosthenorchis elegans in Colombia based on cytochrome c oxidase I (COI) gene sequence. International Journal for Parasitology: Parasites and Wildlife 4, 401407.Google ScholarPubMed
García-Varela, M and de Leon, GP (2015) Advances in the classification of acanthocephalans: evolutionary history and evolution of the parasitism. pp. 182201in Parasite diversity and diversification: evolutionary ecology meets phylogenetics. Serge Morand, Boris R. Krasnov and Timothy J. Littlewood, (Eds), London,Cambridge, University Press, Cambridge.CrossRefGoogle Scholar
García-Varela, M and Nadler, SA (2005) Phylogenetic relationships of Palaeacanthocephala (Acanthocephala) inferred from SSU and LSU rDNA gene sequences. Journal of Parasitology 91, 14011409.CrossRefGoogle ScholarPubMed
García-Varela, M and Nadler, SA (2006) Phylogenetic relationships among Syndermata inferred from nuclear and mitochondrial gene sequences. Molecular Phylogenetics and Evolution 40, 6172.CrossRefGoogle ScholarPubMed
García-Varela, M, Pérez-Ponce de León, G, de la Torre, P, et al. (2000) Phylogenetic relationships of Acanthocephala based on analysis of 18S ribosomal RNA gene sequences. Molecular Phylogenetics and Evolution 50, 532540.CrossRefGoogle ScholarPubMed
García-Varela, M, Cummings, MP, Pérez-Ponce de León, G, et al. (2002) Phylogenetic analysis based on 18S ribosomal RNA gene sequences supports the existence of class Polyacanthocephala (Acanthocephala). Molecular Phylogenetics and Evolution 23, 288292.CrossRefGoogle Scholar
Gazi, M, Sultana, T, Min, GS, et al. (2012) The complete mitochondrial genome sequence of Oncicola luehei (Acanthocephala: Archiacanthocephala) and its phylogenetic position within Syndermata. Parasitology International 61, 307316.CrossRefGoogle ScholarPubMed
Golvan, YJ (1956) Acanthocéphales d'oiseaux. (Cinquième note). Les espèces du genre Oligacanthorhynchus Travassos 1915 (Archiacanthocephala-Oligacanthorhynchidae Meyer 1931) dans l'ancien monde. Bulletin de la Société Zoologique du France 81, 344353.Google Scholar
Ha, NV, Amin, OM, Ngo, HD, et al. (2018) Descriptions of acanthocephalans, Cathayacanthus spinitruncatus (Rhadinorhynchidae) male and Pararhadinorhynchus magnus n. sp. (Diplosentidae), from marine fish of Vietnam, with notes on Heterosentis holospinus (Arhythmacanthidae). Parasite 25, 35.Google Scholar
Heckmann, RA, Amin, OM, Halajian, A, et al. (2013a) The morphology and histopathology of Nephridiacanthus major (Acanthocephala: Oligacanthorhynchidae) from hedgehogs in Iran. Parasitology Research 112, 543548.CrossRefGoogle Scholar
Heckmann, RA, Amin, OM and El-Naggar, AM (2013b) Micropores of Acanthocephala, a scanning electron microscopy study. Scientia Parasitologica 14, 105113.Google Scholar
Kamimura, K, Yonemitsu, K, Maeda, K, et al. (2018) An unexpected case of a Japanese wild boar (Sus scrofa leucomystax) infected with the giant thorny-headed worm (Macracanthorhynchus hirudinaceus) on the mainland of Japan (Honshu). Parasitology Research 117, 23152322.CrossRefGoogle Scholar
Kostylev, NN (1916) Thorn-headed worms Acanthocephali (sic). pp. 46–79 in Ovyasnitl'nyï katalog Parazitnykh cherveï zoologicheskogo kabineta imperatorskoï voenno-meditsinskoï Akademii, Kholodkowski, N. A. and Kostylev, N. N. (Eds) Explanatory catalog of the parasitic worms of the zoological department of the Imperial Academy of Military Medicine. Section II. Part II. Petrograd.Google Scholar
Kostylev, NN (1918) On the excretory organs in Gigantorhynchus major Bremser. Izvestiya Rossiskii Akademiï Nauk 12(15), 16871689.Google Scholar
Lee, RE (1992) Scanning electron microscopy and X-ray microanalysis. Englewood Cliffs, New Jersey, Prentice Hall, p. 458.Google Scholar
Meyer, A (1931) Neue Acanthocephalen aus dem Berliner Museum. Bergründung eines neuen Acanthocephalen systems auf Grund einer Untersuchung der Berliner Sammlung. Zoologische Jahrbücher, Abteilung für Systematik, Ökologie und Geographie der Tiere 62, 53108.Google Scholar
Meyer, A (1933) Acanthocephala. Dr. H.G. Bronn's Klassen und Ordnungen des TierReichs. Akademische Verlagsgesellschaft, Leipzig 4, 333582.Google Scholar
Near, TJ, Garey, JR and Nadler, SA (1998) Phylogenetic relationships of the Acanthocephala inferred from 18S ribosomal DNA sequences. Molecular Phylogenetics and Evolution 10, 287298.CrossRefGoogle ScholarPubMed
Petrochenko, VI (1958) Acanthocephala of domestic and wild animals, vol. 2. Moscow, Russia, Isdatel'stvo Akademii Nauk SSSR (in Russian: English translation by Israel Program for Scientific Translations Ltd., Jerusalem, Israel, 1971, p. 478).Google Scholar
Porta, A (1908) Gli acantocefali dei mammiferi. Noto Preventiva, Archives de Parasitologie, Paris 12, 268282.Google Scholar
Telford, MJ and Holland, PW (1993) The phylogenetic affinities of the chaetognaths: a molecular analysis. Molecular Biology and Evolution 10, 660676.Google ScholarPubMed
Weber, M, Wey-Fabrizius, AR, Podsiadlowski, L, et al. (2013) Phylogenetic analyses of endoparasitic Acanthocephala based on mitochondrial genomes suggest secondary loss of sensory organs. Molecular Phylogenetics and Evolution 66, 182189.CrossRefGoogle ScholarPubMed
Westrumb, AHL (1821) De Helminthibus acanthocephalis. Commentatio historico-anatomica adnexo recensu animalium, in Museo Vindobonensi circa helminthes dissectorum, et singularum specierum harum in illis repertarum. p. 85. Hanoverae, Helwing.CrossRefGoogle Scholar
Whitfield, PJ (1979) The biology of parasitism: an introduction to the study of associating organisms. Baltimore, Maryland, University Park Press, p. 277.Google Scholar
Wright, RD and Lumsden, RD (1969) Ultrastructure of the tegumentary pore-canal system of the acanthocephalan Moniliformis dubius. Journal of Parasitology 55, 9931003.CrossRefGoogle Scholar