Skip to main content
SpringerLink
Log in

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

  • Original Paper
  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

Background

Most (82%) of the 46 recognized species of Acanthogyrus (Acanthosentis) Verma and Datta, 1929 are known from Asian freshwater fishes. Only three species of Acanthosentis are known from marine or brackish water fishes from India and Pakistan. We have discovered another marine species of Acanthosentis in the Pacific Ocean, off Vietnam.

Purpose

The purpose is to describe the new species morphologically and molecularly and provide new information of its evolutionally relationships with other species of the subgenus.

Methods

Standard methods of collection and examination of marine hosts, processing and illustrating of specimens, and taxonomic identification of parasites using the extensive collection of the lead author were used. Specimens were further studied using energy-dispersive X-ray analysis and ion sectioning of hooks, SEM analysis, and molecular sequencing. Type specimens were deposited at the Harold W. Manter Lab. collection, Lincoln, Nebraska.

Results

Acanthogyrus (Acanthosentis) fusiformis n. sp. is described from the catfish, Arius sp. (Ariidae: Siluriformes) off the Pacific Coast of Vietnam at Bac Lieu in the Gulf of Thailand. The three other marine Indian species include A. (A.) arii Bilqees, 1971 which is also described from a similar catfish, Arius serratus Day off the Karachi coast in the Arabian Sea, Indian Ocean. Our new species from Vietnam is distinguished from the other 46 species by a combination of characters including a small fusiform trunk, complete circles of small hollow spines covering the entire trunk, prominent double apical organs often extending posteriorly past posterior hooks, middle and posterior hooks of equal size slightly smaller than anterior hooks, large neck continuous with the outline of the proboscis without distinct separation, big drop-shaped cephalic ganglion, extension of the proboscis receptacle anteriorly past the base of the proboscis up to the insertion point of the posterior hooks, presence of two para-receptacle structures (PRSs), free unattached thick lemnisci, short female reproductive system with filamentous attachment of the distal end of the uterine bell to the ventral body wall, and small narrowly ellipsoid eggs with thickened polar ends. Partial sequences of the 18S and internal transcribed spacers (ITS1-5.8S-ITS2) of ribosomal RNA were generated and used for phylogenetic analyses to confirm the taxonomic identity of Acanthogyrus (Acanthosentis) fusiformis n. sp.

Conclusions

We describe unique morphological features of A. fusiformis never before known in the subgenus Acanthosentis. The uniqueness of A. fusiformis is further demonstrated by its EDXA fingerprint characterized by high levels of calcium and phosphorous in hooks. The zoogeography of species of Acanthosentis is elucidated in the Indian subcontinent, the Caribbean, China, and Africa. Molecular data have been available only in few species of Acanthogyrus (Acanthosentis) to date on GenBank database. For 18S, only two sequences from unknown Acanthosentis sp. from India are available, while for the ITS1-5.8S-ITS2 region, only sequences of A. cheni from China and of two unidentified species from Malaysia are available. Additional studies of species of Acanthosentis based on morphological and molecular genetic data will be needed to reconstruct the evolutionary history and phylogenetic affinities of this group of acanthocephalans.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figs. 1–6
Figs. 7–11
Figs. 12–17
Figs. 18–23
Figs. 24–29
Fig. 30
Fig. 31
Fig. 32

Similar content being viewed by others

References

  1. Agrawal N, Singh HS (1982) A new acanthocephalan from a freshwater fish of the Gorakhpur district (India). J Adv Zool 3:85–87

    Google Scholar 

  2. Amin OM (1985) Classification. In: Crompton DWT, Nickol BB (eds) Biology of the Acanthocephala. Cambridge University Press, London, pp 27–72

    Google Scholar 

  3. Amin OM (2005) Occurrence of the subgenus Acanthosentis Verma & Datta, 1929 (Acanthocephala: Quadrigyridae) in Japan, with the description of Acanthogyrus (Acanthosentis) alternatspinus n. sp. and A. (A.) parareceptaclis n. sp. from Lake Biwa drainage fishes and a key to the species of the subgenus. Syst Parasitol 60:125–137. https://doi.org/10.1007/s11230-004-1386-5

    Article  PubMed  Google Scholar 

  4. Amin OM (2013) Classification of the Acanthocephala. Folia Parasitol 60:273–305

    Article  Google Scholar 

  5. Amin OM, Ha NV, Ngo HD (2011) First report of Neoechinorhynchus (Acanthocephala: Neoechinorhynchidae) from marine fish (Belonidae, Clupeidae, Megalopidae, Mugilidae, Sciaenidae) in Vietnamese waters, with the description of six new species with unique anatomical structures. Parasite 18:21–34. https://doi.org/10.1051/parasite/2011181021

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Amin OM, Heckmann RA, Dallarés S, Constenla M, Ha NV (2019) Morphological and molecular description of Rhadinorhynchus laterospinosus Amin, Heckmann, Ha. 2011 (Acanthocephala: Rhadinorhynchidae) from marine fish off the Pacific coast of Vietnam. Parasite 26:14. https://doi.org/10.1051/parasite/2019015

    Article  PubMed  PubMed Central  Google Scholar 

  7. Amin OM, Heckmann RA, Halajian A, El-Naggar AM (2011) The morphology of an unique population of Corynosoma strumosum (Acanthocephala, Polymorphidae) from the Caspian seal, Pusacaspica, in the land-locked Caspian Sea using SEM, with special notes on Histopathology. Acta Parasitol 56:438–445. https://doi.org/10.2478/s11686-011-0070-6

    Article  Google Scholar 

  8. Amin OM, Heckmann RA, Radwan NA, Mantuano JS, 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. J Parasitol 95:656–664. https://doi.org/10.1645/GE-1804.1

    Article  PubMed  Google Scholar 

  9. Amin OM, Heckmann RA, Sharifdini M, Albayati NY (2019) Moniliformis cryptosaudi n. sp., (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 Parasitol 64:195–204. https://doi.org/10.2478/s11686-018-00021-9

    Article  PubMed  Google Scholar 

  10. Amin OM, Heckmann RA, Standing MD (2007) Structural-functional relationship of the para-receptacle structure in Acanthocephala. Comp Parasitol 74:383–387. https://doi.org/10.1654/4257.1

    Article  Google Scholar 

  11. Amin OM, Heckmann RA, 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. J Parasitol 103:458–470. https://doi.org/10.1645/17-27

    Article  PubMed  Google Scholar 

  12. Amin OM, Hendrix SS (1999) Acanthocephala of cichlids (Pisces) in Lake Malawi, Africa with a description of Acanthogyrus (Acanthosentis) malawiensis sp.n. (Quadrigyridae) from Labeo cylindricus Peters, 1852 (Cyprinidae). J Helminthol Soc Wash 66:47–55

    Google Scholar 

  13. Amin OM, Saoud MFA, 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. Parasitol Int 51:171–196

    Article  PubMed  Google Scholar 

  14. Anantaraman S (1980) Acanthosentis oligospinus n. sp. an acanthocephalan parasite of the brackish water fish Mystus (Macroneux) guliox in Madras. Indian J Parasitol 4:21–24

    Google Scholar 

  15. Bilqees FM (1971) Parasites of the cat fish Arius serratus. 1. Acanthocephala. Pak J Zool 3:57–65

    Google Scholar 

  16. Bilqees FM, Khan A (1987) Acanthocephala of fishes of Pakistan. Biological Bulletin of Pakistan. Monograph No. 13:1–28, Figs. 1–38

  17. Bullock WL (1970) The zoogeography and host relations of the eoacanthocephalan parasites of fishes. Symposium on Diseases of Fishes and Shellfishes. The American Fisheries Society, Bethesda, pp 161–173

    Google Scholar 

  18. Byram JE, Fisher FM Jr (1973) The absorptive surface of Moniliformis dubius (Acanthocephala). 1. Fine structure. Tissue Cell 5:553–579

    Article  CAS  PubMed  Google Scholar 

  19. Farooqi HU, Sirikanchana P (1987) Some acanthocephalan parasites of fishes in Thailand. Thai J Agric Sci 20:97–109

    Google Scholar 

  20. Furtado JI (1963) On Acanthogyrus partispinus nov. sp. (Quadrigyridae, Acanthocephala) from Malayan cyprinid, Hampala macrolepidota Van Hasselt. Z Parasitenkd 23:219–225

    Article  CAS  PubMed  Google Scholar 

  21. Galazzo DE, Dayanandan S, Marcogliese DJ, McLaughlin JD (2002) Molecular systematics of some North American species of Diplostomum (Digenea) based on rDNA-sequence data and comparisons with European congeners. Can J Zool 80:2207–2217. https://doi.org/10.1139/z02-198

    Article  CAS  Google Scholar 

  22. Golvan YJ (1994) Nomenclature of the Acanthocephala. Res Rev Parasitol 54:135–205

    Google Scholar 

  23. Golvan YJ (1959) Le Phylum des Acanthocephala. Deuxièmenote. La Classe de Eoacanthocephala (Van Cleave, 1936). Ann Parasitol Hum Comp 34:5–52

    Article  Google Scholar 

  24. Heckmann RA, Amin OM, El-Naggar AM (2013) Micropores of Acanthocephala, a scanning electron microscopy study. Sci Parasitol 14:105–113

    Google Scholar 

  25. Heckmann RA, Amin OM, Radwan NAE, Standing MD, Eggett DL, 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). Sci Parasitol 13:37–43

    Google Scholar 

  26. Heckmann RA, Amin OM, 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). Comp Parasitol 74:388–391. https://doi.org/10.1654/4258.1

    Article  Google Scholar 

  27. Kimura S, Nagata Y (1992) Scientific name of Nipponbaratanago, a Japanese bitterling of the genus Rhodeus. Jpn J Ichthyol 38:425–429. https://doi.org/10.11369/jji1950.38.425

    Article  Google Scholar 

  28. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Lee RE (1992) Scanning electron microscopy and X-ray microanalysis. Prentice Hall, Englewood Cliffs, p 458

    Google Scholar 

  30. Littlewood DTJ, Olson PD (2001) Small subunit rDNA and the phylum Platyhelminthes: signal, noise, conflict and compromise. In: Littlewood DTJ, Bray RA (eds) Interrelationships of the Platyhelminthes. Taylor Francis, London, pp 262–278

    Google Scholar 

  31. Marceniuk AP, Menezes NA (2007) Systematics of the family Ariidae (Ostariophysi, Siluriformes), with a redefinition of the genera. Zootaxa 1416:1–126

    Article  Google Scholar 

  32. Masuda H, Amaoka K, Araga C, Uyeno T, Yoshino T (1984) The fishes of the Japanese Archipelago, vol 1. Tokai University Press, Tokyo, p 437

    Google Scholar 

  33. Milne I, Lindner D, Bayer M, Husmeier D, McGuire G, Marshall DF, Wright F (2009) TOPALi v2: a rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics 25:126–127. https://doi.org/10.1093/bioinformatics/btn575

    Article  CAS  PubMed  Google Scholar 

  34. Pethiyagoda R (1991) Freshwater fishes of Sri Lanka. The Wildlife Heritage Trust of Sri Lanka, Colombo, p 362

    Google Scholar 

  35. Petrochenko VI (1956) Acanthocephala of domestic and wild animals, vol 1. Izdatelstvo Akademii Nauk SSSR, Moscow, p 435 (In Russian: English translation by Israel Program for Scientific Translations Ltd., Jerusalem, 1971, 465 pp.)

    Google Scholar 

  36. Rainboth WJ (1996) Fishes of the Cambodian Mekong. FAO species identification field guide for fishery purposes. FAO, Rome, p 265

    Google Scholar 

  37. Robins CR, Ray GC (1986) A field guide to Atlantic coastfishes of North America. Houghton Mifflin Company, Boston, p 354

    Google Scholar 

  38. Sen P (1938) On a new species of Acanthocephala Acanthosentis holospinus sp. nov. from the fish Barbus stigma (Cav. And Val.). Proc Indian Acad Sci, Bangalore 8:41–46

    Google Scholar 

  39. Standing MD, Heckmann RA (2014) Features of Acanthocephalan hooks using dual beam preparation and XEDS phase maps. Microscopy and Microanalysis Meeting: Hartford, CT. Poster. Submission Number 0383-00501

  40. Thapar GS (1927) On Acanthogyrus n.g. from the intestine of the Indian fish Labeo rohita, with a note on the classification of the Acanthocephala. J Helminthol 5:109–120. https://doi.org/10.1017/S0022149X00018678

    Article  Google Scholar 

  41. Thomson JM (1986) Mugilidae. In: Daget J, Gosse J, van Audenaerde DFET (eds) Check-list of the freshwater fishes of Africa (CLOFFA), vol 2. ISNB, Brussels, MRAC, Brussels, pp 344–349

    Google Scholar 

  42. Tripathi YR (1956) Studies on parasites of Indian fishes V. Acanthocephala. Rec Indian Mus 54:61–99

    Google Scholar 

  43. Verma SC, Datta MN (1929) Acanthocephala from Northern India, 1, A new genus Acanthosentis from a Calcutta fish. Ann Trop Med Parasit 23:483–500

    Article  Google Scholar 

  44. Whitehead PJP (1985) FAO species catalogue of the clupeoid fishes of the world. An annotated and illustrated catalogue of the herrings, sardines, pilchards, sprats, shads, anchovies and wolf-herrings. Part 1- Chirocentridae, Clupeidae and Pristigasteridae. FAO Fish Synopsis (125), vol 7, Pt 1, pp 303

  45. Whitehead PJP, Nelson GJ, Wongratana T (1988) FAO species catalogue of clupeoid fishes of the world (suborder Clupeoidei). An annotated and illustrated catalogue of the herrings, sardines, pilchards, sprats, shads, anchovies and wolf- herrings. Part 2-Engraulididae. FAO Fish Synopsis (125) vol 7, Pt 2, 579, pp 456

  46. Whitfield PJ (1979) The biology of parasitism: an introduction to the study of associating organisms. University Park Press, Baltimore, p 277

    Google Scholar 

  47. Wright RD, Lumsden RD (1969) Ultrastructure of the tegumentary pore-canal system of the acanthocephalan Moniliformis dubius. J Parasitol 55:993–1003

    Article  Google Scholar 

  48. Yamaguti S (1963) Systema helminthum, vol 5. Acanthocephala. Wiley Interscience, New York, p 423

    Google Scholar 

  49. Yuma M, Hosoya K, Nagata Y (1998) Distribution of freshwater fishes of Japan: an historical overview. Environ Biol Fishes 52:97–124

    Article  Google Scholar 

Download references

Acknowledgements

This project was supported by the Department of Biology, Brigham Young University (BYU), Provo, Utah, the Vietnam National Program No. 47 under Grant code VAST.DA47.12/16-19, and by an Institutional Grant from the Parasitology Center, Inc. (PCI), Scottsdale, Arizona. We thank Naomi Mortensen, Bean Museum (BYU) for preparation of the SEM plates. We would like to acknowledge the laboratory facilities provided by Department of Zoology, Chaudhary Charan Singh University, Meerut, India.

Author information

Authors and Affiliations

  1. Institute of Parasitic Diseases, 11445 E. Via Linda 2-419, Scottsdale, AZ, 85259, USA

    Omar M. Amin

  2. Molecular Taxonomy Laboratory, Department of Zoology, Chaudhary Charan Singh University, Meerut, UP, 250004, India

    Anshu Chaudhary & Hridaya S. Singh

  3. Department of Biology, Brigham Young University, 1114 MLBM, Provo, UT, 84602, USA

    Richard A. Heckmann

  4. Department of Parasitology, Institute of Ecology and Biological Resources (IEBR), Academy of Science and Technology, 18 Hoang Quoc Viet, CauGiay, Hanoi, Vietnam

    Nguyen V. Ha

Authors
  1. Omar M. Amin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anshu Chaudhary
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Richard A. Heckmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nguyen V. Ha
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hridaya S. Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Omar M. Amin.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest and compliance with all relevant ethical standards.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Amin, O.M., Chaudhary, A., Heckmann, R.A. et al. 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 Parasit. 64, 779–796 (2019). https://doi.org/10.2478/s11686-019-00102-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11686-019-00102-3

Keywords

Search

Navigation