Abstract
Euclinostomum heterostomum and Euclinostomum ardeolae, both encysted metacercariae (EMC), were found to infect farmed Oreochromis niloticus in the Sahary fish hatchery and wild O. niloticus, Sarotherodon galilaeus, and Tilapia zillii in Lake Nasser, Aswan Governorate, Egypt, at a prevalence of 25.25% and an infection intensity of 1–14 EMC/fish. Macroscopic and microscopic examinations were used to identify them morphologically. PCR amplification, sequencing of the 28S large ribosomal RNA region, and phylogenetic analysis were used for molecular characterization. E. heterostomum and E. ardeolae were isolated from farmed O. niloticus kidneys, peritoneum, abdominal cavity, and under the gills attached to the head bone at prevalence of 13.5% and 6%, respectively, and from wild O. niloticus, S. galilaeus, and T. zillii at a prevalence of 15% and 4.5%, 18% and 10%, and 22.5% and 11.5% respectively. The molecular analyses of rRNA-28S marker revealed that the two Euclinostomum species examined are related yet distinct. This is the first molecular and phylogenetic evidence linking E. ardeolae to Euclinostomum. The present study added two new sequences to the GenBank databases for the genus Eulinostomum from Egypt, with accession numbers MW604803 and MW604806. Euclinostomum spp. have been shown to have detrimental and destructive effects on the kidneys of infected fish; these effects may eventually result in the parasites’ cysts replacing the kidney’s tissues. The kidneys of tilapia spp. infected with Euclinostomum spp. displayed degenerative alterations, with dilated renal tubules associated with migratory tunnels composed primarily of leucocytic infiltrations. Euclinostomum spp. exhibited clear hemophagic characteristics.
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Data Availability statement
The data sets used in the present study are accessible on reasonable request from the corresponding author.
References
Athokpam VD, Jyrwa DB, Tandon V (2016) Utilizing ribosomal DNA gene marker regions to characterize the metacercariae (Trematoda: Digenea) parasitizing piscine intermediate hosts in Manipur, Northeast India. Journal of Parasitic Diseases: Official Organ of the Indian Society for Parasitology 40(2):330–338. https://doi.org/10.1007/s12639-014-0504-9
AVMA (American Veterinary Medical Association) (2013) Guidelines for the euthanasia of animals (2013rd ed.). American Veterinary Medical Association 1931 N. Meacham Road Schaumburg, IL 60173: American Veterinary Medical Association. https://www.avma.org/ sites/ default/files/ resources/euthanasia.pdf.
AVMA (American Veterinary Medical Association) (2020) Guidelines for the Euthanasia of Animals: 2020 Edition, 1931 N. Meacham Road, Schaumburg, IL 60173, USA. https://www.avma.org/sites/default/files/2020-01/2020_Euthanasia_Final_1-15-20.pdf
Bancroft JD, Gamble M (2007) Theory and practice of histological techniques, 5th edn. Churchill Livingstone, London, pp 125–138. https://www.sigma aldrich.com/EG/en/product/sigma/ t5321
Briosio-Aguilar R, García-Varela M, Hernández-Mena DI, Rubio-Godoy M, Pérez-Ponce de León G (2019) Morphological and molecular characterization of an enigmatic clinostomid trematode (Digenea: Clinostomidae) parasitic as metacercariae in the body cavity of freshwater fishes (Cichlidae) across Middle America. J Helminthol 93(4):461–474. https://doi.org/10.1017/S0022149X18000445
Britz J, Van As JG, Saayman JE (1985) Occurrence and distribution of Clinostomum tilapiae Ukoli, 1966 and Euclinostomum heterostomum (Rudolphi, 1809) metacercarial infections of freshwater fish in Venda and Lebowa. Southern Africa J Fish Biol 26(1):21–28. https://doi.org/10.1111/j.1095-8649.1985.tb04236.x
Bush AO, Lafferty KD, Lotz JM, Shostak AW (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. The Journal of Parasitology 83(4):575–583. https://doi.org/10.2307/3284227
Caffara M, Locke SA, Cristanini C, Davidovich N, Markovich M, Fioravanti M (2016) A combined morphometric and molecular approach to identifying metacercariae of Euclinostomum heterostomum (Digenea: Clinostomidae). J Parasitol 102(2):239–248. https://doi.org/10.1645/15-823
Caffara M, Locke SA, Echi PC, Halajian A, Benini D, Luus-Powell WJ, Tavakol S, Fioravanti ML (2017) A morphological and molecular study of Clinostomid metacercariae from African fish with a redescription of Clinostomum tilapiae. Parasitology 144(11):1519–1529. https://doi.org/10.1017/S0031182017001068
Caffara M, Locke SA, Echi PC, Halajian A, Luus-Powell WJ, Benini D, Tedesco P, Fioravanti ML (2020) A new species of Clinostomum Leidy, 1856 based on molecular and morphological analysis of metacercariae from African siluriform fishes. Parasitol Res 119(3):885–892. https://doi.org/10.1007/s00436-019-06586-2
Caffara M, Locke SA, Gustinelli A, Marcogliese DJ, Fioravanti ML (2011) Morphological and molecular differentiation of Clinostomum complanatum and Clinostomum marginatum (Digenea: Clinostomidae) metacercariae and adults. J Parasitol 97(5):884–891. https://doi.org/10.1645/GE-2781.1
Caffara M, Locke SA, Halajian A, Luus-Powell WJ, Benini D, Tedesco P, Kasembele GK, Fioravanti ML (2019) Molecular data show Clinostomoides Dollfus, 1950 is a junior synonym of Clinostomum Leidy, 1856, with redescription of metacercariae of Clinostomum brieni n. comb. Parasitology 146(6):805–813. https://doi.org/10.1017/S0031182018002172
Claude EB, Tucker CS (1998) Pond Aquaculture Water Quality Management, 1st edn. Springer, , USA. https://doi.org/10.1007/978-1-4615-5407-3
Dereeper A, Guignon V, Blanc G, Audic S, Buffet S, Chevenet F, Dufayard JF, Guindon S, Lefort V, Lescot M, Claverie JM, Gascuel O (2008) Phylogeny fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 36(Web Server issue):W465-469. https://doi.org/10.1093/nar/gkn180
Dzikowski R, Levy MG, Poore MF, Flowers JR, Paperna I (2004) Clinostomum complanatum and Clinostomum marginatum (Rudolphi, 1819) (Digenea: Clinostomidae) are separate species based on differences in ribosomal DNA. J Parasitol 90(2):413–414. https://doi.org/10.1645/GE-159R
Echi P, Eyo J, Okafor F, Onyishi G, Ivoke N (2012) First record of co-infection of three clinostomatid parasites in Cichlids (Osteichthyes: Cichlidae) in a tropical freshwater lake. Iran J Public Health 41(7):86–90
Eissa, A. E. (2016). Clinical and laboratory manual of fish diseases. LAP LAMBERT Academic Publishing. https://www.morebooks.shop/store/ gb/book/clinical-and-laboratory -manual-of-fish-diseases/isbn/978–3–659–87612–7
El-Naffar MK, Khalifa RM (1981) Euclinostomum ardeolae sp. nov. (Trematoda: Clinostomatidae). J. Egypt. Soc. Parasitol 11(1):175–181
FAO (Food and Agriculture Organization) (2018) The state of world fisheries and aquaculture 2018 - meeting the sustainable development goals. Rome. Licence: CC BY-NC-SA 3.0 IGO. http://www.fao.org/3/i9540en/i9540en.pdf
Ezzat SM, ElKorashey RM, Sherif MM (2012) The economical value of Nile Tilapia Fish "Oreochromis niloticus" in relation to water quality of Lake Nasser, Egypt. Journal of American Science 8(9): 234–247. https://www.researchgate.net/publication/297569885_The_economic_value_of_Nile_Tilapia_Fish_Oreochromis_niloticus_in_relation_to_water_quality_of_lake_Nasser_Egypt
Fischthal JH, Kuntz RE (1963) Trematode Parasites of Fishes from Egypt Part VI. The Metacercaria of Euclinostomum heterostomum (Rudolphi, 1809) Travassos, 1928 (Clinostomidae), with a Review of the Genus. Transactions of the American Microscopical Society 82(3):335–342. https://doi.org/10.2307/3223934
Gustinelli A, Caffara M, Florio D, Otachi EO, Wathuta EM, Fioravanti ML (2010) First description of the adult stage of Clinostomum cutaneum Paperna, 1964 (Digenea: Clinostomidae) from grey herons Ardea cinerea L. and a redescription of the metacercaria from the Nile tilapia Oreochromis niloticus niloticus (L.) in Kenya. Syst Parasitol 76:39–51. https://doi.org/10.1007/s11230-010-9231-5
Halls AS, Habib OA, Nasr-Allah A, Dickson M (2015) Lake Nasser fisheries: Literature review and situation analysis. Penang, Malaysia: WorldFish. Program Report: 2015–42. http://pubs.iclarm.net/resource_centre/2015-42.pdf
Hamouda AH (2014) Studies on the trematodal and cestodal diseasesin cultured freshwater fish in Kafr El-Sheikh Governorate. PhD thesis, Egypt: Faculty of Veterinary Medicine, Kafrelsheikh University.
Hamouda AH, Abd Alkareem OM (2021) Insight into the correlation between parasitic infestation and heavy metal concentrations in tilapia species inhabiting Lake Nasser. Egypt Aquaculture Research 52(7):3425–3437. https://doi.org/10.1111/are.15187
Hamouda AH, Moustafa EM, Zayed MM (2019). Overview on the most prevailing bacterial diseases infecting Oreochromis niloticus at Aswan fish hatchery, Egypt. Adv. Anim. Vet. Sci. 7(11): 950–961. https://nexusacademicpublishers.com/uploads/files/AAVS_7_11_950-961.pdf
Hamouda AH, Sorour SS, El-Habashi NM, El-Hussein AA (2018). Parasitic infection with emphasis on Tylodelphys spp. as new host and locality records in Nile Perch; Lates niloticus from Lake Nasser, Egypt. World Veterinary Journal, 8(1), 19–33. https://wvj.science-line.com/attachments/article/52/WVJ%208(1)%2019-33,%20Mar%2025,%202018.pdf
Hamouda AH, Younis AE (2021) Characterization of Clinostomum cutaneum and Clinostomum phalacrocoracis in tilapia species of Aswan Governorate, Egypt: A morphological, molecular and histopathological study. Aquac Res 00:1–15. https://doi.org/10.1111/are.15543
Kanev I, Radev V, Fried B (2002). Family Clinostomidae Luhe, 1901. In Keys to the Trematoda, Volume 1. Gibson DI, Jones A, Bray RA (eds.). CAB International and the Natural History Museum, London, U.K., p. 113–120. https://www.cabi.org/bookshop/book/9780851995472/
Li F, Liu X, Ge H, Xie CH, Cai R, Hu Z, Zhang Y, Wang Z (2018) The discovery of Clinostomum complanatum metacercariae in farmed Chinese sucker. Myxocyprinus Asiaticus.Aquaculture 495(2018):273–280. https://doi.org/10.1016/j.aquaculture.2018.05.052
Mahdy O, Abdel- Maogood S, Mohammed F, Salem M (2017) Effect of verbesina alternifolia and mentha piperita oil extracts on newly excysted metacercaria of Euclinostomum heterostomum (Rudolphi, 1809) (Digenea: clinostomatidae) from naturally infected kidneys of Tilapia zillii in Egypt. J Egypt Soc Parasitol 47(3):513–521. https://doi.org/10.21608/jesp.2017.77706
Mahdy OA, Abdelsalam M, Abdel- Maogood SZ, Shaalan M, Salem MA (2021) First genetic confirmation of Clinostomidae metacercariae infection in Oreochromis niloticus in Egypt. Aquac Res 00:1–9. https://doi.org/10.1111/are.15565
Mansour R (2019) First record of Euclinostomum heterostomum from the naturally-infected heron “Ardeola ralloides” in Egypt: a light & scanning electron microscopy study. Egyptian Journal of Zoology 72(72):22–31. https://doi.org/10.21608/ejz.2019.18363.1015
Mashego SN, Saayman JE (1989) Digenetic trematodes and cestodes of Clarias gariepinus (Burchell, 1822) in Lebowa, South Africa, with taxonomic notes. S. A. J. Wildlife Res. 19 (1): 17–20.https://www.researchgate.net/profile/Sevid-Mashego/publication/285810796_Digenetic_trematodes_and_cestodes_of_Clarias_gariepinus_Burchell_1822_in_Lebowa_South_Africa_with_taxonomic_notes/links/5b3100f40f7e9b0df5c7ed8f/Digenetic-trematodes-and-cestodes-of-Clarias-gariepinus-Burchell-1822-in-Lebowa-South-Africa-with-taxonomic-notes.pdf
Mohamed FAS (2009) Histopathological Studies on Tilapia zillii and Solea vulgaris from Lake Qarun, Egypt. World. J. Fish. Mar. Sci., 1(1): 29–39. https://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.533.5081&rep=rep1&type=pdf
Morenikeji OA, Adepeju AI (2009) Helminth communities in Cichlids in natural and man-made ponds in southwest Nigeria. Researcher 1(3):84–92. https://sciencepub.net/researcher/ 0103/13_0727_helminth_research0103.pdf.
Nasr-Allah AM, Habib OA, Dickson M, Dickson C (2016) Value chain analysis of Lake Nasser fisheries in Aswan, Upper Egypt. Penang, Malaysia: WorldFish. Program Report: 2016–11. https://digitalarchive.worldfishcenter.org/bitstream/handle/20.500.12348/531/Program%20Report_2016-11_Value%20Chain%20Analysis%20of%20Lake%20Nasser%20Fisheries%20in%20Aswan%2C%20Upper%20Egypt_FA_lowres.pdf?sequence=12&isAllowed=y
Oğuz AR (2015) A histological study of the kidney structure of Van fish (Alburnus tarichi) acclimated to highly alkaline water and freshwater. Mar Freshw Behav Physiol 48(2):135–144. https://doi.org/10.1080/10236244.2015.1004838
Oliver PAS, Luus-Powell WJ, Saayman JE (2009) Report on some monogenean and clinostomid infestations of freshwater fish and waterbird hosts in Middle Letaba Dam, Limpopo Province, South Africa. Onderstepoort j. vet. res. 76 (2):187–199. http://www.scielo.org.za/pdf/ojvr/v76n2/04.pdf
McL PC, Evensen Ø (1999) The morphology of the immune system in teleost fishes. Fish Shellfish Immunol 9(4):309–318. https://doi.org/10.1006/fsim.1998.0181
Scholz T, Vanhove M, Smit N, Jayasundera Z, Gelnar M (2018). A Guide to the Parasites of African Freshwater Fishes: Diversity, Ecology and Research Methods. ABC Taxa. CEBioS, Royal Belgian Institute of Natural Sciences. http://biblio.naturalsciences.be/rbins-publications/abc-txa/abc-taxa-18/abctaxa18_final_hr-intro.pdf
Sereno-Uribe AL, Pinacho-Pinacho CD, García-Varela M, de León GP (2013) Using mitochondrial and ribosomal DNA sequences to test the taxonomic validity of Clinostomum complanatum Rudolphi, 1814 in fish-eating birds and freshwater fishes in Mexico, with the description of a new species. Parasitol Res 112(8):2855–2870. https://doi.org/10.1007/s00436-013-3457-5
Shareef PAA, Abidi MAS (2015) Studies on the epidemiology and histopathology of Euclinostomum heterostomum (Trematoda; Digenea) infection in Channa punctata from North India. Arch Pol Fish 23:133–140. https://doi.org/10.1515/aopf-2015-0015
Suanyuk N, Mankhakhet S, Soliman H, Saleh M, El-Matbouli M (2013) Euclinostomum heterostomum infection in guppies Poecilia reticulata cultured in southern Thailand. Dis Aquat Org 104:121–127. https://doi.org/10.3354/dao02595
Senapin S, Phiwsaiya K, Laosinchai P, Kowasupat C, Ruenwongsa P, Panijpan B (2014) Phylogenetic analysis of parasitic trematodes of the genus Euclinostomum found in Trichopsis and Betta fish. J Parasitol 100(3):368–371. https://doi.org/10.1645/13-285.1
Taher GA (2009) Some studies on metacercarial infection in Oreochromis niloticus in Assuit Governorate and their role in transmission of some trematodes to dogs. Assiut University Bulletin for Environmental Researches 12.1(12.1):63–78. https://doi.org/10.21608/auber.2009.149541
Tkach V, Pawlowski J, Mariaux J (2000) Phylogenetic analysis of the suborder plagiorchiata (Platyhelminthes, Digenea) based on partial lsrDNA sequences. Int J Parasitol 30(1):83–93. https://doi.org/10.1016/s0020-7519(99)00163-0
Ukoli F (1966) On Euclinostomum heterostomum (Rudolphi, 1809). J Helminthol 40(1–2):227–234. https://doi.org/10.1017/S0022149X00034210
van Zwieten PAM, Bene C, Kolding J, Brummett R, Valbo-Jorgensen J (2011) Review of tropical reservoirs and their fisheries – The cases of Lake Nasser, Lake Volta and Indo-Gangetic Basin reservoirs. FAO Fisheries and Aquaculture Technical Paper No. 557. Rome: Food and Agriculture Organization of the United Nations. http://www.fao.org/3/i1969e/i1969e00.pdf
Vankara A, Mani G, Vijayalakshmi C (2011) A report on various digenetic metacercariae from the freshwater fishes of River Godavari. Rajahmundry Journal of Parasitic Diseases 35(2):177–185. https://doi.org/10.1007/s12639-011-0041-8
Zhokhov AE, Morozova D (2020) Clinostomid Metacercariae (Clinostomidae Lühe, 1901) in Fishes of Lake Tana (Ethiopia). Inland Water Biology 13(2):279–290. https://doi.org/10.1134/S1995082920020157
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The authors would like to thank Ashraf Emam, Professor of Applied Geology at Aswan University’s Faculty of Science, for his assistance in creating the location map.
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Younis, A.E., Hamouda, A.H. & Moustafa, E.M. Euclinostomum heterostomum and E. ardeolae in tilapia species of Aswan Governorate, Egypt: morphological, molecular, and histopathological characterization. Aquacult Int 30, 825–844 (2022). https://doi.org/10.1007/s10499-022-00839-1
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DOI: https://doi.org/10.1007/s10499-022-00839-1