Hostname: page-component-745bb68f8f-d8cs5 Total loading time: 0 Render date: 2025-01-22T05:43:58.280Z Has data issue: false hasContentIssue false
  • English
  • Français

Lifecycle of an introduced Dollfustrema (Bucephalidae) trematode in the Tone River system, Japan

Published online by Cambridge University Press:  20 January 2025

Y. Saito ,
S. Iwata ,
M. Hayashi ,
M. Nitta ,
T. Ishikawa ,
T. Hagiwara ,
H. Ikezawa ,
N. Mano  and
T. Waki Open the ORCID record for T. Waki [Opens in a new window]
Y. Saito
Affiliation:
Toho University, Faculty of Science, 2-2-1 Miyama, Funabashi, Chiba 274-8510, Japan
S. Iwata
Affiliation:
Toho University, Faculty of Science, 2-2-1 Miyama, Funabashi, Chiba 274-8510, Japan
M. Hayashi
Affiliation:
Toho University, Faculty of Science, 2-2-1 Miyama, Funabashi, Chiba 274-8510, Japan
M. Nitta
Affiliation:
Pathology Division, Nansei Field Station, Fisheries Technology Institute, Japan Fisheries Research and Education Agency, 422 1, Nakatsuhamaura, Minami Ise, Watarai, Mie 516 0193, Japan
T. Ishikawa
Affiliation:
College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa, 252-0880, Japan
T. Hagiwara
Affiliation:
Global Environmental Forum, 8th Floor Kuramae Intelligent Bldg., 3-17-3 Kuramae, Taito, Tokyo, 111-0051, Japan
H. Ikezawa
Affiliation:
Ibaraki Nature Museum, 700, Osaki, Bando, Ibaraki 306-0622, Japan
N. Mano
Affiliation:
College of Bioresource Sciences, Nihon University, 1866 Kameino, Fujisawa, Kanagawa, 252-0880, Japan
T. Waki*
Affiliation:
Toho University, Faculty of Science, 2-2-1 Miyama, Funabashi, Chiba 274-8510, Japan
*
Corresponding author: T. Waki; Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

During 2021 through 2023, the golden mussel Limnoperna fortunei and freshwater fishes were sampled from 28 sites in the Tone River system, Japan, and adult trematodes of Dollfustrema were found in the fishes. Molecular and morphological analyses based on 28S rDNA and the ITS1−5.8S−ITS2 region revealed the trematode as ‘Dollfustrema hefeiense’, previously reported in Mainland China and likely introduced to Japan. Given that its scientific name was considered invalid, we re-described the species as Dollfustrema invadens n. sp. Additionally, the DNA-based survey helped clarify the trematode’s life cycle in the river system. A sporocyst and metacercariae were detected in the golden mussel’s visceral mass and in the muscles of two small freshwater fish species, respectively. The channel catfish Ictalurus punctatus harboured mature trematodes in its intestine, and adult trematodes were also found in the muscles of fishes infected with metacercariae, suggesting direct metacercariae development in fish muscle. Furthermore, another introduced bucephalid trematode, Prosorhynchoides ozakii, previously reported in the river system, was detected in the mussels and fishes. Moreover, co-infection of both bucephalid trematodes was observed in certain fishes.

Keywords

Dollfustrema hefeienseDollfustrema invadenslife cyclenomen nudumProsorhynchoides ozakii
Type
Research Paper
Information
Journal of Helminthology , Volume 99 , 2025 , e12
Copyright
© The Author(s), 2025. 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

Anglade, T and Randhawa, HS (2018) Gaining insights into the ecological role of the New Zealand sole (Peltorhamphus novaezeelandiae) through parasites. Journal of Helminthology 92, 187−196.CrossRefGoogle ScholarPubMed
Atopkin, DM, Shedko, MB, Rozhkovan, KV, Nguyen, HV and Besprozvannykh, VV (2022) Rhipidocotyle husi n. sp. and three known species of Bucephalidae Poche, 1907 from the East Asian Region: Morphological and molecular data. Parasitology 149, 774−785.CrossRefGoogle Scholar
Baba, T and Urabe, M (2011) Examination methods for the bucephalids which use Limnoperna fortunei as the first intermediate host. Report of Yahagi River Institute 15, 97−101.Google Scholar
Baba, T and Urabe, M (2015) Parasites of Limnoperna fortunei. In Boltovskoy, D. (ed), fortunei, Limnoperna. Berlin: Springer, 55−65.CrossRefGoogle Scholar
Boltovskoy, D (2015) Distribution and colonization of Limnoperna fortunei: special traits of an odd mussel. In Boltovskoy, D. (ed), Limnoperna fortunei. Berlin: Springer, 301−311.CrossRefGoogle Scholar
Bott, NJ, Miller, TL and Cribb, TH (2013) Bucephalidae (Platyhelminthes: Digenea) of Plectropomus (Serranidae: Epinephelinae) in the tropical Pacific. Parasitology Research 112, 2561−2584.CrossRefGoogle Scholar
Bullard, SA and Overstreet, RM (2008) Digeneans as enemies of fishes. In Eiras, J, Segner, H, Wahil, T and Kapoor, BG (eds), Fish Diseases, vol 2. Boca Raton: CRC Press, 817−976.Google Scholar
Chen, D (2007) Molecular Phylogeny of Sinipercid Fish (Perciformes: Sinipercidae) and Their Two Bucephalid Digeneans (Digenea: Bucephalidae). Wuhan: Institute of Hydrobiology, Chinese Academy of Sciences.Google Scholar
Chen, D, Wang, G, Yao, W and Nie, P (2007) Utility of ITS1–5.8 S–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 Scholar
Choudhary, K, Verma, AK, Swaroop, S and Agrawal, N (2015) A review on the molecular characterization of digenean parasites using molecular markers with special reference to ITS region. Helminthologia, 52, 167−187.CrossRefGoogle 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 ScholarPubMed
Cremonte, F, Gilardoni, C, Pina, S, Rodrigues, P and Ituarte, C (2015) Revision of the family Gymnophallidae Odhner, 1905 (Digenea) based on morphological and molecular data. Parasitology International 64, 202−210.CrossRefGoogle ScholarPubMed
Cremonte, F, Pina, S, Gilardoni, C, Rodrigues, P, Chai, JY and Ituarte, C (2013) A new species of gymnophallid (Digenea) and an amended diagnosis of the genus Gymnophalloides Fujita, 1925. Journal of Parasitology 99, 85−92.CrossRefGoogle Scholar
Curran, SS, Calhoun, DM, Tkach, VV, Warren, MB and Bullard, SA (2022) A new species of Prosorhynchoides Dollfus, 1929 (Digenea: Bucephalidae) infecting chain pickerel, Esox niger Lesueur, 1818 (Perciformes: Esocidae), from the Pascagoula River, Mississippi, USA, with phylogenetic analysis and nucleotide-based elucidation of a three-host life cycle. Comparative Parasitology 89, 82–101.CrossRefGoogle Scholar
de Oliveira, AGL, Menezes, RC, Keidel, L, Mello-Silva, CC and Santos, CP (2022) Morphological, histopathological and molecular assessments of Prosorhynchoides sp. (Digenea: Bucephalidae) in Perna perna (Bivalvia: Mytilidae) mussels sampled off the coast of Rio de Janeiro, southeastern Brazil. Journal of Invertebrate Pathology 195, 107832.CrossRefGoogle Scholar
Froese, R and Pauly, D (Eds) (2024). FishBase version (06/2024). Accessed at www.fishbase.org (accessed on 17 December 2024).Google Scholar
Fukuchi, T, Matsuzawa, Y and Sado, T (2018) First records of Odontobutis potamophila (Japanese Name: Kara-Donko) in Japan as an introduced species. Bulletin of the Biological Society of Chiba 67, 45–49. [in Japanese with English abstract]Google Scholar
Galaktionov, KV, Gonchar, A, Postanogova, D, Miroliubov, A and Bodrov, SY (2024) Parvatrema spp. (Digenea, Gymnophallidae) with parthenogenetic metacercariae: Diversity, distribution and host specificity in the palaearctic. International Journal for Parasitology 54, 333–355.Google ScholarPubMed
Gibson, D (2020) Dollfustrema hefeiense Liu in Zhang et al., 1999. Accessed at https://www.marinespecies.org/aphia.php?p=taxdetails&id=1418120 (4 October 2024).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
Hasegawa, M, Kishino, H and Yano, T (1985) Dating the human-ape split by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160–174.CrossRefGoogle ScholarPubMed
Hayakawa, K, Urabe, M and Taniguchi, Y (2019) New record of bucephalid trematodes from the invasive golden mussel Limnopera fortune in the Yahagi River. Report of Yahagi River Institute 23, 29−30.Google Scholar
Hayashi, M, Sano, Y, Ishikawa, T, Hagiwara, T, Sasaki, M, Nakao, M, Urabe, M and Waki, T (2022) Invasion of fish parasite Prosorhynchoides ozakii (Trematoda: Bucephalidae) into Lake Kasumigaura and surrounding rivers of eastern Japan. Diseases of Aquatic Organisms 152, 47–60.CrossRefGoogle ScholarPubMed
Hoffmann, RW, Körting, W, Fischer-Scherl, T and Schäfer, W (1990) An outbreak of bucephalosis in fish of the Main river. Angewandte Parasitologie 31, 95−99.Google ScholarPubMed
Hosoya, K (2019) Freshwater Fishes of Japan. Tokyo: Yama-Kei Publishers.Google Scholar
International Commission on Zoological Nomenclature (ICZN) (1999) International Code of Zoological Nomenclature, 4th edn. London: International Trust for Zoological Nomenclature, c/o The Natural History Museum.Google Scholar
Ito, K (2007) Spatial distribution of golden mussel, Limnoperna fortunei, in Lake Kasumigaura, Ibaraki Prefecture, Japan. Japanese Journal of Benthology 62, 34−38.CrossRefGoogle Scholar
Japan Wild Research Center (2008) A Photographic Guide to the Invasive Alien Species in Japan. Tokyo: Heibonsha.Google Scholar
Kimura, M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.CrossRefGoogle ScholarPubMed
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: Molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 1547−1549.CrossRefGoogle ScholarPubMed
Li, QK (2019) Bucephalidae Poche, 1907. In Qiu, ZZ, Li, QK and Liu, W (eds), Fauna Sinica Invertebrata Vol. 52 Platyhelminthes Trematoda Dgenea (III). Beijing: Science Press, 91−185. [in Chinese]Google Scholar
Liu, C (1985) Survey of fish trematode in Anhui Province with descriptions of five new species. China Zoological Society, National Parasite Symposium Workshop and Proceedings of the General Meeting 1–14. [in Chinese]Google Scholar
Liu, SF, Peng, WF, Gao, P, Fu, MJ, Wu, HZ, Lu, MK, Gao, JQ and Xiao, J (2010) Digenean parasites of Chinese marine fishes: A list of species, hosts and geographical distribution. Systematic Parasitology 75, 1–52.CrossRefGoogle ScholarPubMed
MacKenzie, K (1991) Massive infection of cod, Gadus morhua L., in the Firth of Clyde with metacercariae of the digenean Bucephaloides gracilescens (Rudolphi, 1819). Bulletin of the European Association of Fish Pathologists 11, 125−126.Google Scholar
Madhavi, R (1974) Digenetic trematodes from marine fishes of Waltair Coast, Bay of Bengal. Family Bucephalidae. Rivista di Parassitologia 5, 189–199.Google Scholar
Magara, Y, Matsui, Y, Goto, Y and Yuasa, A (2001) Invasion of the non-indigenous nuisance mussel, Limnoperna fortunei, into water supply facilities in Japan. Journal of Water Supply: Research and Technology-Aqua 50, 113−124.CrossRefGoogle Scholar
Malsawmtluangi, C and Lalramliana, (2023) A new species of Prosorhynchoides Dollfus, 1929 (Digenea: Bucephalidae) from Xenentodon cancila Hamilton, 1822 in Mizoram, Northeast India. Parasitology International 92, 102690.CrossRefGoogle ScholarPubMed
Moravec, F and Sey, O (1989) Some trematodes of freshwater fishes from North Vietnam with a list of recorded endohelminths by fish hosts. Folia Parasitologica 36, 243–262.Google ScholarPubMed
Masuda, O and Uchiyama, R (2004) Freshwater Mollusks of Japan (2) Freshwater Mollusks from Japan, Including Brackish Water Areas. Tokyo: Pieces Incorporated.Google Scholar
Nakabo, T (2013) Fishes of Japan with Pictorial Keys to the Species, 3rd edn. Hadano: Tokai University Press. (in Japanese)Google Scholar
Nakano, D, Baba, T, Endo, N, Nagayama, S, Fujinaga, A, Uchida, A, Shiragane, A, Urabe, M and Kobayashi, T (2015) Invasion, dispersion, population persistence and ecological impacts of a freshwater mussel (Limnoperna fortunei) in the Honshu Island of Japan. Biological Invasions 17, 743−759.CrossRefGoogle Scholar
Nakao, M, Waki, T, Sasaki, M, Anders, JL, Koga, D and Asakawa, M (2017) Brachylaima ezohelicis sp. nov. (Trematoda: Brachylaimidae) found from the land snail Ezohelix gainesi, with a note of an unidentified Brachylaima species in Hokkaido, Japan. Parasitology International 66, 240−249.CrossRefGoogle ScholarPubMed
NatureServe (2013) Ictalurus punctatus. The IUCN Red List of Threatened Species 2013: e.T202680A18236665. Gland: International Union for Conservation of Nature and Natural Resources. Available at https://www.iucnredlist.org/species/202680/18236665 (accessed 19 July 2024).Google Scholar
Nishimura, T and Habe, T (1987) Contamination of Chinese freshwater bivalves in imported freshwater clams. Chiribotan 18, 110−111.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
Ogawa, K, Nakatsugawa, T and Yasuzaki, M (2004) Heavy metacercarial infections of cyprinid fishes in Uji River. Fisheries Science 70, 132−140.CrossRefGoogle Scholar
Overstreet, RM and Curran, SS (2002) Superfamily Bucephaloidea Poche, 1907. In Gibson, DI, Jones, A and Bray, RA (eds), Keys to the Trematoda 1. London: CAB International and the Natural History Museum, 67−110.CrossRefGoogle Scholar
Ozaki, M and Miyabe, T (2007) The fishing conditions of channel catfish, Ictalurus punctatus, caught in the lower Tone River based on reports from fisherman. Bulletin of the Chiba Prefectural Fisheries Research Center 2, 33−41.Google Scholar
Seno, H and Matsuzawa, Y (2008) Guidebook of Introduced Fish in Japan. Tokyo: Bun-ichi Co. Ltd. (in Japanese)Google Scholar
Shimazu, T (2003) Turbellarians and trematodes of freshwater animals in Japan. In Otsuru, M, Kamegai, S and Hayashi, S (eds), Progress of Medical Parasitology in Japan, 7th edn. Tokyo: Muguro Parasitological Museum, 63–86.Google Scholar
Shimazu, T (2014) Digeneans parasitic in freshwater fishes (Osteichthyes) of Japan. III. Azygiidae and Bucephalidae. Bulletin of the National Museum of Nature and Science. Series A, Zoology 40, 167−190.Google Scholar
Shirakashi, S, Waki, T and Ogawa, K (2020) Bucephalid metacercarial infection in wild larval and juvenile ayu Plecoglossus altivelis. Fish Pathology 54, 93−100.CrossRefGoogle Scholar
Skrjabin, KI and Guschanskaja, LH (1962) Order Bucephalidida (Odening, 1960) Skrjabin et Guschanskaja, 1962. Osnovy Trematodologii 20, 166–559. (In Russian)Google Scholar
Snyder, SD and Tkach, VV (2001) Phylogenetic and biogeographical relationships among some holarctic frog lung flukes (Digenea: Haematoloechidae). Journal of Parasitology 87, 1433–1440.CrossRefGoogle ScholarPubMed
Tkach, VV, Kudlai, O and Kostadinova, A (2016) Molecular phylogeny and systematics of the Echinostomatoidea Looss, 1899 (Platyhelminthes: Digenea). International Journal for Parasitology 46, 171–185.CrossRefGoogle ScholarPubMed
Tominaga, A, Goka, K, Kimura, T and Ito, K (2009) Genetic structure of Japanese introduced populations of the Golden Mussel, Limnoperna fortunei, and the estimation of their range expansion process. Biodiversity 10, 61–66.CrossRefGoogle Scholar
Tseng, S (1930) Sur un gasterostomide immature chez Siniperca. Annales de Parasitologie Humaine et Comparée 8, 554–561.CrossRefGoogle Scholar
Tsuji, S, Doi, H, Hibino, Y, Shibata, N and Watanabe, K (2024) Rapid assessment of invasion front and biological impact of the invasive fish Coreoperca herzi using quantitative eDNA metabarcoding. Biological Invasions 26, 3107–3123.CrossRefGoogle Scholar
Urabe, M, Ogawa, K, Nakatsugawa, T, Imanishi, Y, Kondo, T, Okunishi, T, Kaji, Y and Tanaka, H (2001) Newly recorded gasterostome trematode (Digenea: Bucephalidae) in the Uji River: The life cycle history, distribution and damage to fishes. Bulletin of Kansai Organization for Nature Conservation 23, 13−21.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
Wang, PQ (1985) Note on some species of gasterostome trematodes of fishes mainly from Fujian Province. The Journal of Fujian Teachers University (Natural Science) 4, 73–83. (In Chinese)Google Scholar
Wang, G and Wang, W (1998a) Taxonomy of the family Bucephalidae (Digenea). Acta Hyorobiologica Sinica 22, 89–99.Google Scholar
Wang, G and Wang, W (1998b) Taxonomy and keys to the bucephalid species in China with description of three new species. Acta Hyorobiologica Sinica 22, 100–110.Google Scholar
Wang, G and Wang, W (1998c) Development and differentiation and the taxonomy of organ of bucephalids. Acta Hyorobiologica Sinica 22, 203–207.Google Scholar
Wu, BH, Sun, X and Song, CC (1991) Fauna of Zhejiang, Trematoda. Zhejiang: Zhejiang Science and Technology Publishing House.Google Scholar
Yamaguti, S (1975) A Synoptical Review of Life Histories of Digenetic Trematodes of Vertebrates, with Special Reference to the Morphology of their Larval Forms. Tokyo: Keigaku Publishing Co.Google Scholar
Zhang, JY, Qiu, ZZ and Ding, XJ (1999) Parasites and Parasitic Diseases of Fishes. Beijing: Science Press. (in Chinese)Google Scholar
Supplementary material: File

Saito et al. supplementary material 1

Saito et al. supplementary material
Download Saito et al. supplementary material 1(File)
File 44.5 KB
Supplementary material: File

Saito et al. supplementary material 2

Saito et al. supplementary material
Download Saito et al. supplementary material 2(File)
File 39.4 KB
Supplementary material: File

Saito et al. supplementary material 3

Saito et al. supplementary material
Download Saito et al. supplementary material 3(File)
File 46.6 KB