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New perspectives of Microsentis wardae Martin & Multani, 1966 (Acanthocephala: Neoechinorhynchidae) from Gillichthys mirabilis Cooper in California, with scanning electron microscopy images and energy dispersive X-ray analysis

Published online by Cambridge University Press:  21 June 2022

O. M. Amin*
Affiliation:
Institute of Parasitic Diseases, 11445 E. Via Linda 2-419, Scottsdale, Arizona 85259, USA
A. Chaudhary
Affiliation:
Molecular Taxonomy Laboratory, Department of Zoology, Chaudhary Charan Singh University, Meerut, Uttar Pradesh, 250004, India
H. S. Singh
Affiliation:
Molecular Taxonomy Laboratory, Department of Zoology, Chaudhary Charan Singh University, Meerut, Uttar Pradesh, 250004, India Vice Chancellor, Maa Shakumbhari University, Saharanpur, Uttar Pradesh, 247120, India
*
Author for correspondence: O.M. Amin, E-mail: [email protected]

Abstract

Fully developed, sexually mature small male and female acanthocephalans, Microsentis wardae Martin & Multani, 1966 (Neoechinorhynchidae) reaching only 2.25 mm and 2.42 mm, respectively, were collected from the rectum of longjaw mudsuckers, Gillichthys mirabilis Cooper, in the salty marches of Anaheim Bay and San Diego Bay, California. Our specimens were half the size of those reported in the original description from the same host in Scammon's Lagoon over 700 km to the south. The ratio of proboscis and receptacle size to trunk size was markedly higher in our specimens compared to the larger specimens measured in the original description. The anatomy of all structures in our specimens from Anaheim Bay was comparable to that of the larger Scammon's Lagoon specimens that have apparently realized more growth in the Scammon's Lagoon. We have observed more structures that are not reported in the original description, especially evident from our scanning electron microscopy images, which are not possible to observe in the original line drawings. In our specimens, the micropores were unusually widely spaced and the energy dispersive X-ray analysis showed longitudinal hook sections with high levels of sulphur and phosphorus and moderate levels of calcium, but the whole hooks showed highest levels of sodium and magnesium – the biochemical hook signature of this species. Sequences of the small subunit (18S) of the nuclear ribosomal DNA were generated and compared with acanthocephalan sequences available from GenBank. As M. wardae comprises a monotypic genus, therefore, phylogenetic analyses inferred from the 18S gene showed its relationship with other species of closely related genera of Eoacanthocephala. This is the first report of molecular data of M. wardae.

Type
Research Paper
Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Amin, OM (1986) Acanthocephala from lake fishes in Wisconsin: Morphometric growth of Neoechinorhynchus cylindratus (Neoechinorhynchidae) and taxonomic implications. Transactions of the American Microscopical Society 105(4), 375380.10.2307/3226524CrossRefGoogle Scholar
Amin, OM (2013) Classification of the acanthocephala. Folia Parasitol 60(4), 273305.10.14411/fp.2013.031CrossRefGoogle Scholar
Amin, OM and Bullock, WL (1998) Neoechinorhynchus rostratum sp. n. (Acanthocephala: Neoechinorhynchidae) from the eel, Anguilla rostrata, in estuarine waters of northeastern North America. Journal of the Helminthological Society of Washington 65(2), 169173.Google Scholar
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 Helminthological Society of Washington 65(2), 189200.Google Scholar
Amin, OM and Heckmann, RA (1992) Description and pathology of Neoechinorhynchus idahoensis n. sp. (Acanthocephala: Neoechinorhynchidae) in Catostomus coumbianus from Idaho. Journal of Parasitology 78(1), 3439.10.2307/3283682CrossRefGoogle Scholar
Amin, OM and Redlin, MJ (1980) The effect of host species on growth and variability of Echinorhynchus salmonis Müller, 1784 (Acanthocephala: Echinorhynchidae), with special reference to the status of the genus. Systematic Parasitology 2(1), 920.10.1007/BF00015091CrossRefGoogle Scholar
Amin, OM, Heckmann, RA, Radwan, NA, Mantuano, JS and Alcivar, MAZ (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(3), 656664.10.1645/GE-1804.1CrossRefGoogle Scholar
Amin, OM, Heckmann, RA, Halajian, A and El-Naggar, AM (2011) The morphology of an [sic] 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(4), 438445.Google Scholar
Amin, OM, Heckmann, RA and Bannai, MA (2018) Cavisoma magnum (Cavisomidae), a unique Pacific acanthocephalan redescribed from an unusual host, Mugil cephalus (Mugilidae), in the Arabian Gulf, with notes on histopathology and metal analysis. Parasite 25, 5.10.1051/parasite/2018006CrossRefGoogle Scholar
Amin, OM, Sharifdini, M, Heckmann, RA and Ha, NV (2019a) On three species of Neoechinorhynchus (Acanthocephala: Neoechinorhynchidae) from the Pacific Ocean off Vietnam with the molecular description of Neoechinorhynchus (N.) dimorphospinus Amin and Sey, 1996. Journal of Parasitology 105(4), 606618.10.1645/19-29CrossRefGoogle Scholar
Amin, OM, Heckmann, RA, Sharifdini, M and Albayati, NY (2019b) Moniliformis cryptosaudi n. sp. (Acanthocephala: Moniliformidae) from the Long-eared Hedgehog Hemiechinus auritus (Gmelin) (Erinaceidae) in Iraq; A Case of Incipient Cryptic Speciation Related to M. saudi in Saudi Arabia. Acta Parasitologica 64(1), 195204.10.2478/s11686-018-00021-9CrossRefGoogle Scholar
Amin, OM, Chaudhary, A, Heckmann, RA, Ha, NV and Singh, HS (2019c) The morphological and molecular description of Acanthogyrus (Acanthosentis) fusiformis n. sp. (Acanthocephala: Quadrigyridae) from the catfish Arius sp. (Ariidae) in the Pacific Ocean off Vietnam, with notes on zoogeography. Acta Parasitologica 64(4), 779796.10.2478/s11686-019-00102-3CrossRefGoogle Scholar
Amin, OM, Sharifdini, M, Heckmann, RA, Rubtsova, N and Chine, HJ (2020) On the Neoechinorhynchus agilis (Acanthocephala: Neoechinorhynchidae) complex, with the description of Neoechinorhynchus ponticus n. sp. from Chelon auratus Risso in the Black Sea. Parasite 27, 48.10.1051/parasite/2020044CrossRefGoogle Scholar
Amin, OM, Heckmann, RA, Chaudhary, A, Rubtsova, NY and Singh, HS (2021) Redescription and molecular analysis of Pallisentis (Pallisentis) nandai Sarkar, 1953 (Acanthocephala: Quadrigyridae) in India. Journal of Helminthology 95, e3.10.1017/S0022149X20001005CrossRefGoogle ScholarPubMed
Anonymous (2009) Sedimentology and Oceanography of Coastal Lagoons in Baja California, Mexico—Geological Society of America Bulletin. Available at gsabulletin.gsapubs.org (accessed 1 November 2009).Google Scholar
Byram, JE and Fisher, FM Jr (1973) The absorptive surface of Moniliformis dubius (Acanthocephala). 1. Fine structure. Tissue and Cell 5(4), 553579.10.1016/S0040-8166(73)80045-XCrossRefGoogle Scholar
Eschmeyer, WN, Herald, ES and Hamann, H (1983) A field guide to pacific coast fishes of North America. Peterson field guide series. Boston, MA, Houghton Mifflin Co.Google Scholar
García-Prieto, L, García-Varela, M, Mendoza-Garfias, B and Pérez-Ponce de León, G (2010) Checklist of the Acanthocephala in wildlife vertebrates of Mexico. Zootaxa 2419, 150.10.11646/zootaxa.2419.1.1CrossRefGoogle 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(6), 14011409.10.1645/GE-523R.1CrossRefGoogle Scholar
García-Varela, M, Pérez-Ponce de León, G, de la Torre, P, Cummings, MP, Sarma, SS and Laclette, JP (2000) Phylogenetic relationships of Acanthocephala based on analysis of 18S ribosomal RNA gene sequences. Journal of Molecular Evolution 50(6), 532540.10.1007/s002390010056CrossRefGoogle Scholar
García, E (2018) Genomic analysis of disjunct marine fish populations of the northeastern Pacific and Sea of Cortez. Thesis, UC Santa CruzGoogle Scholar
Heckmann, RA, Amin, OM and Standing, MD (2007) Chemical analysis of metals in acanthocephalans using energy dispersive X-ray analysis (EDXA, XEDS) in conjunction with a scanning electron microscope (SEM). Comparative Parasitology 74(2), 388391.10.1654/4258.1CrossRefGoogle Scholar
Heckmann, RA, Amin, OM, Radwan, NAE, Standing, MD and Eggett, DL (2012a) Comparative chemical element analysis using energy dispersive x-ray microanalysis (EDXA) for four species of Acanthocephala. Scientia Parasitologica 13, 2735.Google Scholar
Heckmann, RA, Amin, OM, Radwan, NAE, Standing, MD, Eggett, DL and El Naggar, AM (2012b) Fine structure and energy dispersive X-ray analysis (EDXA) of the proboscis hooks of Radinorynchus ornatus, Van Cleave 1918 (Rhadinorynchidae: Acanthocephala). Scientia Parasitologica 13(1), 3743.Google Scholar
Heckmann, RA, Amin, OM and El Naggar, AM (2013) Micropores of Acanthocephala, a scanning electron microscopy study. Scientia Parasitologica 14(3), 105113.Google Scholar
Kamimura, K, Yonemitsu, K, Maeda, K, Sakaguchi, S, Setsuda, A, Varcasia, A and Sato, H (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(7), 23152322.10.1007/s00436-018-5922-7CrossRefGoogle Scholar
Lee, R (1992) Scanning electron microscopy and X-ray microanalysis. Englewood Cliffs, New Jersey, Prentice Hall, p. 464.Google Scholar
Malyarchuk, B, Derenko, M, Mikhailova, E and Denisova, G (2014) Phylogenetic relationships among Neoechinorhynchus species (Acanthocephala: Neoechinorhynchidae) from North-East Asia based on molecular data. Parasitology International 63(1), 100107.10.1016/j.parint.2013.09.012CrossRefGoogle Scholar
Martin, WE and Multani, S (1966) Microsentis wardae n. g., n. sp. (Acanthocephala) in the marine fish Gillichthys mirabilis Cooper. Transactions of the American Microscopical Society 85(4), 536540.10.2307/3224478CrossRefGoogle Scholar
Martin, WE and Multani, S (1970) Some helminths of the mudsucker fish, Gillichthys mirabilis Cooper. Bulletin of the Society of the California Academy of Sciences 69(1), 161168.Google Scholar
Milne, I, Lindner, D, Bayer, M, Husmeier, D, Mcguire, G, Marshall, DF and Wright, F (2009) TOPALiv2: A rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics 25(1), 126127.10.1093/bioinformatics/btn575CrossRefGoogle 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(3), 287298.10.1006/mpev.1998.0569CrossRefGoogle Scholar
Phleger, FB and Clifford, CE (2009) Ewing. “Protected Areas Programme - Whale Sanctuary of El Vizcaino”. Available at www.unep-wcmc.org (accessed 1 November 2009).Google Scholar
Posada, D (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25(7), 12531256.10.1093/molbev/msn083CrossRefGoogle Scholar
Rubtsova, NY and Heckmann, RA (2019) Structure and morphometrics of Ancyrocephalus paradoxus (Monogenea: Ancyrocephalidae) from Sander lucioperca (Percidae) in Czechia. Helminthologia 56(1), 1121.10.2478/helm-2018-0037CrossRefGoogle Scholar
Rubtsova, NY and Heckmann, RA (2020) Morphological features and structural analysis of plerocercoids of Spirometra erinaceieuropaei (Cestoda: Diphyllobothriidae) from European pine marten, Martes martes (Mammalia: Mustelidae) in Ukraine. Comparative Parasitology 87(1), 109117.10.1654/1525-2647-87.1.109CrossRefGoogle Scholar
Rubtsova, NY, Heckmann, RA, Smit, WS, Luus-Powell, WJ, Halajian, A and Roux, F (2018) Morphological studies of developmental stages of Oculotrema hippopotami (Monogenea: Polystomatidae) infecting the eye of Hippopotamus amphibius (Mammalia: Hippopotamidae) using SEM and EDXA with notes on histopathology. Korean Journal of Parasitology 56(5), 463475.10.3347/kjp.2018.56.5.463CrossRefGoogle Scholar
Sharifdini, M, Amin, OM and Heckmann, RA (2021) The molecular profile of Acanthogyrus (Acanthosentis) kashmirensis from the Indian subcontinent. Acta Parasitologica 66(3), 863870.10.1007/s11686-020-00331-xCrossRefGoogle Scholar
Standing, MD and Heckmann, RA (2014) Features of Acanthocephalan hooks using dual beam preparation and XEDS phase maps. Microscopy and Microanalysis Meeting, Hartford, Connecticut, USA, No 0383–00501.10.1017/S143192761400837XCrossRefGoogle Scholar
Stegman, JK (2005) Stedman's Medical Dictionary for health professions and Nursing. 5th Edition. Baltimore, Maryland, USA, Lippincott, Williams and Wilkins.Google Scholar
Suzuki, N, Hoshino, K, Murakami, K, Takeyama, H and Chow, S (2008) Molecular diet analysis of Phyllosoma larvae of the Japanese spiny lobster Palinurus japonicas (Decapoda: Crustacea). Marine Biotechnology 10(1), 4955.10.1007/s10126-007-9038-9CrossRefGoogle Scholar
Tamura, K, Stecher, G and Kumar, S (2021) MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution 38(7), 30223027.10.1093/molbev/msab120CrossRefGoogle Scholar
Thompson, JD, Gibson, TJ, Plewniak, F, Jeanmougin, F and Higgins, DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25(24), 48764882.10.1093/nar/25.24.4876CrossRefGoogle 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(5), 9931003.10.2307/3277165CrossRefGoogle Scholar