Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-28T01:01:33.492Z Has data issue: false hasContentIssue false
  • English
  • Français

Redescription and molecular analysis of Pallisentis (Pallisentis) nandai Sarkar, 1953 (Acanthocephala: Quadrigyridae) in India

Published online by Cambridge University Press:  28 January 2021

O.M. Amin Open the ORCID record for O.M. Amin [Opens in a new window] ,
R.A. Heckmann ,
A. Chaudhary ,
N.Y. Rubtsova  and
H.S. Singh
O.M. Amin*
Affiliation:
Institute of Parasitic Diseases, 11445 E. Via Linda 2-419, Scottsdale, AZ85259, USA
R.A. Heckmann
Affiliation:
Department of Biology, Brigham Young University, 1114 MLBM, Provo, UT84602, USA
A. Chaudhary
Affiliation:
Molecular Taxonomy Laboratory, Department of Zoology, Chaudhary Charan Singh University, Meerut, UP250004, India
N.Y. Rubtsova
Affiliation:
Institute of Parasitic Diseases, 11445 E. Via Linda 2-419, Scottsdale, AZ85259, USA
H.S. Singh
Affiliation:
Molecular Taxonomy Laboratory, Department of Zoology, Chaudhary Charan Singh University, Meerut, UP250004, India
*
Author for correspondence: O.M. Amin, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Pallisentis (Pallisentis) nandai Sarkar, 1953 is a freshwater fish parasite restricted to the Indian subcontinent in the Ganga River and its tributaries. It was described from the leaffish, Nandus nandus (Hamilton) from the Ganga River delta at Calcutta. We recovered variant specimens from the same host species from the Ganga near its headwaters at Bijnor about 1500 km away. Our specimens were clearly identifiable as P. nandai but varied considerably from those in the original description, especially in the size of proboscis hooks, receptacle and lemnisci. The original description was incomplete (missing line drawings of female trunk and reproductive system, male trunk, complete proboscis, hooks and hook roots) and inaccurate (proboscis, hooks, receptacle wall), and some measurements were lumped together for both sexes. We provide a complete description and include new morphological information including the first description of para-receptacle structure in the genus Pallisentis Van Cleave, 1928, scanning electron microscopy and microscope images, molecular analysis, and energy dispersive X-ray analysis (EDXA) of hooks and spines of our specimens for the first time. Additional details of proboscis hook roots, trunk spines, micropores and micropore distribution are described. The unique metal composition of hooks (EDXA) demonstrated a considerably high but variable level of sulphur and negligible level of calcium in collar and trunk spines and hook tips, but a higher level of sulphur and calcium at the hook basal arch than at the hook tip and edge. A comparison with the EDXA pattern of another species of Pallisentis, P. İndica Mital & Lal, 1976, were considerably different. The phylogenetic position of P. nandai within Eoacanthocephala was generated to assess the molecular characterization based on 18S and ITS1-5.8S-ITS2 ribosomal DNA sequences. Maximum likelihood and Bayesian inference analyses placed P. nandai in a clade with other Pallisentis species under the family Quadrigyridae. This is the first report based on molecular evidence for P. nandai.

Keywords

AcanthocephalaPallisentis nandaiIndiaredescriptionnew featuresmolecular profile
Type
Research Paper
Information
Journal of Helminthology , Volume 95 , 2021 , e3
Copyright
Copyright © The Author(s), 2021. 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

Ahmed, ATA (1981) Helminth infection in freshwater fishes of Bangladesh. Fish Pathology 15, 229–236.CrossRefGoogle Scholar
Alam, MN and Alam, J (2014) A comparative study of endoparasite infestation of Oreochromis niloticus (Linnaeus, 1758) in polluted and non-polluted water bodies of Bangladesh. International Journal of Fauna and Biological Studies 1, 4–9.Google Scholar
Amin, OM (2005) Occurrence of the subgenus Acanthosentis Verma & Datta, 1929 (Acanthocephala; Quadrigyridae) in Japan, with the description of Acanthogyrus (Acanthosentis) alternatspinus sp. n. and A. (A.) parareceptaclis sp. n. from Lake Biwa drainage fishes and a key to species of the subgenus. Systematic Parasitology 60, 125–137.CrossRefGoogle Scholar
Amin, OM (2013) Classification of the Acanthocephala. Folia Parasitologica 60, 273–305.CrossRefGoogle ScholarPubMed
Amin, OM (2019) Redescription of Rhadinorhynchus trachuri Harada, 1935 (Acanthocephala: Rhadinorhynchidae) from marine fish in Vietnam and California with a discussion of its zoogeography. Acta Parasitologica 65, 77–89.CrossRefGoogle ScholarPubMed
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 Washington 65, 189–200.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, 40.CrossRefGoogle Scholar
Amin, OM, Heckmann, RA, Ha, NV, Luc, PV and Doanh, PN (2000) Revision of the genus Pallisentis (Acanthocephala: Quadrigyridae) with the erection of three new subgenera, the description of Pallisentis (Brevitritospinus) vietnamensis subgen. et sp. n., a key to species of Pallisentis, and the description of a new quadrigyrid genus, Pararaosentis gen. n. Comparative Parasitology 67, 40–50.Google Scholar
Amin, OM, Saoud, MFA and Alkuwari, KSR (2002) Neoechinorhynchus qatarensis sp. n. (Acanthocephala: Neoechinorhynchidae) from the blue-barred flame parrot fish, Scarus gobban Forsskål, 1775, in Qatar waters of the Arabian Gulf. Parasitology International 51, 171–196.CrossRefGoogle Scholar
Amin, OM, Heckmann, RA and Standing, MD (2007) Structural-functional relationship of the para-receptacle structure in Acanthocephala. Comparative Parasitology 74, 383–387.CrossRefGoogle 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, 656–664.Google ScholarPubMed
Amin, OM, Ha, NV and Ngo, HD (2011a) First report of Neoechinorhynchus (Acanthocephala: Neoechinorhynchidae) from marine fish of the eastern seaboard of Vietnam, with the description of six species. Parasite 18, 21–34.CrossRefGoogle Scholar
Amin, OM, Heckmann, RA, Halajian, A and El-Naggar, AM (2011b) The morphology of a 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, 438–445.CrossRefGoogle Scholar
Amin, OM, Heckmann, RA and Zargar, UR (2017) Description of a new quadrigyrid acanthocephalan from Kashmir, with notes on metal analysis and histopathology, and a key to species of the subgenus Acanthosentis from the Indian subcontinent. Journal of Parasitology 103, 458–470.CrossRefGoogle Scholar
Amin, OM, Heckmann, RA, Ha, NV and Pham, DN (2018a) Revision of the genus Pallisentis (Acanthocephala: Quadrigyridae) with the erection of three new subgenera, the description of Pallisentis (Brevitritospinus) vietnamensis subgen. et sp. n., a key to species of Pallisentis, and the description of a new quadrigyrid genus, Pararaosentis gen. n. Comparative Parasitology 67, 40–50.Google Scholar
Amin, OM, Heckmann, RA and Ha, NV (2018b) 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, 572–585.CrossRefGoogle Scholar
Amin, OM, Chaudhary, A, Heckmann, R, Ha, NV and Singh, HS (2019a) Redescription and molecular analysis of Neoechinorhynchus (Neoechinorhynchus) johnii Yamaguti, 1939 (Acanthocephala: Neoechinorhynchidae) from the Pacific Ocean off Vietnam. Parasite 26, 43.CrossRefGoogle Scholar
Amin, OM, Chaudhary, A, Heckmann, R, Ha, NV and Singh, HS (2019b) 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, 779–796.CrossRefGoogle Scholar
Amin, OM, Sharifdini, M, Heckmann, RA and Ha, NV (2019c) 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, 606–618.CrossRefGoogle Scholar
Amin, OM, Heckmann, RA, Sharifdini, M and Albayati, NY (2019d) 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, 195–204.CrossRefGoogle Scholar
Anonymous (2019) Nandus nandus was reported from 11 countries/islands. Available at https://www.fishbase.se/Country/CountryList.php?ID=10260&GenusName=Nandus&SpeciesName=nandus (accessed 12/2019).Google Scholar
Bhattacharya, SB (2007) Handbook on Indian Acanthocephala. 255 pp. Kolkata, India, Zoological Survey of India.Google Scholar
Bhuiyan, AL (1964) Fishes of Dacca. Publ. No. 13, 107–108 pp. Dacca, Asiatic Society of Pakistan.Google Scholar
Byram, JE and Fisher, FM Jr (1973) The absorptive surface of Moniliformis dubius (Acanthocephala). 1. Fine structure. Tissue and Cell 5, 553–579.CrossRefGoogle Scholar
Chaudhary, A, Amin, OM and Singh, HS (2019) Molecular characterization and phylogenetic relationships of Pallisentis (Brevitritospinus) indica (Acanthocephala: Quadrigyridae), a parasite of the spotted snakehead (Channa punctatus). Journal of Parasitology 105, 180–185.CrossRefGoogle Scholar
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) jmodeltest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772–772.CrossRefGoogle ScholarPubMed
Galazzo, D, Dayanandan, S, Marcogliese, DJ and McLaughlin, JD (2002) Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNA sequence data and comparisons with European congeners. Canadian Journal of Zoology 80, 2207–2217.CrossRefGoogle Scholar
García-Varela, M, Mendoza-Garfias, B, Choudhury, A and Pérez-Ponce de León, G (2017) Morphological and molecular data for a new species of Pomphorhynchus Monticelli, 1905 (Acanthocephala: Pomphorhynchidae) in the Mexican redhorse Moxostoma austrinum Bean (Cypriniformes: Catostomidae) in central Mexico. Systematic Parasitology 94, 989–1006.CrossRefGoogle Scholar
García-Varela, M, Park, JK, Hernández-Orts, JS and Pinacho-Pinacho, CD (2019) Morphological and molecular data on a new species of Plagiorhynchus Lühe, 1911 (Acanthocephala: Plagiorhynchidae) from the long-billed curlew (Numenius americanus) from northern Mexico. Journal of Helminthology 94, e61.CrossRefGoogle ScholarPubMed
Gautam, NK, Upadhyay, MK, Maurya, R, Verma, SK and Saxena, AM (2017) Molecular and morphological study of a new species Pallisentis anandai n. sp. (Quadrigyridae, Van Cleave, 1920) of Channa punctatus. Trends in Biosciences 10, 1540–1543.Google Scholar
Gautam, NK, Misra, PK and Saxena, AM (2019) Four New Species of the Genus Pallisentis (Quadrigyridae, Van Cleave, 1920) from Freshwater Fish in Uttar Pradesh, India. Acta Parasitologica 64, 71–85.CrossRefGoogle Scholar
Gautam, NK, Misra, PK, Saxena, AM and Monks, S (2020) Description of Pallisentis thapari n. sp. and a re-description of Acanthosentis seenghalae (Acanthocephala, Quadrigyridae, Pallisentinae) using morphological and molecular data, with analysis on the validity of the sub-genera of Pallisentis. Zootaxa 4766, 139–156.CrossRefGoogle Scholar
Gupta, N, Gupta, DK and Singhal, P (2015a) Description of Pallisentis (Brevitritospinus) punctati n. sp. (Acanthocephala: Quadrigyridae) from Channa punctatus in Bareilly, Uttar Pradesh, India. Iranian Journal of Parasitology 10, 605–616.Google Scholar
Gupta, R, Maurya, R and Saxena, AM (2015b) Two new species of the genus Pallisentis Van Cleave, 1928 (Acanthocephala: Quadrigyridae) from the intestine of Channa punctatus (Bloch, 1793) from the River Gomti at Lucknow, India. Iranian Journal of Parasitology 10, 116–121.Google Scholar
Ha, NV, Amin, OM, Ngo, HD and Heckmann, RA (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 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, 388–391.CrossRefGoogle Scholar
Heckmann, RA, Amin, OM, Radwan, NAE, Standing, MD, Eggett, DL and El Naggar, AM (2012) Fine structure and energy dispersive X-ray analysis (EDXA) of the proboscis hooks of Radinorynchus ornatus, Van Cleave 1918 (Rhadinorynchidae: Acanthocephala). Scientia Parasitologica 13, 37–43.Google Scholar
Heckmann, RA, Amin, OM and El-Naggar, AM (2013) Micropores of Acanthocephala, a scanning electron microscopy study. Scientia Parasitologica 14, 105–113.Google Scholar
Hossain, MA, Parween, S and Rahman, MA (1992) Food and feeding habit of Nandus nandus (Hamilton-Buchanan). The Rajshahi University Studies (Part-B) 20, 279–286.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for Bigger Datasets. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle ScholarPubMed
Lee, RE (1992) Scanning electron microscopy and X-ray microanalysis. 458 pp. Englewood Cliffs, New Jersey, Prentice Hall.Google Scholar
Li, L, Chen, HX and Yang, Y (2018) Morphological and molecular study of Neorhadinorhynchus nudus (Harada, 1938) (Acanthocephala: Cavisomidae) from Auxis thazard Lacepede (Perciformes: Scombridae) in the South China Sea. Acta Parasitologica 63, 479–485.CrossRefGoogle Scholar
Lisitsyna, OI, Kudlai, O, Cribb, TH and Smit, NJ (2019) Three new species of acanthocephalans (Palaeacanthocephala) from marine fishes collected off the East Coast of South Africa. Folia Parasitologica 66, 012.CrossRefGoogle Scholar
Littlewood, DTJ and Olson, PD (2001) Small subunit rDNA and the phylum Platyhelminthes: signal, noise, conflict and compromise. pp. 262–278 in Littlewood, DTJ and Bray, RA (Eds) Interrelationships of the Platyhelminthes. London, UK, Taylor and Francis.Google Scholar
Luton, K, Walker, D and Blair, D (1992) Comparison of ribosomal internal transcribed spacers from two congeneric species of flukes (Platyhelminthes: Trematoda: Digenea). Molecular and Biochemical Parasitology 56, 323–328.Google Scholar
Menasria, A, Barčák, D, Kaouachi, N, Bensouilah, M, Scholz, T and Hernández-Orts, JS (2019) Redescription of Acanthogyrus (Acanthosentis) maroccanus (Dollfus, 1951) (Acanthocephala: Quadrigyridae), a parasite of the Algerian barb Luciobarbus callensis (Valenciennes) (Cyprinidae) in Algeria, and first molecular data. Journal of Helminthology 94, e82.CrossRefGoogle ScholarPubMed
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, 126–127.CrossRefGoogle Scholar
Mital R, P and Lal, SS (1976) Two new acanthocephalan worms Pallisentis croftoni sp. nov. and P. indica sp. nov. (Family-Pallisentidae) from fresh-water fishes of the genus Ophicephalus. Indian Journal of Zootomy 17, 169–175.Google Scholar
Naidu, KV (2012) Fauna of India and adjacent countries-Acanthocephala. 638 pp. Kolkata, India, Zoological Survey of India.Google Scholar
Parveen, S and Sultana, S (2014) Infestation of helminth parasites in Gangetic leaffish Nandus nandus (Hamilton, 1822). Bangladesh Journal of Zoology 42, 183–190.CrossRefGoogle Scholar
Pichelin, S and Cribb, TH (2001) The status of the Diplosentidae (Acanthocephala: Palaeacanthocephala) and a new family of acanthocephalans from Australian wrasses (Pisces: Labridae). Folia Parasitologica 48, 289–303.CrossRefGoogle Scholar
Pinacho-Pinacho, CD, García-Varela, M, Sereno-Uribe, AL and de León, GPP (2018) A hyper-diverse genus of acanthocephalans revealed by tree-based and non-tree-based species delimitation methods: ten cryptic species of Neoechinorhynchus in Middle American. Molecular Phylogenetics and Evolution 127, 30–45.Google ScholarPubMed
Rainboth, WJ (1996) Fishes of the Cambodian Mekong. 265 pp. FAO species identification field guide for fishery purposes, FAO, Rome.Google Scholar
Sarkar, HL (1953) On a new Acanthocephala, Pallisentis nandai, from the fish Nandus nandus (Hamilton), with notes on other species of the genus. Proceedings of the Zoological Society of Bengal 6, 139–147.Google Scholar
Sharifdini, M, Amin, OM and Heckmann, RA (2020) The molecular profile of Paratrajectura longcementglandatus Amin, Heckmann Et Ali, 2018 (Acanthocephala: Transvenidae) from percid fishes in the marine waters of Iran and Iraq. Helminthologia 57, 1–11.CrossRefGoogle ScholarPubMed
Soota, TD and Bhattacharya, SB (1982) On the validity of the species of Pallisentis Van Cleave, 1928 (Acanthocephala: Pallisentidae) from the Indian Subcontinent. Records of the Zoological Survey of India 80, 157–167.Google 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. Poster. Submission number 0383–00501.CrossRefGoogle Scholar
Tadros, G (1966) On three new Acanthocephala of the genera Pallisentis Van Cleave, Saccosentis gen. nov. and Acanthocephalus koelreuther, from fish. Journal of Helminthology 40, 155–180.Google Scholar
Thompson, JD, Higgins, DG and Gibson, TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
Whitfield, PJ (1979) The biology of parasitism: an introduction to the study of associating organisms. 277 pp. Baltimore, Maryland, University Park Press.Google Scholar
Wongkham, W and Whitfield, PJ (1999) Pallisentis rexus n. sp. (Eocanthocephala: Quadrigyridae) from snakehead fish, Channa striata Bloch, from Chiang Mai Basin. Thailand. Thai Journal of Agricultural Sciences 32, 241–261.Google Scholar
Wright, RD and Lumsden, RD (1969) Ultrastructure of the tegumentary pore-canal system of the acanthocephalan Moniliformis dubius. Journal of Parasitology 55, 993–1003.CrossRefGoogle Scholar