Scanning Electron Microscopy of Acanthocephala Isolated from Saurida tumbil in Minab City, Hormozgan Province, South Coast of Iran

Document Type : Original Article

Authors

1 Department of Pathobiology, Faculty of Veterinary Medicine, Shahid Bahonar University of Kerman, Kerman, Iran

2 Department of Basic Sciences, Faculty of Veterinary Medicine, Shahid Bahonar University of Kerman, Kerman, Iran

Abstract

The Synodontidae family is a group of marine fish that includes four genera and 57 species and is distributed throughout all waters of the world. A total of 150 lizardfish (Saurida tumbil) were randomly sampled from various fish markets in Minab city, Hormozgan province, Iran, from June 2022 to May 2023. The fish were dissected, and their digestive tracts were examined for acanthocephalans. Taxonomic identification of the parasites was based on morphological characteristics described using a light microscope and then confirmed by Scanning Electron Microscope (SEM) to clarify ambiguous details. To prepare the parasites for observation using SEM, some samples were placed in 2.5% glutaraldehyde diluted with 0.1 M sodium cacodylate buffer for 2 to 4 hours at 4°C.  After primary fixation, washing was performed three times with 0.1 M sodium cacodylate buffer, each wash lasting 15 minutes. For secondary fixation, 1% osmium tetroxide was applied for two hours. Following a repeat of the washing steps, the dehydration stage was performed using ascending grades of alcohol, with each grade applied for 15 minutes. Finally, the samples were dehydrated and dried in a desiccator. The prepared samples were mounted on copper stubs, then coated with a 4 to 7 nm thick layer of gold using a sputter machine to enable imaging. The images were acquired using a Leo scanning electron microscope. The collected specimens exhibited characteristics typical of the genus. Parasite indices of prevalence, intensity, and mean abundance were evaluated for each parasite species. The discovered samples were identified morphologically as Neoechinorhynchus spp. and Quadrigyrus spp. from ten Saurida tumbil. This is the first report of Neoechinorhynchus and Quadrigyrus parasitizing Saurida tumbil.

Keywords


  1. Azari A, Shamsaie Mehrgan M, Tatina M, Rajabi Islami H. Effect of feeding with different levels of trisodium citrate on growth performance, immunocompetence triats, and digestive enzymes in goldfish (Carassius auratus). Iran J Fish Sci. 2021; 20 (4):1192–205.
  2. Kalhoro MA, Liu Q, Valinassab T, Waryani B, Abbasi AR, Memon KH. Population dynamics of greater lizardfish, Saurida tumbil from Pakistani waters. Pak J Zool. 2015; 47 (4):921–31.
  3. Zellibooriabadi M, Gorgin S, Fujimori Y, Zare P, Niri AS, Susanto A. Estimation of gillnets selectivity for greater lizardfish, Saurida tumbil (Bloch, 1795) in coastal waters of the Oman Sea:—. Int J Aquat Biol. 2023; 11 (3):230–41.
  4. Doustdar M, Hashemi SA, Rahmati R. The feeding and reproductive habits of Saurida tumbil and Rastrelliger kanagurata in the northern Oman Sea. Iran J Fish Sci. 2022; 21 (3):816–28.
  5. Jaziri AA, Shapawi R, Mokhtar RAM, Noordin WNM, Huda N. Physicochemical and microstructural analyses of pepsin-soluble collagens derived from lizardfish, Saurida tumbil skin, bone and scales. Gels. 2022; 8(8):471.
  6. Sakthivel A, Gopalakrishnan A. Prevalence and pathology manifestation of Acanthocephalus ranae infestation in finfishes of Tamil Nadu, southeast coast of India. World News Nat Sci. 2021; 33: 1–19.
  7. Abd El-Ghany AM, Nada MSM, Nadler SA. Morphological and molecular characterization of larval Echinocephalus sp. (Spirurida: gnathostomatidae), a parasite of the greater lizard fish (Saurida undosquamis) and red porgy or common seabream (Pagrus pagrus). Parasitol Res. 2023 Oct; 122 (10):2405–11.
  8. Buchmann K, Karami AM. Fish Acanthocephalans as Potential Human Pathogens. Curr Clin Microbiol Rep. 2024 Mar 15; 11 (2):99–106.
  9. Buchmann K, Karami AM. Fish acanthocephalans as potential human pathogens. Current Clinical Microbiology Reports. 2024 Jun; 11 (2):99-106.
  10. Kleinertz S, Eckhardt KU, Theisen S, Palm HW, Leinweber P. Acanthocephalan fish parasites (Rhadinorhynchidae Lühe, 1912) as potential biomarkers: Molecular–chemical screening by pyrolysis-field ionization mass spectrometry. J Sea Res. 2016; 113: 5 1–7.
  11. Rahimi-Esboei B, Najm M, Shaker M, Fakhar M, Mobedi I. Prevalence of Corynosoma caspicum infection in Gasterosteus aculeatus fish in Caspian Sea, Northern Iran. Vet World. 2017; 10 (9):1139.
  12. Gibson DI, Bray RA, Hunt D, Georgiev BB, Scholz T, Harris PD, et al. Fauna Europaea: helminths (animal parasitic). Biodivers Data J. 2014; (2):e1060.
  13. Bennett J, Poulin R, Presswell B. Acanthocephalan diversity and host associations revealed from a large-scale biodiversity survey. Diversity. 2023; 15 (5):665.
  14. Smales LR. A review of the genus Neoechinorhynchus (Acanthocephala: Neoechinorhynchidae) from Australia with the description of two new species. J Parasitol. 2013; 99 (6):1106–12.
  15. Gallas M, Utz LR. Quadrigyrus torquatus cystacants Van Cleave, 1920 (Acanthocephala: Quadrigyridae) parasitizing species of Astyanax (Characiformes: Characidae) from southern Brazil. Biota Neotropica. 2019; 19 (3):e20180693.
  16. Rosim DF, Ceccarelli PS, Silva-Souza AT. Parasitismo de Hoplias malabaricus (Bloch, 1794) (Characiformes, Erythrinidae) por Quadrigyrus machadoi Fábio, 1983 (Eoacanthocephala, Quadrigyridae) de uma Lagoa em Aguaí, Estado De São Paulo, Brasil. Rev Bras Parasitol Vet. 2005; 14 (4):147–53.
  17. Pavanelli GC, Machado MH, Takemoto RM, Guidelli GM, Lizama M de los AP. Helminth fauna of fishes: diversity and ecological aspects. Up Paraná River Its Floodplain Phys Asp Ecol Conserv Neth Backhuys Publ Leiden. 2004;1: 309–29.
  18. Chemes SB, Brusa RG. Description of Quadrigyrus Machadoi (Fabio, 1983) (Acanthocephala, Quadrigyridae) in native fish of Wetlands associated with the San Javier. Neotropical Helminthol. 2013; 7 (2):187–94.
  19. Bazh EKA, Hamouda AH. Scanning morphology, prevalence and histopathology of some acanthocephalans infecting some River Nile fish. Bulg J Vet Med Online First [Internet]. 2019; 87.
  20. Sheema SH, John MV, George PV. SEM studies on acanthocephalan parasite, Echinorhynchus veli infecting the fish Synaptura orientalis (Bl & Sch, 1801). J Parasit Dis. 2017 Mar; 41 (1):71–5.
  21. Jawad LA, Al‐Jufaili SM. Scale morphology of greater lizardfish Saurida tumbil (Bloch, 1795) (Pisces: Synodontidae). J Fish Biol. 2007 Apr; 70 (4):1185–212.
  22. Amin OM. Marine flora and fauna of the Eastern United States: Acanthocephala. 1998.
  23. Yamaguti S. Systema Helminthum. Vol 5: Acanthocephala. John Wiley & Sons; 1963.
  24. Ward HB. On the structure and classification of North American parasitic worms. J Parasitol. 1917; 4 (1):1–12.
  25. Van Cleave HJ. Two new genera and species of acanthocephalous worms from Venezuelan fishes. Vol. 58. 1920.
  26. Amin OM, Ha NV, Ha DN. First report of Neoechinorhynchus (Acanthocephala: Neoechinorhynchidae) from marine fish of the eastern seaboard of Vietnam, with the description of six new species. Parasite J Société Fr Parasitol. 2011; 18 (1):21.
  27. Kir I, Ozan ST. Seasonal distributions and effects of parasites in pike (esox lucius l., 1758) inhabiting the işikli dam lake (Denizli). Turk Parazitolojii Derg. 2005; 29 (4):291–4.
  28. Nikishin VP. Ultrastructure of the egg shell of the acanthocephalan Neoechinorhynchus crassus. J Helminthol. 2007; 81 (3):233–7.
  29. Popiołek M, Okulewicz J. Helminth’s fauna of fishes in the Mała Panew river drainage basin. Wiad Parazytol. 2000; 46 (1):63–73.
  30. Salgado-Maldonado G, Caspeta-Mandujano JM, Martínez-Ramírez E. Neoechinorhynchus (Neoechinorhynchus) chimalapasensis n. sp. (Acanthocephala: Neoechinorhynchidae) from the freshwater fish Awaous banana (Valenciennes) (Gobiidae) in Mexico. Syst Parasitol. 2010 Mar; 75 (3):231–7.
  31. Uzunay E, Soylu E. Metazoan parasites of carp (Cyprinus carpio Linnaeus, 1758) and vimba (Vimba vimba Linnaeus, 1758) in the Sapanca Lake. Turk Parazitolojii Derg. 2006; 30 (2):141–50.
  32. Violante-González J, Aguirre-Macedo MaL, Mendoza-Franco EF. A checklist of metazoan parasites of fish from Tres Palos Lagoon, Guerrero, Mexico. Parasitol Res. 2007 Oct 18; 102 (1):151–61.
  33. Violante-González J, Rojas-Herrera A. Seasonal patterns in metazoan parasite community of the" fat sleeper" Dormitator latifrons (Pisces: Eleotridae) from Tres Palos Lagoon, Guerrero, Mexico. Rev Biol Trop. 2008; 56 (3):1419–27.
  34. Uliya R, Yusni E. Endoparasitic worms inventory on Skipjack Tuna (Katsuwonus pelamis) gastrointestinal from North Sumatera Indian Ocean, Indonesia. In: IOP Conference Series: Earth and Environmental Science. IOP Publishing; 2020 [cited 2025 Feb 21]. p. 012122.
  35. Aniñon AK, Paylangco R. Detection of Neoechinorhynchus sp. (Acanthocephala: Neoechinorhynchidae) in the Gut of Wild Nile Tilapia (Oreochromis niloticus, L.) from Lake Mainit, Caraga, Philippines. Ann Stud Sci Humanit. 2024; 5 (1):10–7.
  36. Tavakol S, Amin OM, Luus-Powell WJ, Halajian A. The acanthocephalan fauna of Iran, a check list. Zootaxa. 2015; 4033 (2):237–58.
  37. Okoye IC, Abu JS, Obiezue NN, Ofoezie EI. Prevalence and seasonality of parasites of fish in Agulu Lake, Southeast, Nigeria. Afr J Biotechnol [Internet]. 2014; 13 (3).
  38. Chine HJ, Saad CB, Gargouri L. Seasonality and histopathology of Neoechinorhynchus sp.(Rudolphi, 1819)(Acanthocephala: Neoechinorhynchidae) in the flathead grey mullet Mugil cephalus (Linnaeus, 1758) from Ichkeul lagoon in Northern Tunisia. Bull Eur Fish Pathol. 2020; 40: 95–105.
  39. Thomas JD. The ecology of fish parasites with particular reference to helminth parasites and their salmonid fish hosts in Welsh rivers: a review of some of the central questions. 2002.
  40. Emshiheet KA, Elmajdoub LO, Ali KS, Abushiba FM, Elzwawy SE, Abusahal MM, et al. Occurrence of Neoechinorhynchus sp. in Infected Organs of Lizardfish (Saurida undosquamis) in Misurata, Libya. Environ Sci. 2024; 3 (1):67.
  41. Amin OM, Sharifdini M, Heckmann R, Ha NV. 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. J Parasitol. 2019; 105 (4):606–18.
  42. Amin OM, Chaudhary A, Heckmann R, Ha NV, Singh HS. Redescription and molecular analysis of Neoechinorhynchus (Neoechinorhynchus) johnii Yamaguti, 1939 (Acanthocephala, Neoechinorhynchidae) from the Pacific Ocean off Vietnam. Parasite. 2019; 26: 43.
  43. Amin OM, Heckmann RA, Dallarés S, Constenla M, Rubtsova NY, Kuzmina T. New perspectives on Aspersentis megarhynchus (Acanthocephala: Heteracanthocephalidae) from Notothenia coriiceps Richardson (Nototheniidae) in the West Antarctic, with emended generic diagnosis. J Helminthol. 2021; 95: e27.
  44. Solaimani A, Kamrani E, Zamanirad M, Kleinertz S. Parasitic contaminationof Mudskipper (Boleophthalmus dussumieri) in coastal waters of Banddar-Abbas. Iran Vet J. 2014; 10 (1):68–76.
  45. Fujimoto RY, Barros ZMN de, Marinho-Filho AN, Diniz DG, Eiras JC. Parasites of four ornamental fish from the Chumucuí River (Bragança, Pará, Brazil). Rev Bras Parasitol Veterinária. 2013; 22 (1):34–8.