Hostname: page-component-848d4c4894-5nwft Total loading time: 0 Render date: 2024-06-13T07:10:37.050Z Has data issue: false hasContentIssue false
  • English
  • Français

Rhipidocotyle husi n. sp. and three known species of Bucephalidae Poche, 1907 from the East Asian Region: morphological and molecular data

Published online by Cambridge University Press:  04 March 2022

Dmitry M. Atopkin Open the ORCID record for Dmitry M. Atopkin [Opens in a new window] ,
Marina B. Shedko ,
Konstantin V. Rozhkovan ,
Ha V. Nguyen  and
Vladimir V. Besprozvannykh
Dmitry M. Atopkin*
Affiliation:
Federal Scientific Center of East Asia Terrestrial Biodiversity, Far Eastern Branch of Russian Academy of Sciences, 690022, Vladivostok, Russia Department of Cell Biology and Genetics, Far Eastern Federal University, 690051, Ajax-10 str., Vladivostok, Russia
Marina B. Shedko
Affiliation:
Federal Scientific Center of East Asia Terrestrial Biodiversity, Far Eastern Branch of Russian Academy of Sciences, 690022, Vladivostok, Russia
Konstantin V. Rozhkovan
Affiliation:
Saint-Petersburg State University Clinic, St. Petersburg, Russia State Research Institute on Lake and River Fishery (FGBNU ‘GOSNIORKh), St. Petersburg, Russia
Ha V. Nguyen
Affiliation:
Institute of Ecology and Biological Resources, Vietnamese Academy of Sciences and Technology, Hanoi, Vietnam
Vladimir V. Besprozvannykh
Affiliation:
Federal Scientific Center of East Asia Terrestrial Biodiversity, Far Eastern Branch of Russian Academy of Sciences, 690022, Vladivostok, Russia
*
Author for correspondence: Dmitry M. Atopkin, E-mail: atop82@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Morphological data and the first molecular data are provided for four species of the trematode family Bucephalidae Poche, 1907 from marine and freshwater teleost fish species of East Asia. A new species, Rhipidocotyle husi n. sp., was isolated from Huso dauricus from the Amur River, Russia. Adult worms of this species were distinguished from their congeners Rhipidocotyle illense and Rhipidocotyle kovalai by morphological analysis. Three other known species were identified: Bucephalus skrjabini and Prosorhynchus cf. squamatus were detected in Siniperca chuatsi from the Amur River and in Myoxocephalus spp. from the Okhotsk Sea, Russia, respectively, while Prosorynchoides karvei was extracted from Strongylura strongylura from Halong Bay, Vietnam. The 28S ribosomal DNA (rDNA)-based phylogenetic analysis showed that the new species formed a shared polytomy clade with Rhipidocotyle fennica. Phylogenetic analysis of all available molecular data showed that four genera, namely Rhipidocotyle, Bucephalus, Prosorynchoides and Prosorhynchus, are para- or polyphyletic. Molecular-based phylogenetic analysis of morphologically validated bucephalid species indicated that three genera – Rhipidocotyle, Bucephalus and Prosorynchoides – were monophyletic. The genus Prosorhynchus maintained paraphyly, and P. cf. squamatus was more closely related to Dollfustrema spp. than to other Prosorhynchus spp. These findings do not exclude the possibility that representatives of Dollfustrema and P. cf. squamatus belong to the same genus.

Keywords

BucephalidaeBucephalusDNA sequenceProsorhynchoidesProsorhynchusRhipidocotyle
Type
Research Article
Information
Parasitology , Volume 149 , Issue 6 , May 2022 , pp. 774 - 785
Check for updates
Copyright
Copyright © The Author(s), 2022. 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

Akhmerov, AH (1963) Two new Far Eastern bucephalid species (Trematoda, Bucephalidae). In Schikhobalova, NP et al. (ed), Helminths of man, Animals and Plants and Their Control: Papers on Helminthology Presented to Academician K. I. Skryabin on his 85th Birthday. Moscow, URRS: Academy of Science Publishing, pp. 126–129.Google Scholar
Andres, MJ, Pulis, EE, Cribb, TH and Overstreet, RM (2014) Erection of the haploporid genus Litosaccus n.g. and its phylogenetic relationship within the Haploporidae Nicoll, 1914. Systematic Parasitology 89, 185–194.CrossRefGoogle ScholarPubMed
Baba, T, Nakamura, D, Hosoi, M and Urabe, M (2012) Molecular identification of larval bucephalids, Prosorhynchoides ozakii and Parabucephalopsis parasiluri, infecting the golden mussel, Limnoperna fortunei, by PCR-RFLP. Journal of Parasitology 98, 669–673.CrossRefGoogle ScholarPubMed
Benz, JW and Bullard, SA (2004) Metazoan parasites and associates of chondrichthyans with emphasis on taxa harmful to captive hosts. In Smith, M, Warmolts, D, Thoney, D and Hueter, R (eds), The Elasmobranch Husbandry Manual: Captive Care of Sharks, Rays and Their Relatives. Special Publication of the Ohio Biological Survey. USA: Ohio Biological Survey, pp. 325–416.Google Scholar
Besprozvannykh, VV, Tatonova, YV and Shumenko, PG (2019) Life cycle, morphology of developmental stages of Metorchis ussuriensis sp. nov. (Trematoda: Opisthorchiidae), and phylogenetic relationships with other opisthorchiids. Journal of Zoological Systematics and Evolutionary Research 57, 24–40.CrossRefGoogle Scholar
Bhalerao, GD (1937) Studies on the helminths of India. Trematoda IV. Journal of Helminthology 15, 97–103.CrossRefGoogle Scholar
Bray, RA and Justine, J-L (2006) Prosorhynchus maternus n. sp. (Digenea: Bucephalidae) from the Malabar grouper Epinephelus malabaricus (Perciformes: Serranidae) off New Caledonia. Folia Parasitologica 53, 181–188.CrossRefGoogle Scholar
Brinkmann, A (1957) Fish trematodes from Norwegian Waters II a. The Norwegian species of the Order Aspidogastrea and Digenea (Gasterostomata). University of Bergen Press, pp. 1–29.Google Scholar
Chen, D, Wang, G, Yao, W and Nie, P (2007) Utility of ITS1–5.8S–ITS2 sequences for species discrimination and phylogenetic inference of two closely related bucephalid digeneans (Digenea: Bucephalidae): Dollfustrema vaneyi and Dollfustrema hefeiensis. Parasitology Research 101, 791–800.CrossRefGoogle ScholarPubMed
Cheung, P (1993) Parasitic diseases of elasmobranchs. In Stoskopf, MK (ed.), Fish Medicine. Philadelphia, USA: Saunders Publishing, pp. 782–807.Google Scholar
Corner, RD, Cribb, TH and Cutmore, SC (2020) A new genus of Bucephalidae Poche, 1907 (Trematoda: Digenea) for three new species infecting the yellowtail pike, Sphyraena obtusata Cuvier (Sphyraenidae), from Moreton Bay, Queensland, Australia. Systematic Parasitology 97, 455–476.CrossRefGoogle Scholar
Curran, SS and Overstreet, RM (2009) Rhipidocotyle tridecapapillata n. sp. and Prosorhynchoides potamoensis n. sp. (Digenea: Bucephalidae) from inland fishes in Mississippi, U.S.A. Comparative Parasitology 76, 24–33.CrossRefGoogle Scholar
Cutmore, SC, Nolan, MJ and Cribb, TH (2018) Heterobucephalopsine and prosorhynchine trematodes (Digenea: Bucephalidae) from teleost fishes of Moreton Bay, Queensland, Australia, with the description of two new species. Systematic Parasitology 95, 783–806.CrossRefGoogle ScholarPubMed
Darriba, D, Taboada, GL, Doallo, R and Posada, D (2012) jModeltest2: more models, new heuristics and parallel computing. Nature Methods 9, 772.CrossRefGoogle Scholar
Dawes, E (1947) The Trematode of British Fishes. NY, USA: Palala Press.Google Scholar
Durio, WO and Manter, HW (1968) Some digenetic trematodes of marine fishes of New Caledonia. Part I. Bucephalidae, Monorchiidae, and some smaller families. Proceedings of Helminthological Society, Washington 35, 143–153.Google Scholar
Eckmann, F (1932) Beiträge zur Kenntnis der Trematodenfamilie Bucephalidae. Zeitschrift für Parasitenkunde 5, 94–111.CrossRefGoogle Scholar
Gibson, D, Taskinen, J and Valtonen, TE (1992) Studies on bucephalid digeneans parasitising molluscs and fishes in Finland. II. The description of Rhipidocotyle fennica n. sp. and its discrimination by principal components analysis. Systematic Parasitology 23, 67–79.CrossRefGoogle Scholar
Gupta, SP (1956) A redescription of Bucephalopsis magnum (Verma, 1936) Srivastava, 1938 and Bucephalopsis karvei Bhalerao, 1937. Indian Journal of Helminthology 8, 112–121.Google Scholar
Hammond, MD, Cribb, TH and Bott, NJ (2018) Three new species of Prosorhynchoides (Digenea: Bucephalidae) from Tylosurus gavialoides (Belonidae) in Moreton Bay, Queensland, Australia. Parasitology International 67, 454–464.CrossRefGoogle ScholarPubMed
Hammond, MD, Cribb, TH, Nolan, MJ and Bott, NJ (2020) Two new species of Prosorhynchoides (Digenea: Bucephalidae) from Tylosurus crocodilus (Belonidae) from the great barrier reef and French Polynesia. Parasitology International 75, 102005.CrossRefGoogle ScholarPubMed
Huelsenbeck, JP, Ronquist, F, Nielsen, R and Bollback, JP (2001) Bayesian inference of phylogeny and its impact on evolutionary biology. Science (New York, N.Y.) 294, 2310–2314.CrossRefGoogle ScholarPubMed
Ivanov, VP (1967) New species of the genus Rhipidocotyle - Rhipidocotyle kovalai sp.n. (Nrematoda, Bucephalidae) from acipenserid fish of the Volga River. Zoology Bulletin 5, 81–83.Google Scholar
Kuklin, V, Kuklina, M and Kisova, NE (2012) Species composition and seasonal dynamics of the helminthofauna of the bullroat (Myoxocephalus scorpius, Cottidae) from Kola Bay of the Barents Sea. Russian Journal of Zoology 91, 131–137.Google Scholar
Kumar, S, Stecher, G and Tamura, K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0. Molecular Biology and Evolution 33, 1870–1874.CrossRefGoogle ScholarPubMed
Luton, K, Walker, D and Blair, D (1992) Comparisons of ribosomal internal transcribed spacer from two congeric species of flukes (Platyhelminthes: Trematoda: Digenea). Molecular Biochemical Parasitology 56, 323–328.CrossRefGoogle Scholar
Manter, HW (1940) Digenetic trematodes of fishes from the Galapagos Islands and the neighboring Pacific. Allan Hancock Pacific Expeditions 2, 325–497.Google Scholar
Manter, HW (1963) Studies on digenetic trematodes of fishes of Fiji, IV. Families Haploporidae, Angiodictydae, Monorchiidae and Bucephalidae. Proceedings of Helminthological Society of Washington 30, 224–232.Google Scholar
Maurya, R, Gupta, R and Saxena, AM (2018) Taxonomic redescriptions and a review of the Status of Prosorhynchoides spp. (Digenea: Bucephalidae) infecting some freshwater fishes of India. Comparative Parasitology 85, 159–176.CrossRefGoogle Scholar
McDonald, TE and Margolis, L (1995) Synopsis of the parasites of fishes of Canada: supplement (1978–1993). Canadian special publication of fisheries and aquatic sciences 122, 1–265.Google Scholar
Nagaty, HF (1937) Trematodes of fishes from Red Sea. Part I. Studies on the family Bucephalidae Poche, 1907. Egyptian University Faculty of Medicine 12, 1–172.Google Scholar
Nolan, MJ and Cribb, TH (2010) Two new species of flukes (Digenea: Bucephalidae: Prosorhynchinae) from the Western Moray Gymnothorax woodwardi (Anguilliformes: Muraenidae) from off Western Australia, with replacement of the pre-occupied generic name Folliculovarium Gu & Shen, 1983. Systematic Parasitology 76, 81–92.CrossRefGoogle ScholarPubMed
Nolan, MJ, Curran, SS, Miller, TL, Cutmore, SC, Cantacessi, C and Cribb, TH (2015) Dollfustrema durum n. sp. and Heterobucephalopsis perardua n. sp. (Digenea: Bucephalidae) from the giant moray eel, Gymnothorax javanicus (Bleeker) (Anguilliformes: Muraenidae), and proposal of the Heterobucephalopsinae n. subfam. Parasitology International 64, 559–570.CrossRefGoogle Scholar
Olson, PD, Cribb, TH, Tkach, VV, Bray, RA and Littlewood, DTJ (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33, 733–755.CrossRefGoogle Scholar
Pérez-Ponce de León, G and Hernández-Mena, DI (2019) Testing the higher-level phylogenetic classification of Digenea (Platyhelminthes, Trematoda) based on nuclear rDNA sequences before entering the age of the ‘next-generation’ tree of life. Journal of Helminthology 93, 260–276.CrossRefGoogle ScholarPubMed
Petkevičiūtė, R, Stunžėnas, V and Stanevičiūtė, G (2014) Differentiation of European freshwater bucephalids (Digenea: Bucephalidae) based on karyotypes and DNA sequences. Systematic Parasitology 87, 199–212.CrossRefGoogle ScholarPubMed
Polyansky, YI (1955) Materials on fish parasitology of northern seas of USSR. Fish parasites of Barencevo Sea. Proceedings of Zoological Institute of USSR Academy of Science 20, 5–170.Google Scholar
Posada, D (2003) Using MODELTEST and PAUP* to select a model of nucleotide substitution. Current Protocols in Bioinformatics 6, 6.5.1–6.5.14.Google Scholar
Pratt, I and McCauley, JE (1961) Trematodes of the Pacific Northwest. An Annotated Catalog. OR, USA: Oregon State University Press.Google Scholar
Shvetsova, LS and Pozdnyakov, SE (1999) Class Trematoda. In Pozdnyakov, SE (ed.), Parasitic Flatworms of Far Eastern Seas and Nearest Aquatories of the Pacific Ocean. Vladivostok, Russia: TINRO Publishing House, pp. 23–51.Google Scholar
Skrjabin, KI (1962) Trematodes of Animals and Human. Basis of Trematodology XX. Moscow, USSR: Academy of Science Publishing.Google Scholar
Skrjabina, ES (1974) Helminthes of Sturgeons (Acipenseridae Bonaparte, 1831). Moscow, USSR: Academy of Science Publishing.Google Scholar
Stunžėnas, V, Cryan, JR and Molloy, DP (2004) Comparison of rDNA sequences from colchicine treated and untreated sporocysts of Phyllodistomum folium and Bucephalus polymorphus (Digenea). Parasitology International 53, 223–228.CrossRefGoogle Scholar
Stunžėnas, V, Petkevičiūtė, R, Stanevičiūtė, G and Binkiene, R (2014) Rhipidocotyle fennica (Digenea: Bucephalidae) from Anodonta anatine and pike Esox lucius in Lithuania. Parasitology Research 113, 3881–3883.CrossRefGoogle Scholar
Tamura, K and Nei, M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Molecular Biology and Evolution 10, 512–526.Google ScholarPubMed
Tkach, VV, Littlewood, DTJ, Olson, PD, Kinsella, JM and Swiderski, Z (2003) Molecular phylogenetic analysis of the Microphalloidea Ward, 1901 (Trematoda: Digenea). Systematic Parasitology 56, 1–15.CrossRefGoogle Scholar
Truett, GE (2006) Preparation of genomic DNA from animal tissues. In Kieleczawa, J (ed.), The DNA Book: Protocols and Procedures for the Modern Molecular Biology. MA, USA: Jones & Bartlett Publisher, pp. 33–46.Google Scholar
Urabe, M, Ogawa, K, Nakatsugawa, T, Nakai, K, Tanaka, M and Wang, G (2007) Morphological description of two bucephalid trematodes collected from freshwater fishes in the Uji River, Kyoto, Japan. Parasitology International 56, 269–272.CrossRefGoogle ScholarPubMed
Zhukov, EV (1960) Endoparasitic worms of fishes of the Japan Sea and Southern Kuril shallow waters. Proceedings of Zoological Institute of USSR Academy of Science 28, 3–146.Google Scholar
Supplementary material: Image

Atopkin et al. supplementary material

Figure S1

Download Atopkin et al. supplementary material(Image)
Image 4.8 MB
Supplementary material: File

Atopkin et al. supplementary material

Table S1

Download Atopkin et al. supplementary material(File)
File 17.2 KB