Clinostomum Sinensis in Red-crowned Cranes (Grus japonensis) and in White-naped Cranes (Grus vipio) - Morphology and Molecular Characterization (original) (raw)

Authors

DOI:

https://doi.org/10.22456/1679-9216.140411

Keywords:

trematodes, Clinostomum sinensis, Clinostomum spp., crane, morphology, 18S rRNA, COI

Abstract

Background : Clinostomum spp. are digenetic trematode parasites of freshwater snails and fishes, fish-eating birds, and humans. There are widely distributed around the world. The metacercariae of the Clinostomum can cause fish trematodes, and adults parasites parasitized in the throat and esophagus of fish-eating birds. The red-crowned crane (Grus japonensis) and white-naped cranes (Grus vipio) are internationally recognized as an endangered species. They are large wading bird species and listed as Class I protected animals in China. To date, there have been no reports of Clinostomum infection in red-crowned cranes (Grus japonensis) and white-naped cranes (Grus vipio) in China.

Materials, Methods & Results : In this study, we isolated specimens of Clinostomum sinensis adults from the oral cavity of red-crowned cranes (Grus japonensis) and white-naped cranes (Grus vipio) and encysted “yellow grub” metacercariae from the forage fish Pseudorasbora parva and used morphological analysis and molecular characterization based on 18S ribosomal RNA and the mitochondrial cytochrome oxidase (COI) loci. The digestive system of the metacercariae was clear, whereas the genital system was not, with the exception of the vitellaria. Morphological features of adults included a small oral sucker, an unclear or absent pharynx, a medium-sized ventral sucker, an ovoid cirrus pouch near the anterior testis, and a uterine sac that extended to the ventral sucker with no folds, especially the entire anterior testis offset to the left by the uterine sac and cirrus sac, and genital pore opening on the right side of the anterior testis and papillae around, compared with the features of other species of Clinostomum. At the 18S loci, the species was in the same clade with C. complanatum from Italy and Israel. It speculated that although the specimens sequenced in this study grouped with the sequences of C. complanatum from Asia, there are so few species that have been sequenced (and verified) that identification of the sequences in this study is still problematic. At the COI loci, Clinostomum spp. were clearcutted into different clades depending on geographical regions. The species isolated in this study was in the same clade as isolates from Asia. While, based on 18S or COI loci sequences analysis, the isolated specimens were identified as C. sinensis. Morphological observation also identified the precise species was C. sinensis. Above of all, we isolated C. sinensis from cranes and P. parva in eastern China firstly, and firstly descripted the morphology of adult of C. sinensis in eastern China.

Discussion : Precise species identification is crucial for controlling and treating parasite infections. Traditionally, morphological characteristics have been used to identify trematode species, although larval stages pose challenges due to fewer features. Molecular methods have proven effective, especially for morphologically similar species. This study identified C. sinensis in red-crowned (Grus japonensis) and white-naped cranes (Grus vipio) and their intermediate host P. parva in eastern China, using both morphology and molecular methods. Morphological analysis showed similarities with previous studies, with clear identification of the oral and ventral suckers in metacercariae, and specific features in adults such as the small oral sucker and ovoid cirrus pouch. Molecular analysis using 18S rRNA and COI loci revealed that the isolates clustered with C. complanatum and C. sinensis from Asia, with minimal sequence differences, confirming the specimens as C. sinensis.

Keywords: trematodes, Clinostomum sinensis, Clinostomum spp., crane, morphology, 18S rRNA, COI.

Downloads

Download data is not yet available.

References

Brant S.V., Morgan J.A.T., Mkoji G.M., Snyder S.D., Rajapakse R.P.V.J. & Loker E.S. 2006. An approach to revealing blood fluke life cycles, taxonomy, and diversity: provision of key reference data including DNA sequence from single life cycle stages. Journal of Parasitology. 92(1): 77-88. DOI: https://doi.org/10.1645/GE-3515.1

Caffara M., Bruni G., Paoletti C., Gustinelli A. & Fioravanti M.L. 2014. Metacercariae of Clinostomum complanatum (Trematoda: Digenea) in European newts Triturus carnifex and Lissotriton vulgaris (Caudata: Salamandridae). Journal of Helminthology. 88(3): 278-285. DOI: https://doi.org/10.1017/S0022149X13000151

Caffara M., Locke S.A., Gustinelli A., Marcogliese D.J. & Fioravanti M.L. 2011. Morphological and Molecular Differentiation of Clinostomum complanatum and Clinostomum marginatum (Digenea: Clinostomidae) Metacercariae and Adults. Journal of Parasitology. 97(5): 884-891. DOI: https://doi.org/10.1645/GE-2781.1

Dias M.L.G.G., Eiras J.C., Machado M.H., Souza G.T.R. & Pavanelli G.C. 2003. The life cycle of Clinostomum complanatum Rudolphi, 1814 (Digenea, Clinostomidae) on the floodplain of the high Paraná river, Brazil. Parasitology Research. 89(6): 506-508. DOI: https://doi.org/10.1007/s00436-002-0796-z

Dzikowski R., Levy M., Poore M., Flowers J. & Paperna I. 2004. Use of rDNA polymorphism for identification of Heterophyidae infecting freshwater fishes. Diseases of Aquatic Organisms. 59: 35-41. DOI: https://doi.org/10.3354/dao059035

Dzikowski R., Levy M.G., Poore M.F., Flowers J.R. & Paperna I. 2004. Clinostomum complanatum and Clinostomum marginatum (Rudolphi, 1819) (Digenea: Clinostomidae) Are Separate Species Based on Differences in Ribosomal DNA. Journal of Parasitology. 90(2): 413-414. DOI: https://doi.org/10.1645/GE-159R

El-Bahy N.M., Bazh E.K., Sorour S.S. & Elhawary N.M. 2017. Molecular characterization of the unique Mesostephanus appendiculatus (Trematoda: Cyathocotylidae) by small ribosomal RNA from Egypt. Parasitology Research. 116(4): 1129-1136. DOI: https://doi.org/10.1007/s00436-016-5342-5

Gholami Z., Mobedi I., Esmaeili H. & Kia E. 2011. Occurrence of Clinostomum complanatum in Aphanius dispar (Actinoptrygii: Cyprinodontidae) collected from Mehran River, Hormuzgan Province, South of Iran. Asian Pacific Journal of Tropical Biomedicine. 1(3): 189-192. DOI: https://doi.org/10.1016/S2221-1691(11)60025-7

Gustinelli A., Caffara M., Florio D., Otachi E.O., Wathuta E.M. & Fioravanti M.L. 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. Systematic Parasitology. 76(1): 39-51. DOI: https://doi.org/10.1007/s11230-010-9231-5

Hara H., Miyauchi Y., Tahara S. & Yamashita H. 2014. Human laryngitis caused by Clinostomum complanatum. Nagoya Journal of Medical Science. 76(1-2): 181-185.

Iwaki T., Waki T., Arakawa J. & Ogawa K. 2018. The Digenean Clinostomum complanatum Found from Great Cormorant Phalacrocorax carbo in Japan. Fish Pathology. 53(4): 132-135. DOI: https://doi.org/10.3147/jsfp.53.132

Kitagawa N., Oda M., Totoki T., Washizaki S., Oda M. & Kifune T. 2003. Lidocaine spray used to capture a live Clinostomum parasite causing human laryngitis. American Journal of Otolaryngology. 24(5): 341-343. DOI: https://doi.org/10.1016/S0196-0709(03)00060-7

Locke S.A., Caffara M., Barčák D., Sonko P., Tedesco P., Fioravanti M.L. & Li W. 2019. A new species of Clinostomum Leidy, 1856 in East Asia based on genomic and morphological data. Parasitology Research. 118(12): 3253-3265. DOI: https://doi.org/10.1007/s00436-019-06536-y

Matthews D. & Cribb T.H. 1998. Digenetic trematodes of the genus Clinostomum Leidy, 1856 (Digenea: Clinostomidae) from birds of Queensland, Australia, including C. wilsoni n. sp. from Egretta intermedia. Systematic Parasitology. 39(3): 199-208. DOI: https://doi.org/10.1023/A:1005982530560

Menconi V., Manfrin C., Pastorino P., Mugetti D., Cortinovis L., Pizzul E., Pallavicini A. & Prearo M. 2020. First Report of Clinostomum complanatum (Trematoda: Digenea) in European Perch (Perca fluviatilis) from an Italian Subalpine Lake: A Risk for Public Health? International Journal of Environmental Research and Public Health. 17(4): 1389. DOI: https://doi.org/10.3390/ijerph17041389

Park C.W., Kim J.S., Joo H.S. & Kim J. 2009. A Human Case of Clinostomum complanatum Infection in Korea. The Korean Journal of Parasitology. 47(4): 401. DOI: https://doi.org/10.3347/kjp.2009.47.4.401

Sereno-Uribe A.L., Pinacho-Pinacho C.D., García-Varela M. & De León G.P.-P. 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. Parasitology Research. 112(8): 2855-2870. DOI: https://doi.org/10.1007/s00436-013-3457-5

Shamsi S., Barton D.P., Day S., Masiga J., Zhu X. & McLellan M. 2021. Characterization of Clinostomum sp. (Trematoda: Clinostomidae) infecting cormorants in south-eastern Australia. Parasitology Research. 120(8): 2793-2803. DOI: https://doi.org/10.1007/s00436-021-07246-0

Shamsi S., Day S., Zhu X., McLellan M., Barton D.P., Dang M. & Nowak B.F. 2021. Wild fish as reservoirs of parasites on Australian Murray cod farms. Aquaculture. 539: 736584. DOI: https://doi.org/10.1016/j.aquaculture.2021.736584

Shareef P.A. & Abidi S. 2012. Incidence and histopathology of encysted progenetic metacercaria of Clinostomum complanatum (Digenea: Clinostomidae) in Channa punctatus and its development in experimental host. Asian Pacific Journal of Tropical Biomedicine. 2(6): 421-426. DOI: https://doi.org/10.1016/S2221-1691(12)60068-9

Shareef P.A.A. & Abidi S.M.A. 2013. Egg viability studies on Clinostomum complanatum (Digenea: Clinostomidae) from two experimental animal model systems. Parasitology Research. 112(5): 2101-2103. DOI: https://doi.org/10.1007/s00436-013-3293-7

Silva-Souza A.T. & Ludwig G. 2005. Parasitism of Cichlasoma paranaense Kullander, 1983 and Gymnotus carapo Linnaeus, 1814 by Clinostomum complanatum (Rudolphi, 1814) metacercariae in the Taquari river. Brazilian Journal of Biology = Revista Brasleira de Biologia. 65(3): 513-519. DOI: https://doi.org/10.1590/S1519-69842005000300017

Simsek E., Yildirim A., Yilmaz E., Inci A., Duzlu O., Onder Z., Ciloglu A., Yetismis G. & Pekmezci G.Z. 2018. Occurrence and molecular characterization of Clinostomum complanatum (Trematoda: Clinostomidae) in freshwater fishes caught from Turkey. Parasitology Research. 117(7): 2117-2124. DOI: https://doi.org/10.1007/s00436-018-5898-3

Sohn W.M. 2009. Fish-borne Zoonotic Trematode Metacercariae in the Republic of Korea. The Korean Journal of Parasitology. 47(Suppl): S103. DOI: https://doi.org/10.3347/kjp.2009.47.S.S103

Tiewchaloern S., Udomkijdecha S., Suvouttho S., Chunchamsri K. & Waikagul J. 1999. Clinostomum trematode from human eye. The Southeast Asian Journal of Tropical Medicine and Public Health. 30(2): 382-384.

Van Steenkiste N., Locke S.A., Castelin M., Marcogliese D.J. & Abbott C.L. 2015. New primers for DNA barcoding of digeneans and cestodes (Platyhelminthes). Molecular Ecology Resources. 15(4): 945-952. DOI: https://doi.org/10.1111/1755-0998.12358

Vilas R., Criscione C.D. & Blouin M.S. 2005. A comparison between mitochondrial DNA and the ribosomal internal transcribed regions in prospecting for cryptic species of platyhelminth parasites. Parasitology. 131(06): 839. DOI: https://doi.org/10.1017/S0031182005008437

Wang M.L., Chen H.Y. & Shih H.H. 2017. Occurrence and distribution of yellow grub trematodes (Clinostomum complanatum) infection in Taiwan. Parasitology Research. 116(6): 1761-1771. DOI: https://doi.org/10.1007/s00436-017-5457-3

Yang R., Brice B., Jian F. & Ryan U. 2018. Morphological and molecular characterisation of Isospora butcherae n. sp. in a silvereye (Zosterops lateralis) (Latham, 1801). Parasitology Research. 117(5): 1381-1388. DOI: https://doi.org/10.1007/s00436-018-5808-8

How to Cite

Wang, F., Ni, G., Chen, C., Cao, L., Hu, F., Xu, L., … Liu , D. (2024). Clinostomum Sinensis in Red-crowned Cranes (Grus japonensis) and in White-naped Cranes (Grus vipio) - Morphology and Molecular Characterization . Acta Scientiae Veterinariae, 52(1). https://doi.org/10.22456/1679-9216.140411

License

Copyright (c) 2024 Feiyan Wang, Guyin Ni, Chen Chen, Liqin Cao, Fei Hu, Lu Xu, Jiaxiu Hou, Jinjun Xu, Jianping Tao, Dandan Liu

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

This journal provides open access to all of its content on the principle that making research freely available to the public supports a greater global exchange of knowledge. Such access is associated with increased readership and increased citation of an author's work. For more information on this approach, see the Public Knowledge Project and Directory of Open Access Journals.

We define open access journals as journals that use a funding model that does not charge readers or their institutions for access. From the BOAI definition of "open access" we take the right of users to "read, download, copy, distribute, print, search, or link to the full texts of these articles" as mandatory for a journal to be included in the directory.

La Red y Portal Iberoamericano de Revistas Científicas de Veterinaria de Libre Acceso reúne a las principales publicaciones científicas editadas en España, Portugal, Latino América y otros países del ámbito latino